Insect Biodiversity: Science and Society, Volume 1 [2 ed.] 9781118945537, 1118945530

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Insect Biodiversity

Insect Biodiversity Science and Society Second Edition Volume I

Edited by Robert G. Foottit

Agriculture and Agri-Food Canada Ottawa Ontario Canada

Peter H. Adler

Clemson University Clemson South Carolina USA

This edition first published 2017 © 2017 John Wiley & Sons First edition published 2009 by John Wiley & Sons Ltd All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by law. Advice on how to obtain permission to reuse material from this title is available at http://www.wiley.com/go/permissions. The right of Robert G. Foottit and Peter H. Adler to be identified as the authors of the editorial material in this work has been asserted in accordance with law. Registered Office(s) John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, USA John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK Editorial Office 9600 Garsington Road, Oxford, OX4 2DQ, UK For details of our global editorial offices, customer services, and more information about Wiley products visit us at www. wiley.com. Wiley also publishes its books in a variety of electronic formats and by print-on-demand. Some content that appears in standard print versions of this book may not be available in other formats. Limit of Liability/Disclaimer of Warranty While the publisher and authors have used their best efforts in preparing this work, they make no representations or warranties with respect to the accuracy or completeness of the contents of this work and specifically disclaim all warranties, including without limitation any implied warranties of merchantability or fitness for a particular purpose. No warranty may be created or extended by sales representatives, written sales materials or promotional statements for this work. The fact that an organization, website, or product is referred to in this work as a citation and/or potential source of further information does not mean that the publisher and authors endorse the information or services the organization, website, or product may provide or recommendations it may make. This work is sold with the understanding that the publisher is not engaged in rendering professional services. The advice and strategies contained herein may not be suitable for your situation. You should consult with a specialist where appropriate. Further, readers should be aware that websites listed in this work may have changed or disappeared between when this work was written and when it is read. Neither the publisher nor authors shall be liable for any loss of profit or any other commercial damages, including but not limited to special, incidental, consequential, or other damages. Library of Congress Cataloging-in-Publication Data applied for. ISBN: 9781118945537

Cover Design: Wiley Cover Image: A sampling of beetle diversity in the Palearctic Region. Images by Kirill Makarov Set in 10/12pt, WarnockPro by SPi Global, Chennai, India 10 9 8 7 6 5 4 3 2 1

v

Brief Table of Contents 1 Introduction  1 2

The Importance of Insects  9



Part I  Insect Biodiversity: Regional Examples 45

3

Insect Biodiversity in the Nearctic Region  47

4 Amazonian Rainforests and Their Richness and Abundance of Terrestrial Arthropods on the Edge of Extinction: Abiotic–Biotic Players in the Critical Zone  65 5

Insect Biodiversity in the Afrotropical Region  93

6

Biodiversity of Australasian Insects  111

7

Insect Biodiversity in the Palearctic Region  141



Part II  Insect Biodiversity: Taxon Examples 203

8

Biodiversity of Aquatic Insects  205

9

Biodiversity of Diptera  229

10

Biodiversity of Heteroptera  279

11

Biodiversity of Coleoptera  337

12

Biodiversity of Hymenoptera  419

13

Diversity and Significance of Lepidoptera: A Phylogenetic Perspective  463



Part III  Insect Biodiversity: Tools and Approaches 497

14

The Science of Insect Taxonomy: Prospects and Needs  499

vi

Brief Table of Contents

15

Insect Species – Concepts and Practice  527

16

Molecular Dimensions of Insect Taxonomy in the Genomics Era  547

17

DNA Barcodes and Insect Biodiversity  575

18

Insect Biodiversity Informatics  593

19

Parasitoid Biodiversity and Insect Pest Management  603

20

The Taxonomy of Crop Pests: The Aphids  627

21 Adventive (Non-Native) Insects and the Consequences for Science and Society of Species that Become Invasive  641 22

Biodiversity of Blood-sucking Flies: Implications for Humanity  713

23

Reconciling Ethical and Scientific Issues for Insect Conservation  747

24

Taxonomy and Management of Insect Biodiversity  767

25

Insect Biodiversity – Millions and Millions  783

vii

Detailed Table of Contents List of Contributors  xix Foreword, Second Edition  xxiii Preface, First Edition  xxvii Preface, Second Edition  xxix Acknowledgements  xxxi 1 Introduction  1 Peter H. Adler and Robert G. Foottit

­References  2

5

The Importance of Insects  9 Geoffrey G. E. Scudder

2.1 Diversity  9 2.2 Ecological Role  10 2.3 Effects on Natural Resources, Agriculture, and Human Health  13 2.4 Insects and Advances in Science  14 2.4.1 Biomechanics  15 2.4.2 Genetics  16 2.4.3 Developmental Biology  16 2.4.4 Evolution  18 2.4.5 Physiology  19 2.4.6 Ecology  20 2.4.7 Paleolimnology and Climate Change  22 2.5 Insects and the Public  23 ­References  25

Part I  Insect Biodiversity: Regional Examples 45

3

Insect Biodiversity in the Nearctic Region  47 Hugh V. Danks and Andrew B. T. Smith

3.1 3.2 3.3 3.3.1 3.3.2

Influence of Insect Biodiversity on Society in the Nearctic Region  49 Insect Conservation  50 Species Diversity and the State of Knowledge  53 Assembling the Data  53 Synopsis of Biodiversity  54

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Detailed Table of Contents

3.3.3 State of Knowledge  55 3.4 Variations in Biodiversity  56 3.4.1 Regional Variation  57 3.4.2 Habitats  58 3.5 Conclusions and Needs  58 ­Acknowledgments  60 ­References  60 4

Amazonian Rainforests and Their Richness and Abundance of Terrestrial Arthropods on the Edge of Extinction: Abiotic–Biotic Players in the Critical Zone  65 Terry L. Erwin, Laura S. Zamorano and Christy J. Geraci

4.1 4.2 4.3 4.4 4.5 4.6 4.7 4.8

The Climatic Setting and Critical Zone Establishment  69 Characterization of Typical Lowland Rainforest Composition in the Western Basin  71 Sampling Arthropod Biodiversity in Amazonian Forests  73 Richness of Various Lineages and Guilds  79 General Patterns  79 Morphospecies Richness to Biodiversity  80 Beetles: Life Attributes Have Led to Contemporary Hyperdiversity  83 Summary and Guide to Future Research, or “Taking a Small Step into the Biodiversity Vortex”  85 ­Acknowledgments  86 ­References  86 5

Insect Biodiversity in the Afrotropical Region  93 Clarke H. Scholtz and Mervyn W. Mansell

5.1 5.2 5.3

What Do We Know about Afrotropical Insects?  95 An Information-Management Program  95 The Role of Insects in Ecosystem Processes and as Indicators of Environmental Quality – Dung Beetles as a Case Study  98 5.3.1 Dung Beetles as Indicators of Regional Biodiversity  99 5.3.2 Dung Beetles as Indicators of Habitat Transformation  100 5.4 Africa-Wide Pests and Training Appropriate Taxonomists – Fruit Flies as a Case Study  100 5.4.1 Invasive Species of Concern in Africa  101 5.4.2 African Indigenous Fruit Flies of Economic Importance  102 5.5 Sentinel Groups  103 5.5.1 Neuroptera  103 5.5.2 Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae)  104 5.6 Conclusions  105 ­References  107 6

Biodiversity of Australasian Insects  111 Peter S. Cranston

6.1 Australasia – The Locale  111 6.2 Some Highlights of Australasian Insect Biodiversity  112 6.2.1 The Lord Howe Island Stick Insect  114 6.2.2 Australasian Birdwing Conservation  115

Detailed Table of Contents

6.3 Drowning by Numbers? How Many Insect Species are in Australasia?  116 6.3.1 Australia  116 6.3.2 New Zealand (Aotearoa), Chatham Islands, and Subantarctic Islands  117 6.3.3 New Guinea  118 6.3.4 New Caledonia and the West Pacific  118 6.4 Australasian Insect Biodiversity – Overview and Special Elements  118 6.4.1 Australia  118 6.4.2 New Zealand  121 6.4.3 New Caledonia, New Guinea, and Melanesia  121 6.5 Threatening Processes to Australasian Insect Biodiversity  123 6.5.1 Land Clearance and Alteration  123 6.5.2 Introduced Animals  123 6.5.3 Climate Change  126 6.6 Australasian Biodiversity Conservation  127 6.7 Conclusion  129 ­References  129 7

Insect Biodiversity in the Palearctic Region  141 Boris A. Korotyaev, Alexander S. Konstantinov and Mark G. Volkovitsh

7.1 Preface: Societal Importance of Biodiversity in the Palearctic Region  141 7.2 Introduction  144 7.3 Geographic Position, Climate, and Zonality  144 7.4 General Features of Palearctic Insect Biodiversity  148 7.5 Biodiversity of Some Insect Groups in the Palearctic  153 7.6 Biodiversity of Insect Herbivores  158 7.7 Boundaries and Insect Biodiversity  162 7.8 Local Biodiversity  164 7.9 Insect Biodiversity and Habitats  166 7.10 Insect Biodiversity and the Mountains  169 7.11 Temporal Changes in Insect Biodiversity  171 7.12 Insect Diversity in Major Biogeographical Divisions of the Palearctic  172 7.12.1 Arctic (Circumpolar Tundra) Region  173 7.12.2 Forest Regions  174 7.12.3 Taiga  176 7.12.4 Nemoral European and Stenopean Forests  177 7.12.5 Hesperian and Orthrian Evergreen Forests  179 7.12.6 Steppe (Scythian) Region  180 7.12.7 Desert (Sethian) Region  183 ­Acknowledgments  187 ­References  189

Part II  Insect Biodiversity: Taxon Examples 203

8

Biodiversity of Aquatic Insects  205 John C. Morse

8.1 8.1.1

Overview of Taxa  206 Mayflies (Ephemeroptera)  206

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8.1.2 Dragonflies and Damselflies (Odonata)  207 8.1.3 Stoneflies (Plecoptera)  207 8.1.4 Cockroaches (Blattodea)  208 8.1.5 Grasshoppers and Crickets (Orthoptera)  208 8.1.6 Earwigs (Dermaptera)  208 8.1.7 Lice (Phthiraptera)  208 8.1.8 Bugs (Hemiptera)  208 8.1.9 Wasps (Hymenoptera)  209 8.1.10 Hellgrammites and Alderflies (Megaloptera)  209 8.1.11 Nerve‐winged Insects (Neuroptera)  209 8.1.12 Scorpionflies (Mecoptera)  210 8.1.13 Beetles (Coleoptera)  210 8.1.14 Caddisflies (Trichoptera)  210 8.1.15 Moths (Lepidoptera)  211 8.1.16 Flies (Diptera)  211 8.2 Species Numbers  212 8.3 Societal Benefits and Risks  214 8.3.1 Societal Benefits of Aquatic Insect Diversity in Food Webs  214 8.3.2 Societal Benefits of Aquatic Insect Diversity in Biomonitoring  215 8.3.3 Societal Benefits of Aquatic Insect Diversity in Fishing  217 8.3.4 Societal Benefits of Aquatic Insect Diversity in Control of Noxious Weeds  217 8.3.5 Societal Risks of Aquatic Insects  217 8.4 Biodiversity Concerns for Aquatic Insects  218 8.4.1 Threats to Freshwater Species of Insects  218 8.4.2 Need for Biodiversity Discovery and Description of Aquatic Insects  219 8.4.3 Need to Refine Definitions of Species of Aquatic Insects  219 8.4.4 Need for New Generation of Aquatic Entomologists  219 ­References  220 9

Biodiversity of Diptera  229 Gregory W. Courtney, Thomas Pape, Jeffrey H. Skevington and Bradley J. Sinclair

9.1 Overview of Taxa  239 9.1.1 Lower Diptera  239 9.1.2 Brachycera  241 9.1.2.1 Lower Brachycera  241 9.1.2.2 Empidoidea  242 9.1.2.3 Lower Cyclorrhapha  242 9.1.2.4 Non-calyptrate Schizophora  243 9.1.2.5 Calyptratae  245 9.2 Societal Importance  246 9.2.1 Diptera as Plant Pests (Agriculture, Silviculture, and Floriculture)  246 9.2.2 Medical and Veterinary Importance  247 9.2.2.1 Disease transmission  247 9.2.2.2 Myiasis  248 9.2.3 Invasive Alien Diptera  249 9.2.4 Diptera as a General Nuisance  249

Detailed Table of Contents

9.2.5 Diptera in Biological Control  250 9.2.6 Pollination  251 9.2.7 Other Ecological Services (Scavengers and Decomposers)  252 9.3 Diptera of Forensic, Medicolegal, and Medical Importance  253 9.4 Diptera as Model Organisms and Research Tools  253 9.4.1 Physiology and Genetics  253 9.4.2 Technology  254 9.5 Diptera in Conservation  254 9.5.1 Bioindicators  254 9.5.2 Vanishing Species  255 9.6 Diptera as Part of Our Cultural Legacy  256 References  257 10

Biodiversity of Heteroptera  279 Thomas J. Henry

10.1 Overview of the Heteroptera  280 10.1.1 Euheteroptera  285 10.1.1.1 Infraorder Enicocephalomorpha  285 10.1.1.2 Infraorder Dipsocoromorpha  285 10.1.2 Neoheteroptera  287 10.1.2.1 Infraorder Gerromorpha  287 10.1.3 Panheteroptera  288 10.1.3.1 Infraorder Nepomorpha  288 10.1.3.2 Infraorder Leptopodomorpha  290 10.1.3.3 Infraorder Cimicomorpha  290 10.1.3.4 Infraorder Pentatomomorpha  301 10.2 The Importance of Heteropteran Biodiversity  311 Acknowledgments  313 References  313 11

Biodiversity of Coleoptera  337 Patrice Bouchard, Andrew B. T. Smith, Hume Douglas, Matthew L. Gimmel, Adam J. Brunke and Kojun Kanda

11.1 11.1.1 11.1.2 11.1.3 11.1.3.1 11.1.3.2 11.1.3.3 11.1.3.4 11.1.3.5 11.1.3.6 11.2 11.3 11.3.1

Overview of Extant Taxa  344 Suborders Archostemata and Myxophaga  344 Suborder Adephaga  346 Suborder Polyphaga  347 Series Staphyliniformia  347 Series Scarabaeiformia  349 Series Elateriformia  350 Series Derodontiformia  351 Series Bostrichiformia  352 Series Cucujiformia  352 Overview of Fossil Taxa  357 Societal Benefits and Risks  357 Beetles of Economic Importance  357

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11.3.1.1 Negative Effects of Beetles  357 11.3.1.2 Positive Effects of Beetles  361 11.3.2 Beetles of Cultural Importance  378 11.3.3 Beetles of Medical and Legal Importance  378 11.3.3.1 Medical Entomology  378 11.3.3.2 Forensic Entomology  379 11.3.4 Beetles as Research Tools  380 11.3.4.1 DNA Barcoding of Beetles – A North American Case Study  382 11.4 Threatened Beetles  394 11.5 Conclusions  395 Acknowledgments  395 References  395 12

Biodiversity of Hymenoptera  419 John T. Huber

12.1 Evolution and Higher Classification  422 12.2 Numbers of Species and Individuals  426 12.3 Morphological and Biological Diversity  428 12.4 Importance to Humans  429 12.4.1 Food and Other Products  429 12.4.2 Stings and Bites  430 12.5 Ecological Importance  431 12.6 Conservation  432 12.7 Fossils  432 12.8 Collecting, Preservation, and Study Techniques  433 12.9 Taxonomic Diversity  436 12.9.1 Symphyta  437 12.9.2 Parasitica  437 12.9.2.1 Stephanoidea  437 12.9.2.2 Megalyroidea  437 12.9.2.3 Trigonaloidea  437 12.9.2.4 Mymarommatoidea  437 12.9.2.5 Evanioidea  438 12.9.2.6 Ichneumonoidea  438 12.9.2.7 Cynipoidea  439 12.9.2.8 Proctotrupoidea  439 12.9.2.9 Platygastroidea  439 12.9.2.10 Diaprioidea 439 12.9.2.11 Ceraphronoidea 440 12.9.2.12 Chalcidoidea 440 12.9.3 Aculeata  443 12.9.3.1 Chrysidoidea  443 12.9.3.2 Vespoidea  444 12.9.3.3 Apoidea  446 12.10 Summary and Conclusions  446 ­Acknowledgments  446 References  447

Detailed Table of Contents

13

Diversity and Significance of Lepidoptera: A Phylogenetic Perspective  463 Paul Z. Goldstein

13.1 Relevance of Lepidoptera: Science  464 13.2 Relevance of Lepidoptera: Society  465 13.3 Diversity and Diversification: A Clarification of Numbers and Challenges  466 13.4 State of Lepidopteran Systematics and Phylogenetics  467 13.5 General Overview  468 13.5.1 Primitive Lepidoptera  477 13.5.2 Ditrysia  478 13.5.2.1 Tineoidea  478 13.5.2.2 Gracillarioidea  479 13.5.2.3 Yponomeutoidea  480 13.5.3 Apoditrysia  480 13.5.3.1 Gelechioidea  480 13.5.3.2 Pterophoroidea  481 13.5.3.3 Tortricoidea  481 13.5.3.4 Cossoidea  481 13.5.3.5 Zygaenoidea  482 13.5.4 Obtectomera  482 13.5.5 Macroheterocera  485 13.6 Needs and Challenges for Advancing Lepidopteran Studies  488 ­Acknowledgments  489 ­ References  489

Part III Insect Biodiversity: Tools and Approaches  497

14

The Science of Insect Taxonomy: Prospects and Needs  499 Quentin D. Wheeler and Kelly B. Miller

14.1 The What and Why of Taxonomy  500 14.1.1 Improving Biology’s “General Reference System”  505 14.1.2 Inter‐Generational Ethics  506 14.1.3 Fulfilling Our Intellectual Manifest Destiny  506 14.1.4 Solving Problems  506 14.1.5 Model Organisms  506 14.1.6 Molecular Tools of the Trade  507 14.1.7 Aesthetics  508 14.1.8 Creating the Vocabulary and Syntax of a Language of Biodiversity  508 14.1.9 Mapping the Biosphere  509 14.2 Insect Taxonomy: Missions and “Big Questions”  509 14.3 Insect Taxonomy’s Grand Challenge Questions  510 14.3.1 What Is a Species?  510 14.3.2 What (and How Many) Insect Species Are There?  511 14.3.3 What Is the Phylogeny of Insects?  512 14.3.4 What Are the Histories of Character Transformation in Insects?  512 14.3.5 Where Are Insect Species Distributed?  512 14.3.6 How Have Insect Distributions Changed through Time?  513 14.3.7 How Can Insect Classifications and Names Be Most Predictive and Informative?  513

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14.4 Transforming Insect Taxonomy  513 14.5 Insect Taxonomy: Needs and Priorities  514 14.5.1 Education  514 14.5.2 Planetary‐Scale Projects and Virtual Species Observatories  515 14.5.3 Cybertaxonomy Infrastructure  515 14.5.4 Web‐Based Revisions, Taxon‐Knowledge Communities and Taxon‐Knowledge Banks  516 14.5.5 Collection Development and Growth  517 14.5.6 Integrative Insect Taxonomy  517 14.6 Accelerating Descriptive Taxonomy  517 14.6.1 (1) Inventories to collections  517 14.6.2 (2) Species descriptions  519 14.6.3 (3) Species tests  519 14.6.4 (4) Species tests to databases  520 14.6.5 (5) Collection data  520 14.6.6 (6) Cladistic analysis  520 14.6.7 (7–10) Phylogenetic classifications, names, and identifications  520 14.6.8 (12–16) Inputs  521 14.7 Beware Sirens of Expediency  521 14.8 Conclusions  522 ­ References  522 15

Insect Species – Concepts and Practice  527 Michael F. Claridge

15.1 Early Species Concepts – Linnaeus  528 15.2 Biological Species Concepts  529 15.2.1 Agamospecies  531 15.2.2 Allopatric Forms  531 15.3 Phylogenetic Species Concepts  533 15.4 Species Concepts and Speciation – a Digression?  534 15.5 Insect Species – Practical Problems  535 15.5.1 Parthenogenetic Insects  536 15.5.2 Species, Host Races, and Biotypes  536 15.5.3 Specific Mate Recognition and Sibling Species  538 15.6 Conclusions  540 ­ References  540 16

Molecular Dimensions of Insect Taxonomy in the Genomics Era  547 Amanda Roe, Julian Dupuis and Felix Sperling

16.1 Opportunities in Insect Taxonomy  547 16.1.1 Determination  548 16.1.2 Discovery  549 16.1.3 Delimitation  550 16.1.4 Phylogeny  552 16.2 Genomic Methods  553 16.2.1 Sequencing Technologies  553

Detailed Table of Contents

16.2.2 Genomic Sampling Strategies  554 16.3 General Challenges and Considerations  556 16.3.1 Data Quantity Versus Quality  556 16.3.2 Phylogenetic Considerations  557 16.3.2.1 Locus Selection  557 16.3.2.2 Missing Data  558 16.3.2.3 Gene Tree/Species Tree Incongruence  558 16.3.3 Computational/Logistical/Bioinformatic Bottlenecks  559 16.3.4 The Role of Morphology in a Post-genomic Era  560 16.4 Conclusions  560 References  561 17

DNA Barcodes and Insect Biodiversity  575 John-James Wilson, Kong-Wah Sing, Robin M. Floyd and Paul D. N. Hebert

17.1 17.2 17.3 17.4 17.5 17.6 17.7 17.8

Species Concepts and Recognition  576 DNA Barcoding Methodology  577 Basal Hexapod Orders  578 Archaeognatha (Bristletails) and Zygentoma (Silverfish)  580 Odonata (Dragonflies)  580 Ephemeroptera (Mayflies)  580 Orthoptera (Grasshoppers)  580 Phasmatodea (Walking Sticks), Embioptera (Webspinners), Grylloblattodea (Icecrawlers), and Mantophasmatodea (Gladiators)  581 17.9 Plecoptera (Stoneflies) and Dermaptera (Earwigs)  581 17.10 Mantodea (Mantids)  581 17.11 Blattodea (Cockroaches) and Isoptera (Termites)  581 17.12 Psocoptera (Booklice) and Phthiraptera (Lice)  581 17.13 Thysanoptera (Thrips) and Hemiptera (True Bugs)  582 17.14 Hymenoptera (Wasps)  582 17.15 Strepsiptera (Twisted-wing Parasites)  582 17.16 Coleoptera (Beetles)  582 17.17 Neuroptera (Lacewings), Megaloptera (Dobsonflies), and Raphidioptera (Snakeflies)  583 17.18 Trichoptera (Caddisflies)  583 17.19 Lepidoptera (Butterflies and Moths)  583 17.20 Diptera (Flies)  584 17.21 Siphonaptera (Fleas) and Mecoptera (Scorpionflies)  584 17.22 Conclusions  584 ­Acknowledgments  585 ­References  585

18

Insect Biodiversity Informatics  593 Norman F. Johnson

18.1 Biodiversity Data  594 18.2 Technical Infrastructure  595 18.3 Standards  597

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18.4 Current Status and Impediments to Progress  599 18.5 Prospects  600 ­Acknowledgments  601 ­References  601 19

Parasitoid Biodiversity and Insect Pest Management  603 John Heraty

19.1 What Is a Parasitoid?  604 19.2 Biodiversity and Success of Insect Parasitoids  605 19.2.1 Hymenoptera (Apocrita)  606 19.2.2 Phoridae  608 19.2.3 Tachinidae  608 19.2.4 Other Groups  610 19.2.5 Where Are Parasitoids Most Diverse?  610 19.2.6 Leaf‐mining Parasitoids and Native Landscapes  610 19.2.7 Are Parasitoids More Diverse in Tropical Versus Temperate Climates?  612 19.3 Systematics, Parasitoids, and Pest Management  612 19.3.1 Molecules and Parasitoid Biodiversity  613 19.3.2 Cryptic Species  614 19.3.3 DNA Barcoding and Biodiversity of Parasitoids  616 19.3.4 Can Molecular Markers Be Applied to Understanding Biodiversity?  617 19.4 Summary  617 ­Acknowledgments  618 ­References  618 20

The Taxonomy of Crop Pests: The Aphids  627 Gary L. Miller and Robert G. Foottit

20.1 Historical Background  627 20.2 Economic Importance and Early Taxonomy  628 20.3 Early Aphid Studies – A North American Example  628 20.4 Recognizing Aphid Species  631 20.5 The Focus Becomes Finer  632 20.6 Adventive Aphid Species  633 20.7 Conclusions  634 ­References  634 21

Adventive (Non-Native) Insects and the Consequences for Science and Society of Species that Become Invasive  641 Alfred G. Wheeler, Jr and E. Richard Hoebeke

21.1 Terminology  642 21.2 Distributional Status: Native or Adventive?  643 21.3 Global Transport: Pathways and Vectors  645 21.4 Early History of Adventive Insects in North America  648 21.5 Numbers, Taxonomic Composition, and Geographic Origins of Adventive Insects  649 21.6 Impact of Adventive Insects  653 21.6.1 Beneficial  656

Detailed Table of Contents

21.6.2 Detrimental  657 21.7 Economic Considerations: Agriculture, Forestry, and Horticulture  658 21.7.1 Crop Losses  658 21.7.2 Plant Diseases and Transmission of Pathogens  660 21.8 Implications for Animal and Human Health  661 21.9 Ecological Impacts  663 21.9.1 Ants  665 21.9.2 Bees and Wasps  666 21.9.3 Forest Pests  667 21.10 Biological Control  667 21.11 Biological Invasions and Global Climate Change  670 21.12 Systematics, Biodiversity, and Adventive Species  671 21.13 Concluding Thoughts  671 ­Acknowledgments  674 ­ References  675 22

Biodiversity of Blood-sucking Flies: Implications for Humanity  713 Peter H. Adler

22.1 Numbers and Estimates  714 22.2 Overview of Blood-sucking Flies and Diseases  717 22.2.1 Athericidae  720 22.2.2 Ceratopogonidae  721 22.2.3 Corethrellidae  721 22.2.4 Culicidae  721 22.2.5 Glossinidae  722 22.2.6 Hippoboscidae  723 22.2.7 Muscidae  723 22.2.8 Psychodidae  724 22.2.9 Rhagionidae  724 22.2.10 Simuliidae  724 22.2.11 Tabanidae  725 22.3 Rationale for Biodiversity Studies of Blood-sucking Flies  725 22.4 Biodiversity Exploration  727 22.5 Societal Consequences of Disregarding Biodiversity  729 22.6 Present and Future Concerns  730 22.7 Conclusions  733 ­Acknowledgments  734 ­ References  734 23

Reconciling Ethical and Scientific Issues for Insect Conservation  747 Michael J. Samways

23.1 23.1.1 23.1.2 23.1.3 23.1.4

Valuing Nature  749 Types of Value  749 Sensitive Use of Ecosystem Services  749 Common‐Good Approaches  751 Intrinsic Value and Conservation Action  752

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23.1.5 Reconciling Values  753 23.2 Insects and Ecosystems  755 23.2.1 Interactions and Multiple Effects  755 23.2.2 Insects and Food Webs  757 23.2.3 Importance of Maintaining Landscape Connectance  757 23.3 Two Challenges  758 23.3.1 The Taxonomic Challenge  758 23.3.2 The Challenge of Complementary Surrogates  759 23.4 Synthesizing Deeper Values and Practical Issues  759 23.5 Summary  760 ­Acknowledgments  760 ­ References  760 24

Taxonomy and Management of Insect Biodiversity  767 Ke Chung Kim

24.1 24.2 24.3 24.4 24.5 24.6 24.7

Insect Biodiversity  768 Biodiversity Loss and Humanity  769 Biodiversity and Taxonomy  770 Biodiversity Inventory and Ecology  772 Backyard Biodiversity and Sustainability  774 Taxonomic Bottlenecks in Managing Insect Biodiversity  775 Advancing the Science of Insect Biodiversity  776 References  777

25

Insect Biodiversity – Millions and Millions  783 May Berenbaum

­

­Acknowledgments  ­ References  791

789



Index 1 (Arthropoda-Hierarchic)  793



Index 2 (Arthropoda-Alphabetic)  825



Index 3 (Non-arthropods)  849



Index 4 (General Index Terms)  855

xix

List of Contributors Peter H. Adler

Gregory W. Courtney

Department of Plant and Environmental Sciences Clemson University Clemson South Carolina USA

Department of Entomology Iowa State University Ames Iowa USA

May Berenbaum

Peter S. Cranston

Department of Entomology University of Illinois Urbana Illinois USA

Evolution, Ecology and Genetics Research School of Biology The Australian National University Canberra Australia

Patrice Bouchard

Hugh V. Danks

Canadian National Collection of Insects, Arachnids and Nematodes Agriculture and Agri‐Food Canada Ottawa Ontario Canada

Biological Survey of Canada Canadian Museum of Nature Ottawa Ontario Canada

Adam J. Brunke

Canadian National Collection of Insects, Arachnids and Nematodes Agriculture and Agri‐Food Canada Ottawa Ontario Canada

Canadian National Collection of Insects, Arachnids and Nematodes Agriculture and Agri‐Food Canada Ottawa Ontario Canada Michael F. Claridge

School of Biosciences Cardiff University Cardiff Wales UK

Hume Douglas

Julian Dupuis

Department of Biological Sciences University of Alberta Edmonton Alberta Canada

xx

List of Contributors

Terry L. Erwin

Department of Entomology National Museum of Natural History Smithsonian Institution Washington DC USA Robin M. Floyd

Wellcome Trust/MRC Stem Cell Institute University of Cambridge Cambridge UK and Centre for Biodiversity Genomics Biodiversity Institute of Ontario University of Guelph Guelph Ontario Canada Robert G. Foottit

Canadian National Collection of Insects, Arachnids and Nematodes Agriculture and Agri‐Food Canada Ottawa Ontario Canada Christy J. Geraci

Department of Entomology National Museum of Natural History, Smithsonian Institution Washington DC USA Matthew L. Gimmel

Invertebrate Zoology Santa Barbara Museum of Natural History Santa Barbara California USA

Paul Z. Goldstein

Systematic Entomology Laboratory Plant Science Institute Agriculture Research Service US Department of Agriculture c/o Smithsonian Institution Washington DC USA Paul D. N. Hebert

Centre for Biodiversity Genomics Biodiversity Institute of Ontario University of Guelph Guelph Ontario Canada Thomas J. Henry

Systematic Entomology Laboratory Plant Science Institute Agriculture Research Service US Department of Agriculture c/o Smithsonian Institution Washington DC USA John Heraty

Department of Entomology University of California Riverside California USA E. Richard Hoebeke

Georgia Museum of Natural History and Department of Entomology University of Georgia Athens Georgia USA John T. Huber

Natural Resources Canada Canadian Forestry Service c/o Canadian National Collection of Insects, Arachnids and Nematodes Ottawa Ontario Canada

List of Contributors

Norman F. Johnson

Gary L. Miller

Department of Evolution, Ecology and Organismal Biology and Department of Entomology Ohio State University Columbus Ohio USA

Systematic Entomology Laboratory Plant Science Institute Agricultural Research Service US Department of Agriculture Beltsville Maryland USA

Kojun Kanda

Kelly B. Miller

Department of Biological Sciences Northern Arizona University Flagstaff Arizona USA

Department of Biology University of New Mexico Albuquerque New Mexico USA

Ke Chung Kim

John C. Morse

Frost Entomological Museum Department of Entomology Pennsylvania State University University Park Pennsylvania USA

Department of Plant and Environmental Sciences Clemson University Clemson South Carolina USA

Alexander S. Konstantinov

Natural History Museum of Denmark University of Copenhagen Copenhagen Denmark

Systematic Entomology Laboratory Plant Science Institute Agriculture Research Service US Department of Agriculture c/o Smithsonian Institution Washington DC USA Boris A. Korotyaev

Zoological Institute Russian Academy of Sciences St Petersburg Russia Mervyn W. Mansell

Department of Zoology and Entomology University of Pretoria Pretoria South Africa

Thomas Pape

Amanda Roe

Natural Resources Canada Canadian Forest Service Great Lakes Forestry Centre Sault Ste. Marie Ontario Canada Michael J. Samways

Department of Conservation Ecology and Entomology Stellenbosch University Matieland South Africa

xxi

xxii

List of Contributors

Clarke H. Scholtz

Department of Zoology and Entomology University of Pretoria Pretoria South Africa Geoffrey G. E. Scudder

Department of Zoology University of British Columbia Vancouver British Columbia Canada Bradley J. Sinclair

Canadian National Collection of Insects and Canadian Food Inspection Agency Ottawa Plant Laboratory – Entomology Ottawa Ontario Canada Kong-Wah Sing

State Key Laboratory of Genetic Resources and Evolution Kunming Institute of Zoology Chinese Academy of Sciences Kunming P. R. China and Institute of Biological Sciences University of Malaya Kuala Lumpur Malaysia Jeffrey H. Skevington

Canadian National Collection of Insects, Arachnids and Nematodes Agriculture and Agri‐Food Canada Ottawa Ontario Canada Andrew B. T. Smith

Research Division Canadian Museum of Nature Ottawa Ontario Canada

Felix Sperling

Department of Biological Sciences Biological Sciences Centre University of Alberta Edmonton Alberta Canada Mark G. Volkovitsh

Zoological Institute Russian Academy of Sciences St Petersburg Russia Alfred G. Wheeler, Jr

Department of Plant and Environmental Sciences Clemson University Clemson South Carolina USA Quentin D. Wheeler

College of Environmental Science and Forestry State University of New York Syracuse New York USA John-James Wilson

International College Beijing China Agricultural University Beijing P. R. China and Institute of Biological Sciences University of Malaya Kuala Lumpur Malaysia Laura S. Zamorano

Department of Entomology National Museum of Natural History Smithsonian Institution Washington DC USA

xxiii

Foreword, Second Edition Insects are the most exuberant manifestation of Earth’s many and varied life forms. Their rather simple unifying body plan has become modified and adapted to produce an enormous variety of species, and insects exploit virtually all terres­ trial and freshwater environments on the planet, as well as many brackish waters. However, as a paradox debated extensively a few decades ago, they are largely absent from the seas and oceans. Features such as wings and the complete meta­ morphosis of many species have been cited fre­ quently as fostering this massive diversity. The “success” of the insects can be measured by many parameters: their long‐term persistence and stability of their basic patterns, the variety of higher groups (with almost 30 orders com­ monly recognized) and, as emphasized in this book, the wealth of species and similar entities. Each of these species has its individual biologi­ cal peculiarities, ecological role, distribution, and interactions within the local community. And each may differ in habit and appearance, both from its close relatives and across its range, to reflect local influences and conditions. Every species is thus a mosaic of physical variety and genetic constitution that can lead to taxonomic and ecological ambiguity in interpreting its integrity and the ways in which it may evolve and persist. Entomologists will continue to debate the number of insect “species” that exist and the levels of past and likely future extinctions that edit any such estimate. The difficulties in gain­ ing consensus have two main axes – first, lack of understanding of how these entities may be

recognized and categorized and, second, that many insect groups remain substantially under­ collected and are poorly known. The first of these themes dominates much of this book  – gaining agreement over “what is a species” is difficult and sometimes contentious. Many tax­ onomists hold strong and individualistic views, molded by years of study, of the limits of species and the validity of infraspecific categories such as subspecies and races that in practice can function as “evolutionarily significant units” in their insect group. One widespread trend, often not appreciated fully, is that widespread gener­ alist insect species may not persist as such as their environment changes  –  loss of resources and fragmentation of previously extensive bio­ topes may cause populations to become iso­ lated, and restricted to a limited subset of resources, such as particular host plants, on which they must then depend and specialize. Such situations may beget speciation, perhaps especially among phytophagous insects that display many examples of such localized but obligatory isolation. Populations involved com­ monly show haplotype differences and bio­ logical idiosyncrasies related to their local conditions, but otherwise are not easily separa­ ble. Generalist “species” may commonly com­ prise complexes of cryptic species masquerading as a single entity. Conventional “typological” taxonomists may tend to mirror the more con­ servative “generalist” approach, whereas other constituents (such as many butterfly collectors) may opt to recognize numerous isolated popu­ lations displaying small phenotypic variations as

xxiv

Foreword, Second Edition

distinct (specific or subspecific) taxa. Individual specialists in any large insect group are likely to occupy different positions along the gradient of “lumpers” to “splitters” in how they treat such  variety, and may defend their stance energetically. Biologists and philosophers alike continue to debate the merits of the numerous species con­ cepts, drawing on the reality quoted by one recent commentator that “there are n+1 defini­ tions of ‘species’ in a room of n biologists,” with the most common inference that “a species is whatever a taxonomist says it is.” All recognized categories, however, are dynamic. Any given fig­ ure for insect diversity (as numbers of species) is a working hypothesis, as is each of the contrib­ uting species – so that complete and enduring enumeration is perhaps impossible to achieve. Documenting and cataloging insect biodiver­ sity as a major component of Earth’s life is a natural quest of human inquiry, but is not an end in itself and, importantly, is not synony­ mous with conserving insects or a necessary prerequisite to assuring their well‐being. Despite many ambiguities in projecting the actual num­ bers of insect species, no one would query that there are a lot, and that the various ecological processes that sustain ecosystems depend heav­ ily on insect activity. Indeed, “ecological ser­ vices” such as pollination, recycling of materials, and the economically important activities of predators and parasitoids are signaled increas­ ingly as part of the rationale for insect conserva­ tion because these values can be appreciated easily through direct economic impacts. All these themes are dealt with in this book, cen­ tered on questions related to our ignorance of fundamental matters of “how many are there?” and “how important are they?”, to which the broad answers of “millions” and “massive” may incorporate considerable uncertainty; this uncertainty, however, is reduced by many of the chapters here. In any investigations of insect biodiversity, the role of inventory tends to be emphasized, despite the impracticability of achieving complete enu­ meration. Documenting numbers of species

(however they are delimited or defined) gives us foci for conservation advocacy and is pivotal in helping to elucidate patterns of evolution and distribution. Recognizing and naming species allow us to transfer information, but high proportions of undescribed or unrecognizable species necessitate the use of terms such as “morphospecies” in much ecological interpreta­ tion of diversity. Accompanying archival deposi­ tion of voucher specimens is then needed as the only reliable means through which the consist­ ency of separations can be affirmed and cross‐ survey comparisons validated. Nevertheless, other than in some temperate regions, particu­ larly in the northern hemisphere, many esti­ mates of insect species richness and the naming of the species present are highly incomplete. Much of the tropics, for example, harbors few resident entomologists other than those involved with pressing problems of human welfare, and more basic and sustained documentation almost inevitably depends on assistance from elsewhere. Some insects, of course, have been explored more comprehensively than others, so that selected taxonomic groups (such as butterflies, larger beetles, and dragonflies) and ecological groups (“pests”) have received more attention than many less charismatic or less economically important groups. Indeed, when collecting Psocoptera in parts of the tropics, I have occa­ sionally been asked by local people why I am not collecting birdwing butterflies, stag beetles, or other “popular” (or commercially desirable!) insects, and my responses have done little to change their opinions of my insanity! In short, many gaps in knowledge of insect diversity persist, and seem unlikely to be redressed effectively in the near future, other than by “guesstimates” extrapolating from sometimes rather dubious foundations. How­ ever, sufficient knowledge does exist to endorse the practical need to protect natural habitats from continued despoliation and, as far as practicable, from the effects of climate change. Citations of impressively large numbers of insect species can become valuable advocacy in  helping to conserve areas with largely

Foreword, Second Edition

unheralded wealth of biodiversity. The pres­ ence of unusual lineages of insects, of narrow‐ range endemics, and highly localized radiations and distributional idiosyncrasies (such as iso­ lated populations beyond the main range of the taxon) are all commonplace scenarios, and may in various ways help us to designate priori­ ties  for allocating the limited conservation resources available. Many such examples from selected insect groups are revealed in this book – but evaluating the richness and ecologi­ cal importance of the so‐called meek inheri­ tors, that vast majority of insects that do not intrude notably on human intelligence and wel­ fare, remains a major challenge. Many such taxa receive attention from only a handful of entomologists at any time, and some are essen­ tially “orphaned” for considerable periods. Progress with their documentation is inevitably slow and sporadic. Some hyperdiverse orders and families of insects exhibit daunting com­ plexity of form and biology, as “black hole groups” whose elucidation is among the major challenges that face us. Insect conservation has drawn heavily on issues relevant to biodiversity and appreciation of the vast richness of insects, not only of easily recognizable “species”, but also of the occur­ rence of subspecies and other infraspecific var­ iants, such as significant populations. This more complex dimension of insect biodiversity is receiving considerable attention as new molecular tools (such as DNA analysis) enable us to probe characters in ways undreamed of only a decade or so ago to augment the per­ spective provided by morphological interpreta­ tion, and assess relationships within lineages and their rates of differentiation. Applications of these tools proliferate, sometimes to the extent where small molecular differences treated in isolation may confuse, rather than clarify, relationships implied from more tradi­ tional approaches. The vast arrays of cryptic species gradually being revealed suggest that even our most up‐to‐date estimates of species numbers based on morphological data may be

woefully inadequate. Insect diversity equates to “variety,” but the subtleties of interpopulation variations in genetic constitution and ecologi­ cal performance are difficult to appraise and to categorize formally  –  and perhaps even more difficult to communicate to non‐entomologists whose powers may determine the future of the systems in which those insects participate. Education and communication, based on the soundest available information, are essential components of insect conservation. This book is a significant contribution to this endeavor, through indicating how we may come to inter­ pret and understand insect biodiversity more effectively. In addition to providing a range of opinions and facts on insect richness in a vari­ ety of taxonomic, geographical, and methodo­ logical contexts, it helps to emphasize the scientific and political importance of accurate species recognition. Failure to recognize adven­ tive alien species may have dire economic or ecological consequences, or confusion between biotypes or cryptic species may invalidate expensive management programs for their sup­ pression or conservation. A new generation of skilled insect systema­ tists – whose visions encompass the wider rami­ fications of insect biodiversity, its importance in understanding the natural world, and the accel­ erating impacts of humans upon it – is an urgent need. They enter an exciting and challenging field of endeavor, and the perspectives included in this volume are essential background to their future contributions. The first edition of this book was a foundation and a stimulating work­ ing tool toward that end, and I expect many of the renewed chapters to become key references as we progressively refine and enlarge the bases of our understanding of insects and their activi­ ties in the modern world. Tim New Department of Ecology, Environment and Evolution La Trobe University

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xxvii

Preface, First Edition Insects are the world’s most diverse group of animals, making up more than 58 percent of the known global biodiversity. They inhabit all habitat types and play major roles in the function and stability of terrestrial and aquatic ecosystems. Insects are closely associated with our lives and affect the welfare of humanity in diverse ways. At the same time, large numbers of insect species, including those not known to science, continue to become extinct or extirpated from local habitats worldwide. Our knowledge of insect biodiversity is far from complete; for  example, barely 65 percent of the  North American insect fauna has been described. Only a relatively few species of insects have been studied in depth. We urgently need to explore and describe insect biodiversity and to better understand the biology and ecology of insects if ecosystems are to be managed sustainably and if the effect of global environment change is to be mitigated. The scientific study of insect biodiversity is at a precarious point. Resources for the support of taxonomy are tenuous worldwide. The number of taxonomists is declining and the output of taxonomic research has slowed. Many taxonomists are reaching retirement age and will not be replaced with trained scientists, which will result in a lack of taxonomic expertise for many groups of insects. These trends contrast with an increasing need for taxonomic information and services in our society, particularly for biodiversity assessment, ecosystem management, conservation, sustainable development, management of climate‐change effects, and pest management.

In light of these contrasting trends, the scientific community and its leadership must increase their understanding of the science of insect biodiversity and taxonomy and ensure that policy makers are informed of the importance of biodiversity for a sustainable future for humanity. We have attended and contributed to many scientific meetings and management and policy gatherings where the future, the resource needs, and importance of insect taxonomy and biodiversity have been debated. In fact, discussion of the future of taxonomy is a favorite pastime of taxonomists; there is no shortage of “taxonomic opinion.” Considerable discussion has focused on the daunting task of describing the diversity of insect life and how many undescribed species are out there. However, we felt that there was a need for an up‐to‐date, quantitative assessment of what insect biodiversity entails, and to connect what we know and don’t know about insect biodiversity with its impact on human society. Our approach was to ask authors to develop accounts of biodiversity in certain orders of insects and geographic regions and along selected subject lines. In all categories, we were limited by the availability of willing contributors and their time and resources. Many insect groups, geographic regions, and scientific and societal issues could not be treated in a single volume. It also was apparent to us, sometimes painfully so, that many taxonomists are wildly overcommitted. This situation can be seen as part of the so‐called “taxonomic impediment” – the lack of available taxonomic expertise is

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Preface, First Edition

compounded by an overburdened community of present‐day taxonomists with too much work and perhaps too much unrealistic enthusiasm. In Chapter 1, we introduce the ongoing challenge to document insect biodiversity and develop its services. Chapter 2 provides a comprehensive overview of the importance and value of insects to humans. The next two sections deal with regional treatments and ordinal‐ level accounts of insect biodiversity. These approaches were a serious challenge to the contributors who had to compile information from a wide array of sources or, alternatively, deal with situations in which accurate information simply is insufficient. In Section III, we document some of the tools and approaches to the science of taxonomy and its applications. Perspective is provided on the past, present, and future of the science of insect taxonomy and the all‐important influence of species concepts and their

operational treatment on taxonomic science and insect biodiversity. Contributions on the increasing role of informatics and molecular approaches are provided, areas with ongoing controversy and differences of opinion. These chapters are followed by contributions on the applications of taxonomic science for which biodiversity information is fundamental, including the increasing impact of adventive insects, pest detection and management, human medical concerns, and the management and conservation of biodiversity. The book ends with an historical view of the continuing attempts to document the extent of world insect biodiversity. Robert G. Foottit Ottawa, Ontario Peter H. Adler Clemson, South Carolina

xxix

Preface, Second Edition In the brief eight years since the publication of the first edition of Insect Biodiversity: Science and Society, there have been a number of sub­ stantial changes to entomology and the study of biodiversity. An additional 55,806 new species have been added to the global number of insect species, which now totals 1,060,704. Chapters have been updated or entirely revised to reflect advances in the understanding and knowledge of insect groups, classification, regional diver­ sity, and a wide range of developing method­ ologies. We have seen the rapidly increasing influence on systematics of genomics and next‐ generation sequencing, as well as significant advances in the use of DNA barcoding in insect systematics and in the broader study of insect biodiversity, including the detection of cryptic species. Advances in information science have

been significant, and the influence of the increased capability to gather, manipulate, and analyze biodiversity information is evident in many of the chapters. The compilation of this book highlighted the rapid growth of insect biodiversity and the need for an expanded treatment to address all insect groups, all zoo­ geographic regions of biodiversity, and the scope of systematics approaches for handling biodiversity data. The current book, thus, becomes the first in a two‐volume companion set of Insect Biodiversity: Science and Society. Robert G. Foottit Ottawa, Ontario Peter H. Adler Clemson, South Carolina

xxxi

Acknowledgements We asked external reviewers to give us perspective on each chapter, and we are grateful for their efforts and appreciative of the time they took from their busy schedules. We would like to thank the following individuals who reviewed one or more chapters: P. Bouchard, C. E. Carlton, M. F. Claridge, P. S. Cranston, T. L. Erwin, C. J. Geraci, D. R. Gillespie, P. W. Hall, R. E. Harbach, J. D. Lafontaine, J. D. Lozier, P. G. Mason, H. E. L. Maw, J. C. Morse, L. A. Mound, G. R. Mullen, T. R. New, J. E. O’Hara, V. H. Resh, M. D. Schwartz, G. G. E. Scudder, D. S. Simberloff, A. Smetana, A. B. T. Smith, J. Sóberon, L. Speers, F. A. H. Sperling, I. C. Stocks, M. W. Turnbull, C.

D. von Dohlen, D. L. Wagner, G. Watson, A. G. Wheeler, Jr., Q. D. Wheeler, B. M. Wiegmann, D. K. Yeates, and P. Zwick. We extend our gratitude to Eric Maw for his tremendous efforts in generating the taxonomic indices for both editions. Finally, we acknowledge the encouragement and support, both moral and technical, of the past and present staff at Wiley‐Blackwell, particularly Laura Bell, Ward Cooper, Rosie Hayden, Kelvin Matthews, David McDade, Delia Sandford, Emma Strick­ land, Priya Subbrayal, Bella Talbot, and Sanjith Udayakumar, and we thank Lewis Packwood for his outstanding copy‐ editing of the entire manuscript.

1

1 Introduction Peter H. Adler1 and Robert G. Foottit2 1 2

Department of Plant and Environmental Sciences, Clemson University, Clemson, South Carolina, USA Canadian National Collection of Insects, Arachnids and Nematodes, Agriculture and Agri‐Food Canada, Ottawa, Ontario, Canada

Every so often, a technical term born in the ­biological community enters the popular vocab­ ulary, usually because of its timeliness, political implications, media hype, and euphonious ability to capture the essence of an issue. “Biotechnology,” “human genome,” and “stem cells” are terms as common in public discourse as they are in scien­ tific circles. “Biodiversity” is another example. Introduced in its portmanteau form in the mid‐ 1980s by Warren G. Rosen (Wilson 1988), the term has grown steadily in popularity. In May 2008, the keyword biodiversity generated 17 mil­ lion hits on Google. Eight years later, the same search produced nearly 53 million hits. Not all scientific terms are value‐neutral (Loike 2014). The word biodiversity, however, has remained largely unencumbered by the eth­ ical or political burden carried by terms such as “cloning” and “genetically modified organism.” Although the term biodiversity generally evokes positive sentiment among both the scientific community and the public, its meaning is often subject to individual interpretation. Abraham Lincoln grappled with a similar concern over the word “liberty.” In an 1864 speech, Lincoln opined, “The world has never had a good defini­ tion of the word liberty, and the American peo­ ple, just now, are much in want of one … but in using the same word we do not all mean the same thing” (Simpson 1998). To the layperson,

biodiversity might conjure a forest, a box of beetles, or perhaps the entire fabric of life. ­ Among scientists, the word has been defined, explicitly and implicitly, ad nauseum, producing a range of variants (e.g., Gaston 1996). In its original context, the term biodiversity encom­ passed multiple levels of life (Wilson 1988), and we embrace that perspective. It is “the variety of all forms of life, from genes to species, through to the broad scale of ecosystems” (Faith 2007). Biodiversity, then, is big biology, describing a holistic view of life. The fundamental units of biodiversity – species – serve as focal points for studying the full panoply of life, allowing work­ ers to zoom in and out along a scale from mol­ ecule to ecosystem. The species‐centered view also provides a vital focus for conserving life forms and understanding the causes of declin­ ing biodiversity. Despite disagreements over issues ranging from definitions of biodiversity to phylogenetic approaches, biologists can agree on four major points: (i) the world supports a great number of insects; (ii) we do not know how many species of insects occupy our planet; (iii) the value of insects to humanity is enormous; and (iv) too few specialists exist to inventory the world’s entomofauna and to provide the expertise ­necessary for conserving and sustainably using its resources for societal benefit.

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

2

Insect Biodiversity: Science and Society

By virtue of the sheer numbers of individuals and species, insects, more than any other mac­ roscopic life form, command the attention of biologists. The number of individual insects on Earth at any given moment has been calculated at one quintillion (1018) (Williams 1964), an unimaginably large number on par with the number of copepods in the ocean (Schubel and Butman 1998) and roughly equivalent to the number of sand grains along a few kilometers of beach (Ray 1996). The total number of insect species also bankrupts the mind. Estimates offered over the past four centuries have increased steadily from 10,000 species, pro­ posed by John Ray in 1691 (Berenbaum, this volume), to as many as 80 million (Erwin 2004). The number of described insect species recently broke the 1 million mark – it currently stands at 1,060,704 (Table 1.1), about 100 times the 1691 estimate. Based on a figure of 1.50 million to 1.74 million described eukaryotic species in the world (May 1998, Costello et  al. 2012), insects represent 61–71% of the total. The members of the class Insecta are arranged in 29 orders. Four of these orders – the Coleop­ tera, Diptera, Hymenoptera, and Lepidoptera  – account for more than 80% of all described spe­ cies of living insects. The beetles are far in front, leading each of the next largest orders, the Diptera and Lepidoptera, by a factor of more than 2.4 (Table 1.1). A growing number of world checklists, catalogs, and inventories are available online for various families and orders. Outfitted with search functions, they provide another tool for handling the taxonomic juggernaut of new species and nomenclatural changes. We can fore­ see a global registry of species in the near future that is updated with each new species or syno­ nym, allowing real‐time counts for any taxon (Polaszek et al. 2005). The greatest concentration of insect species lies in tropical areas of the globe. One hectare of Amazonian forest contains more than 100,000 species of arthropods (Erwin 2004), of which roughly 80–85% are insects (May 1998, Stork et al. 2015). This value is more than 90% of the total described species of insects in the entire Nearctic region. Yet, this tropical skew is

based partly on a view of species as structurally distinct from one another. Morphologically similar, if not indistinguishable, species (i.e., cryptic species) typically are not figured into estimates of the number of insect species. If putatively well‐known organisms as large as crocodiles, elephants, giraffes, and whales are composites of multiple cryptic species (Wada et  al. 2003, Brown et  al. 2007, Hekkala et  al. 2011), a leap of faith is not required to realize that smaller earthlings also consist of addi­ tional, hidden species. When long‐recognized nominal species of insects, from black flies to butterflies, are probed more deeply, the repeti­ tive result is an increase, often manyfold, in the number of species (Hebert et  al. 2004, Post et al. 2007). No zoogeographical bias in cryptic species has been detected, after correcting for species richness and study intensity (Pfenninger and Schwenk 2007). We suspect that the dis­ coveries of additional cryptic species will far outstrip the countering effects of synonymizing existing names. The precise number of species, however, is not what we, as a global society, desperately need. Rather, we require a comprehensive, fully accessible library of all volumes (i.e., species), a colossal compendium of names, descriptions, distributions, and biological information that ultimately can be transformed into a directory of services. An example of societal use of plant diversity provides a view of the potential treas­ ures that insects could hold. Of the top 150 pre­ scribed drugs in the United States, about 56% can be linked to discoveries in the natural plant world (Groombridge and Jenkins 2002). The great numbers of insects hold a vast wealth of various behaviors, chemistries, forms, and functions. Furthermore, individual insects offer a package deal: each insect represents an eco­ system of microbial life, teeming with a vast array of species, many of which are host‐, gen­ der‐, and stage‐specific (Tang et  al. 2012). Of the 1 trillion estimated species of microorgan­ isms on Earth (Locey and Lennon 2016), the proportion specific to insects is unknown. The diversity, roles, and potential benefits that lie within the insect–microbiota relationship

1 Introduction

Table 1.1  World totals of described, living species in the 29 orders of the class Insecta, tallied May 2016. Order*

Described species

References†

Microcoryphia

548

Mendes, Vol. II

Zygentoma

594

Mendes, Vol. II

Ephemeroptera

3,436

Morse, this volume

Odonata

5,956

Morse, this volume

Plecoptera

3,562

Morse, this volume

Embiodea

397

Maehr and Hopkins 2016a

Zoraptera

40

Maehr and Hopkins 2016b

Orthoptera

26,107

Song, Vol. II

Phasmatodea

2,976

Bradler, Vol. II

Dermaptera

1,931

Haas, Vol. II

Grylloblattodea

33

Eberhard et al., Vol. II

Mantophasmatodea

19

Eberhard et al., Vol. II

Blattodea

7,637

Cockroaches (5,565) + termites (2,072), Djernaes, Vol. II

Mantodea

2,469

Otte et al. 2016

Psocoptera

5,640

Mockford, Vol. II

Phthiraptera

5,239

Galloway, Vol. II

Thysanoptera

6,102

ThripsWiki 2015

Hemiptera

106,971

Heteroptera (45,254; Henry, this volume) + Auchenorrhyncha (43,024; Bartlett et al., Vol. II) + Sternorrhyncha (18,693; Hardy, Vol II)

Raphidioptera

248

Oswald, Vol. II

Megaloptera

373

Oswald, Vol. II

Neuroptera

5,813

Oswald, Vol. II

Coleoptera

386,755

Bouchard et al., this volume

Strepsiptera

615

Kathirithamby, Vol. II

Hymenoptera

154,067

Huber, this volume

Mecoptera

713

Bicha, Vol. II

Siphonaptera

2,183

Galloway, Vol. II

Diptera

157,971

Courtney et al., this volume

Trichoptera

14,548

Morse, this volume

Lepidoptera

157,761

Goldstein, this volume

Total

1,060,704

* While recognizing the dynamic nature of the higher classification of the hexapods, including the combining of traditional orders (e.g., Misof et al. 2014), we follow the ordinal classification recognized by the authors of the chapters in Volumes I and II of Insect Biodiversity: Science and Society. The three orders of the Entognatha – the Collembola (ca. 8,600 species; Bellinger et al. 1996–2016), Diplura (ca. 800 species; Tree of Life Web Project 1995), and Protura (ca. 750 species; Szeptycki 2007) – are not included here with the Insecta. These three orders would add about 10,150 species, giving a total of roughly 1,071,000 species of Hexapoda in the world. † Species counts are drawn from various sources, typically from online catalogs and checklists, which are summarized by the authors of chapters in the two volumes of Insect Biodiversity: Science and Society, unless otherwise indicated.

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Insect Biodiversity: Science and Society

r­epresent one of the frontiers for biodiversity research (Currie 2015). To harvest the potential benefits of insects, taxonomists and systematists first must reveal Earth’s species and organize them appropriately with collateral information that can be retrieved with ease. In some respects, this is a race against time. Biodiversity science must keep pace with the changing face of the planet, particularly spe­ cies extinctions and reshufflings driven largely by human activities such as commerce, land conversion, and pollution. By 2007, for example, 1321 introduced species had been documented on the Galapagos Islands, of which at least 37% are insects, including some, such as fire ants (Wasmannia auropunctata and Solenopsis geminata) and the parasitic fly Philornis downsi, that have had devastating consequences for the native flora and fauna (Anonymous 2007, Causton and Sevilla 2008). As some species of insects are being redistributed, others are disap­ pearing, particularly in the tropics, although the data are murky. We are forced into an intracta­ ble bind, for we cannot know all that we are los­ ing if we do not know all that we have. We do know, however, that extinction  –  the biodiver­ sity crisis  –  is an inevitable consequence of planetary abuse. Roughly 500 sq km of Brazil’s Amazon rainforest were deforested in 1 month in 2015 (Butler 2016). Using Erwin’s (2004) ­figure of 3 × 1010 individual terrestrial arthro­ pods per hectare of tropical rainforest, we lost habitat for more than one quadrillion arthro­ pods in that one point in space and time. The urgency to inventory the world’s insect fauna is gaining some balance through the cur­ rent revolution in technology, aimed in large measure at the molecular level. Coupled with powerful electronic capabilities, the explosion of biodiversity information can be networked worldwide to facilitate not only communication and information storage and retrieval but also taxonomy itself  –  cybertaxonomy (sensu Wheeler 2007). Efforts to apply bioinformatics on a global scale are well underway (e.g., Maddison et  al. 2007, Barcode of Life Data Systems 2014, Encyclopedia of Life 2016). We

can imagine that in our lifetimes, automated complete‐genome sequencing will be available to identify specimens as routinely as biologists today use identification keys. The futuristic handheld gadget that can read a specimen’s genome and provide immediate identification, with access to all that is known about the organ­ ism (Janzen 2004), is no longer strictly science fiction. Yet, each new technique for revealing and organizing the elements of biodiversity comes with its own set of limitations, some of which we do not yet know. DNA‐sequence readers, for instance, will help little in identify­ ing fossil organisms. An integrated methodol­ ogy, mustering information from molecules to morphology, will continue to prove its merit, although it is the most difficult approach for the individual worker to master. Given the vast number of insect species, however, today’s chal­ lenges are likely to remain the same well beyond the advent of handheld, reveal‐all devices: an unknown number of species, too few experts, and too little appreciation of the value of insect biodiversity. Those who study insect biodiversity do so largely out of a fascination for insects; no eco­ nomic incentive is needed. But for most people, from land developer to subsistence farmer, a per­ sonal, typically economic, reason is required to appreciate the value of insect biodiversity. This value, therefore, must be translated into eco­ nomic gain. Papua New Guinea’s butterfly ranch­ ing program is a spectacular example of the sustainable use of insect ­biodiversity – ­conserving biodiversity while providing economic rewards to villagers (Insect Farming and Trading Agency 2008). Today’s biologists place a great deal of emphasis on discovering species, cataloging them, and inferring their evolutionary relation­ ships. Rightly so. But these activities will not, in themselves, curry favor with the majority. We believe that, now, equal emphasis must be placed on developing the services of insects. We envi­ sion a new era, one of entrepreneurial biodiver­ sity that crosses disciplinary boundaries and links the expertise of insect systematists with that of biotechnologists, chemists, economists, engi­

1 Introduction

neers, marketers, pharmacologists, and others. Only then can we expect to tap the magic well of benefits that can be derived from insects and broadly applied to society while maintaining a sustainable environment and conserving its bio­ diversity. And this enterprise just might reinvig­ orate interest in biodiversity among aspiring professionals and the young. The chapters in this volume are written by biologists who share a passion for insect biodi­ versity. The text moves from a scene‐setting overview of the value of insects through exam­ ples of regional biodiversity, taxon biodiversity, tools and approaches, and management and conservation to a historical view of the quest for the true number of insect species. The case is made throughout these pages that real progress has been achieved in discovering and organiz­ ing insect biodiversity and revealing the myriad ways, positive and negative, that insects influ­ ence human welfare. Although the job remains unfinished, we can be assured that the number of insect‐derived benefits yet to be realized is far greater than the number of species yet to be discovered.

­References Anonymous. 2007. CDF supports Galapagos in danger decision. Galapagos News Fall/Winter 2007: 2. Barcode of Life Data Systems. 2014. http://www. boldsystems.org/ [Accessed 18 June 2016]. Bellinger, P. F., K. A. Christiansen and F. Janssens. 1996–2016. Checklist of the Collembola of the world. http://www.collembola.org [Accessed 18 June 2016]. Brown, D. M., R. A. Brenneman, K.‐P. Koepfli, J. P. Pollinger, B. Milá, N. J. Georgiadis, E. E. Louis, Jr., G. F. Grether, D. K. Jacobs and R. K. Wayne. 2007. Extensive population genetic structure in the giraffe. BMC Biology 5: 57. Butler, R. 2016. Calculating deforestation figures for the Amazon. http://rainforests.mongabay. com/amazon/deforestation_calculations.html [Accessed 1 May 2016].

Causton, C. E. and C. Sevilla. 2008. Latest records of introduced invertebrates in Galapagos and measures to control them. Pp. 142–145. In Galapagos Report 2006–2007, CDF, GNP and INGALA, Puerto Ayora, Galapagos, Ecuador. Costello, M. J., S. Wilson and B. Houlding. 2012. Predicting total global species richness using rates of species description and estimates of taxonomic effort. Systematic Biology 61: 871–883. Currie, C. 2015. NIH Antibiotic Discovery. https://currielab.wisc.edu/research.php?area= NIH+Antibiotic+Discovery [Accessed 18 June 2016]. Encyclopedia of Life. 2016. http://www.eol.org/ [Accessed 3 May 2016]. Erwin, T. L. 2004. The biodiversity question: how many species of terrestrial arthropods are there? Pp. 259–269. In M. D. Lowman and H. B. Rinker (eds). Forest Canopies. 2nd edition. Elsevier Academic Press, Burlington, MA. Faith, D. P. 2007. Biodiversity. In E. N. Zalta (principal ed.). Stanford Encyclopedia of Philosophy. Metaphysics Research Lab, Stanford University, Stanford, CA. http://plato. stanford.edu/entries/biodiversity/ [Accessed 6 May 2016]. Gaston, K. J. (ed). 1996. Biodiversity: a Biology of Numbers and Difference. Blackwell Science, Oxford, UK. 396 pp. Groombridge, B. and M. D. Jenkins. 2002. World Atlas of Biodiversity: Earth’s Living Resources for the 21st Century. University of California Press, Berkeley, CA. 256 pp. Hebert, P. D. N., E. H. Penton, J. M. Burns, D. H. Janzen and W. Hallwachs. 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences USA 101: 14812–14817. Hekkala, E., M. H. Shirley, G. Amato, J. D. Austin, S. Charter, J. Thorbjarnarson, K. A. Vliet, M. L. Houck, R. Desalle and M. J. Blum. 2011. An ancient icon reveals new mysteries: mummy DNA resurrects a cryptic species within the Nile crocodile. Molecular Ecology 20: 4199–4215.

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Insect Farming and Trading Agency. 2008. Papua New Guinea. http://web.archive.org/ web/20120204215326/http://www.ifta.com.pg/ [Accessed 6 May 2016]. Janzen, D. H. 2004. Now is the time. Philosophical Transactions of the Royal Society of London B 359: 731–732. Locey, K. J. and J. T. Lennon. 2016. Scaling laws predict global microbial diversity. Proceedings of the National Academy of Sciences USA 113: 5970–5975. Loike, J. D. 2014. Loaded words. The Scientist 28 (12) http://www.the‐scientist.com/?articles. view/articleNo/41502/title/Loaded‐Words/ [Accessed 18 June 2016]. Maddison, D. R., K.‐S. Schulz and W. P. Maddison. 2007. The Tree of Life Web Project. Pp. 19–40. In Z.‐Q. Zhang and W. A. Shear (eds). Linnaeus Tercentenary: Progress in Invertebrate Taxonomy. Zootaxa 1668: 1–766. Maehr, M. D. and H. Hopkins. 2016a. Embioptera Species File. Version 5.0/5.0. http://Embioptera. SpeciesFile.org [Accessed 18 June 2016]. Maehr, M. D. and H. Hopkins. 2016b. Zoraptera Species File. Version 5.0/5.0. http://Zoraptera. SpeciesFile.org [Accessed 18 June 2016]. May, R. M. 1998. The dimensions of life on Earth. Pp. 30–45. In P. H. Raven (ed). Nature and Human Society: the Quest for a Sustainable World. National Academy Press, Washington, DC. Misof, B., S. Liu, K. Meusemann, R. S. Peters, A. Donath, C. Mayer et al. [95 additional authors]. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346: 763–767. Otte, D., L. Spearman and M. B. D. Stiewe. 2016. Mantodea Species File Online. Version 5.0/5.0. http://Mantodea.SpeciesFile.org [Accessed 18 June 2016]. Pfenninger, M. and K. Schwenk 2007. Cryptic animal species are homogenously distributed among taxa and biogeographical regions. BMC Evolutionary Biology 7: 121. Polaszek, A. D., D. Agosti, M. Alonso‐Zarazaga, G. Beccaloni, P. de P. Bjørn, P. Bouchet, D. J. Brothers, Earl of Cranbrook, N. Evenhuis, H. C.

J. Godfray, N. F. Johnson, F.‐T. Krell, D. Lipscomb, C. H. C. Lyal, G. M. Mace, S. Mawatari, S. E. Miller, A. Minelli, S. Morris, P. K. L. Ng, D. J. Patterson, R. L. Pyle, N. Robinson, L. Rogo, J. Taverne, F. C. Thompson, J. van Tol, Q. D. Wheeler and E. O. Wilson. 2005. A universal register for animal names. Nature 437: 477. Post, R. J., M. Mustapha and A. Krueger. 2007. Taxonomy and inventory of the cytospecies and cytotypes of the Simulium damnosum complex (Diptera: Simuliidae) in relation to onchocerciasis. Tropical Medicine and International Health 12: 1342–1353. Ray, C. C. 1996. Stars and sand. New York Times, 5 March 1996. Schubel, J. R. and A. Butman. 1998. Keeping a finger on the pulse of marine biodiversity: how healthy is it? Pp. 84–103. In P. H. Raven (ed). Nature and Human Society: the Quest for a Sustainable World. National Academy Press, Washington, DC. Simpson, B. D. 1998. Think Anew, Act Anew: Abraham Lincoln on Slavery, Freedom, and Union. Harlan Davidson, Wheeling, IL. 205 pp. Stork, N. E, J. McBroom, C. Gely and A. J. Hamilton. 2015. New approaches, narrow global species estimates for beetles, insects, and terrestrial arthropods. Proceedings of the National Academy of Sciences USA 112: 7519–7523. Szeptycki, A. 2007. Catalogue of the World Protura. Wydawnictwa Instytutu Systematyki i Ewolucji Zwierzat Polskiej Akademii Nauk, Kraków, Poland. 210 pp. Tang, X., P. H. Adler, H. Vogel and L. Ping. 2012. Gender‐specific bacterial composition of black flies (Diptera: Simuliidae). FEMS Microbiology Ecology 80: 659–670. ThripsWiki. 2015. ThripsWiki – providing information on the World’s thrips. http:// thrips.info/wiki/Main_Page [Accessed 21 March 2016]. Tree of Life Web Project. 1995. Diplura. Version 01 January 1995 (temporary). http://tolweb. org/Diplura/8204/1995.01.01 in The Tree of

1 Introduction

Life Web Project, http://tolweb.org/ [Accessed 18 June 2016]. Wada, S., M. Oishi and T. K. Yamada. 2003. A newly discovered species of living baleen whale. Nature 426: 278–281. Wheeler, Q. D. 2007. Invertebrate systematics or spineless taxonomy? Zootaxa 1668: 11–18.

Williams, C. B. 1964. Patterns in the Balance of Nature and Related Problems in Quantitative Biology. Academic Press, London, UK. 324 pp. Wilson, E. O. (ed) 1988. Biodiversity. National Academy of Sciences/Smithsonian Institution. Washington, DC. 538 pp.

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2 The Importance of Insects Geoffrey G. E. Scudder Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada

Insects nurture and protect us, sicken us, kill us. They bring both joy and sorrow. They drive us from fear to hate, then to tolerance. At times they bring us up short to a realization of the way the world really is, and what we have to do to improve it. Their importance to human welfare transcends the grand battles we fight against them to manage them for our own ends. Most of us hate them, but some of us love them. Indeed at times they even inspire us. (McKelvey 1975) Insects are important because of their diversity, ecological role, and influence on agriculture, human health, and natural resources. They have been used in landmark studies in biomechanics, climate change, developmental biology, ecology, evolution, genetics, paleolimnology, and physi­ ology. Because of their many roles, they are familiar to the general public. Their conserva­ tion, however, is a challenge. The goal of this chapter is to document the dominance of insects in the living world and to show how they have been central to many advances in science.

2.1 ­Diversity Considerable debate continues over how many species of insects there are in the world. Estimates

range from 2 million to 80 million (Stork 1993, Erwin 2004). The lower figure is from Hodkinson and Casson (1991). The higher figure of up to 80 million is from Erwin (2004) and, like an earlier estimate of 30 million (Erwin 1982, 1983), is based on numbers obtained from canopy fogging in the tropical forests of the Americas. These high estimates have been questioned, however, because of the assumptions made and the lack of real evidence for vast numbers of undescribed species (Stork 1993). Other methods of estima­ tion have been used by May (1988), Stork and Gaston (1990), and Gaston (1991), and from these other data Stork (1993) concluded that a global total of 5 million–15 million is more rea­ sonable. Gaston (1991) gave a figure of about 5 million, and this estimate was accepted by Grimaldi and Engel (2005), although Hammond (1992) gave an estimate of 12.5 million species. The number of insects described at present is estimated to be 1,060,704 (this volume), in a total biota described to date of 1.4 million to 1.8 million (Stork 1988, 1993; May 1990; Hammond 1992). Grimaldi and Engel (2005), however, suggest that only about 20% of the insects have been named. Most species on Earth are insects. They have invaded every niche, except the oceanic benthic zone (Grimaldi and Engel 2005). Hammond (1992) calculated that arthropods constitute 65% of the total known biodiversity. Grimaldi and Engel (2005) put the figure at about 58%,

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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Insect Biodiversity: Science and Society

and Samways (1993) noted that they constitute 81.3% of described animal species, excluding the Protozoa. Thus, from a modest beginning some 400 mya, insects have become the domi­ nant component of the known diversity on Earth, with 100 million species having ever lived (Grimaldi and Engel 2005). Wheeler (1990) in his “species scape,” pictori­ ally illustrated the current dominance of insects, and Samways (1993) noted that if all insect species on Earth were described, the beetle rep­ resenting the proportion of insect species in the world might have to be drawn up to 10 times larger. Wheeler (1990) used a beetle to depict the arthropods in his species scape because the Coleoptera are the dominant insect order, con­ stituting roughly 40% of the estimated total number of insects (Nielsen and Mound 2000). The dominance of the Coleoptera was said to have led J. B. S. Haldane, when asked what he could infer about the work of the creator, to respond that the creator must have had “an inordinate fondness for beetles,” although there is some doubt about the provenance of this phrase (Fisher 1988). The success of the order Coleoptera is claimed to have been enabled by the rise of flowering plants (Farrell 1998). Although Wheeler’s (1990) species scape is based on the described world biota, a similar species scape could depict most terrestrial com­ munities and ecosystems. Asquith et  al. (1990) calculated the species richness in old‐growth Douglas‐fir forest in Oregon, showing that in the H. J. Andrews Experimental Forest near Eugene, arthropods are dominant, constituting 84.9% of the richness, with vascular plants comprising 11.5%, and vertebrates only 3.6%. Asquith et al. (1990) remarked that in such terrestrial ecosys­ tems, animal diversity is almost synonymous with arthropod diversity. They noted, however, that this vast arthropod diversity is to a large extent an invisible diversity. Yet,  it is the glue that holds diversity together (Janzen 1987). Hexapods not only dominate in number of species, but also in number of individuals. Collembola can occur at densities of 104 to 105 per m2 in most terrestrial ecosystems (Petersen

and Luxton 1982). Such statistics led Fisher (1998) to state that “whether measured in terms of their biomass or their numerical or ecological dominance, insects are a major constituent of terrestrial ecosystems and should be a critical component of conservation research and man­ agement programs.” In terms of biomass and their interactions with other terrestrial organ­ isms, insects are the most important group of  terrestrial animals (Grimaldi and Engel 2005)  –  so important that if all were to disap­ pear, humanity probably could not last more than a few months (Wilson 1992). On land, insects reign (Grimaldi and Engel 2005) and are the chief competitors with humans for the dom­ ination of this planet (Wigglesworth 1976).

2.2 ­Ecological Role Insects create the biological foundation for all terrestrial ecosystems. They cycle nutrients, pollinate plants, disperse seeds, maintain soil structure and fertility, control populations of other organisms, and provide a major food source for other taxa (Majer 1987). Soil insects are essential for the maintenance of healthy and productive agricultural ecosystems (Cock et al. 2012). Almost any depiction of a food web in a terrestrial or freshwater ecosystem will show insects as a key component, although food‐web architectures in these two ecosystems are quite different (Shurin et al. 2005). Insects are of great importance as a source of food for diverse predators (Carpenter 1928). Aquatic insect larvae serve as food for fishes, and many stream fish seem to be limited by the availability or abundance of such prey, at least on a seasonal basis (Richardson 1993). Myriads of adult mayflies are devoured at the season of their emergence by trout (Carpenter 1928), and this phenomenon forms the basis of the fly fish­ ing sport (McCafferty 1981). Insects provide the  major food supply of many lizards. Many amphibians are carnivorous, especially after they reach maturity, and insects form the bulk of their animal food (Brues 1946).

2  The Importance of Insects

Birds of many families take insects as their staple food, at least during part of the year (Carpenter 1928), with martins, swallows, and swifts almost completely dependent on flying insects for survival. For the yellow‐headed blackbird in the Cariboo region of British Columbia, success in rearing young is linked to the emergence of damselflies (Orians 1966). Mammals such as the American anteater, sloth bears, sun bears, and the African and Oriental pangolins are especially tied to ant and termite colonies, and a number of mammalian predators use insects as food. The British badger often digs out wasp nests to feed on the grubs (Carpenter 1928), and in North America, black bears in north‐central Minnesota feed on ants in the spring for quick sources of protein and to obtain essential amino acids and other trace elements that are unavailable in other spring foods (Noyce et al. 1997). Aggregations of the alpine army cutworm moth Euxoa auxiliaris (Grote) are an important, high‐quality, preferred summer and early‐fall food for grizzly bears in Glacier National Park, Montana (White et al. 1998). Insects are an important supplementary source of calories and protein for humans in many regions of the world (Bodenheimer 1951; DeFoliart 1989, 1992, 1999), and some 500 spe­ cies in more than 260 genera and 70 families of insects are known to be consumed (DeFoliart 1989, Groombridge 1992). Insects of most major orders are eaten, but the most widely used species are those that habitually occur in large numbers in one place (such as termites) or that periodically swarm (such as locusts), or large species such as saturniid moth larvae. The seasonal abundance at certain times of the year makes them especially important when other food resources may be lacking (Groombridge 1992). In future, insects may prove especially relevant to food security (Gahukar 2011, Martin 2014). No accurate estimates are available for the total number of insect natural enemies of other insects, but there might be as many, or perhaps more, entomophagous insects as prey or hosts

(DeBach 1974). The habit of feeding on other insects is found in all major insect orders (Clausen 1940). Included here are predators and parasitoids, both of which are involved in natu­ ral and practical control of insects (Koul and Dhaliwal 2003). The control of the cottony‐ cushion scale Icerya purchasi Maskell in California by the predatory vedalia beetle Rodolia cardinalis (Mulsant) imported from Australia established the biological control method in 1888–89 (DeBach 1974, Caltagirone 1981, Caltagirone and Doutt 1989). Conservatively, some 400,000 species of known insects are plant feeders (New 1988). Thus, phytophagous insects make up at least 25% of all living species on earth (Strong et al. 1984). The members of many orders of insects are almost entirely phytophagous (Brues 1946), conspicuous orders being the Hemiptera, Lepidoptera, and Orthoptera. The influence of insects, as plant‐feeding organisms, exceeds that of all other animals (Grimaldi and Engel 2005). Under natural conditions, insects are a prime factor in regulating the abundance of all plants, particularly the flowering plants, as the latter are especially prone to insect attack (Brues 1946). Insects have exploited and profited from their food supply more thoroughly than any other animals (Brues 1946). This ability was harnessed when the moth Cactoblastis cactorum Berg was used to control the prickly pear cactus in Australia in 1920–25 (DeBach 1974). But plants occasionally turn the tables on their predators: among the flowering plants are a number of truly insectivorous forms that belong to several diverse groups (Brues 1946). Food webs involving insects can be quite com­ plex (Elkinton et al. 1996, Liebhold et al. 2000) and relevant to human health in unexpected ways. In oak (Quercus spp.) forests of the east­ ern United States, defoliation by gypsy moths (Lymantria dispar L.) and the risk of Lyme dis­ ease are determined by interactions among acorns, white‐footed mice (Peromyscus leucopus (Rafinesque)), gypsy moths, white‐tailed deer (Odocoileus virginianus Zimmermann), and

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black‐legged ticks (Ixodes scapularis Say) (Jones et  al. 1998). Experimental removal of mice, which eat gypsy moth pupae, demonstrated that moth outbreaks are caused by reductions in mouse density that occur when there are no acorns. Experimental acorn addition increased mouse and tick density and attracted deer, which are key tick hosts. Mice are primarily responsi­ ble for infecting ticks with the Lyme disease agent, the spirochete bacterium Borrelia burgdorferi. Lyme disease risk and human health are thus connected to insects indirectly. Miller (1993) has categorized how insects interact with other organisms as providers, eliminators, and facilitators. Insects serve as providers in communities and ecosystems by serving as food or as hosts for carnivorous plants, parasites, and predatory animals. They also produce byproducts such as honeydew, frass, and cadavers that sustain other species. As eliminators, insects remove waste products and dead organisms (decomposers and detritivores), consume and recycle live plant material (herbi­ vores), and eat other animals (carnivores). Many insect taxa are coprophagous. Scarab beetles in the families Geotrupidae and Scarabaeidae are well‐known dung feeders (Ritcher 1958, Hanski and Cambefort 1991), with adults of some species provisioning larval burrows with balls of dung. The dung‐beetle community in North America is dominated by accidentally or intentionally introduced species, with aphodiines dominant in northern localities and scarabaeines dominant in southern areas (Lobo 2000). Australia has imported copropha­ gous scarabs from South Africa and the Mediterranean region for the control of cattle dung (Waterhouse 1974). African species have also been introduced into North America to improve the yield of pasture land through effec­ tive removal of dung and to limit the prolifera­ tion of flies and nematodes that inhabit the dung (Fincher 1986). Dung beetles in tropical forests also have an important role in secondary seed dispersal because they bury seeds in dung,  protecting them from rodent predators (Shepherd and Chapman 1998).

Leaf‐cutter ants, not large herbivores, are the principal plant feeders in Neotropical forests (Wilson 1987). Insects, not birds or rodents, are the most important consumers in temperate old fields (Odum et al. 1962). Spittlebugs, for exam­ ple, ingest more than do mice or sparrows (Wiegert and Evans 1967). Insect herbivory can affect nutrient cycling through food‐web interactions (Wardle 2002, Weisser and Siemann 2004). Insect herbivores influence competitive interactions in the plant community, affecting plant‐species composi­ tion (Weisser and Siemann 2004). Tree‐infest­ ing insects are capable of changing the composition of forest stands (Swaine 1933), and insects can influence the floristic composition of grasslands (Fox 1957). Soil animals, many of which are insects, ultimately regulate decom­ position and soil function (Moore and Walter 1988) through trophic interactions and bio­ physical mechanisms, which influence micro­ habitat architecture (McGill and Spence 1985). Soil insects are essential for litter breakdown and provide a fast  return of nutrients to pri­ mary producers (Wardle 2002). Ants and ter­ mites are fine‐scale ecosystem engineers (Jones et al. 1994, Lavelle 2002, Hastings et al. 2006). The attine ants are the chief agents for intro­ ducing organic matter into the soil in tropical rainforests (Weber 1966). Overall, termites are perhaps the most impressive decomposers in the insect world (Hartley and Jones 2004) and are major regulators of the dynamics of litter and soil organic matter in many ecosystems (Lavelle 1997). Insects serve as facilitators for interspecific interactions through phoresy, transmission of pathogenic organisms, pollination, seed dispersal and alteration of microhabitat structure by tun­ neling and nesting (Miller 1993). Insect pollina­ tion is an essential contribution to agriculture, on which many crops are dependent (Cock et  al. 2012). The process of insect pollination is thought to be the basis for the evolutionary history of flowering plants, spanning at least 135 million years (Crepet 1979, 1983), although the origin of insect pollination, which is an integrating factor

2  The Importance of Insects

of biocenoses (Vogel and Westerkamp 1991), is  still being debated (Pellmyr 1992, Kato and Inoue 1994). Approximately 85% of angiosperms are polli­ nated by insects (Grimaldi and Engel 2005). Yucca moths (Tegeticula spp.) exhibit an extra­ ordinary adaptation for flower visitation, and yuccas depend on these insects for pollination (Frost 1959, Aker and Udovic 1981, Addicott et al. 1990, Powell 1992). Similarly, figs and chal­ cid wasps have a remarkable association (Frost 1959, Baker 1961, Galil 1977, Janzen 1979, Wiebes 1979). Orchid species have developed floral color, form, and fragrance that allow these flowers to interject themselves into the life cycle of their pollinators to accomplish their fertiliza­ tion (Dodson 1975).

2.3 ­Effects on Natural Resources, Agriculture, and Human Health Less than 1–2% of phytophagous insects that are potential pests ever achieve the status of  being even minor pests (DeBach 1974). However, those that become major pests can have a devastating effect. Insect defoliators have major effects on the growth (Mott et  al. 1957) and survival of forest trees (Morris 1951), and can alter forest‐­ecosystem function (Naiman 1988, Carson et  al. 2004). The native mountain pine beetle Dendroctonus ponderosae Hopkins, the primary host of which is  lodgepole pine (Pinus contorta var. latifolia Engel), has devastated pine stands in British Columbia over the past two decades. By 2002, the current pine‐beetle outbreak, which began during the 1990s, covered 4.5 million hectares (Taylor and Carroll 2004), and by 2006 it cov­ ered more than 8.7 million hectares. It still has not reached its peak in south‐central parts of the province and could well spread across the whole of the boreal forest and sweep across Canada. As it does so, it also could negatively affect the stability of wildlife populations (Martin et al. 2006). In such circumstances, the beetle acts as a keystone species, causing strong

top‐down effects on the community (Carson et al. 2004). Few would argue that one of the world’s most destructive insects is the brown planthopper Nilaparvata lugens (Stål) (Nault 1994). Each year, it causes more than US$1.23 billion in losses to rice in Southeast Asia (Herdt 1987). These losses are caused by damage from feeding injury and by plant viruses transmitted by this planthopper (Nault 1994). Desert locusts are well known for their devas­ tating effect on crops in Africa (Baron 1972), and almost any book on applied entomology will list innumerable pests. Pfadt (1962), for example, considers pests of corn, cotton, fruits, households, legumes, livestock, poultry, small grains, stored products, and vegetable crops. Most major insect pests in agriculture are non‐native species that have been introduced into a new ecosystem, usually without their nat­ ural biological control agents (Pimentel 2002). Introduced insects in Australia are responsible for as much as $5 billion–8 billion in annual damage and control costs (Pimentel 2002). Transmission of plant‐disease agents by insects has been known for a long time (Leach 1940). Insect vectors of disease agents have probably affected humans more than have any other eukaryotic animals (Grimaldi and Engel 2005). Their epidemics have profoundly shaped human culture, military campaigns, and history (Zinsser 1934, McNeill 1976, R. K. D. Peterson 1995). Enormous effort has been made over the years to control insect‐borne diseases (Busvine 1993). Tens of millions of people throughout the world died in historical times as a result of just  six major insect‐borne diseases: epidemic typhus (a spirochete carried by Pediculus lice), Chagas disease (a trypanosome carried by tri­ atomine bugs), plague (a bacterium carried by Pulex and Xenopsylla fleas), sleeping sickness (a  trypanosome carried by tsetse), malaria (Plasmodium spp. carried by Anopheles mos­ quitoes), and yellow fever (a virus carried by Aedes mosquitoes) (Grimaldi and Engel 2005). Mosquitoes also are involved in the transmis­ sion of West Nile virus, now a major concern in

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North America (Enserink 2000). From the 15th century to the present, successive waves of mos­ quito invasions have been facilitated by world­ wide transport (Lounibos 2002). The story of the struggle in Africa to over­ come tsetse and the disease agents they trans­ mit is one of the major epics in human history (McKelvey 1973). Worldwide, arthropod‐borne pathogens still take an enormous toll on human mortality, morbidity, and loss of productivity (Aultman et al. 2000). Of all the ills that affect humankind, few have taken a higher toll than malaria (Alvardo and Bruce‐Chwatt 1962). More than 400 million people fall ill each year with malaria, and 1  million–3 million die, mostly children younger than 5 years old, and most of them in Africa (Marshall 2000). Evidence seems to indicate that the toll has been increasing in recent years (Marshall 2000). As a result, malaria still casts a deadly shadow over Africa (Miller and Greenwood 2002). Certain insects can be beneficial. Losey and  Vaughan (2006) estimate that the annual value of ecological services provided by insects in the United States is at least $57 billion. Insect pollination, for example, is of great eco­ nomic value in the fruit‐growing industry, the greenhouse industry, and in the growing of forage crops such as alfalfa (Free 1993, Proctor et al. 1996). The annual benefit of honey bees to US  agricultural consumers is on the order of $1.6 billion–8.3 billion (Southwick and Southwick 1992). Ample evidence shows, however, that pollina­ tor diversity and crop pollination services are at risk as a result of pesticide use; habitat altera­ tion, fragmentation, and destruction; introduc­ tion of alien species; and diseases (Johansen 1977, Kevan et  al. 1990, Royce and Rossignol 1990, Watanabe 1994, Raloff 1996, Kearns and Inouye 1997, Kearns et  al. 1998, Kremen et  al. 2002, Steffan‐Dewenter et al. 2005). The innu­ merable insect predators and parasites are invaluable for natural biological control. Natural pest‐control services maintain the stability of agricultural systems worldwide and are crucial

for food security, rural household incomes, and national incomes in many countries (Naylor and Ehrlich 1997). Enough cases of highly effective natural biological control have been studied to indicate that 99% or more of potential pest insects are under such natural control (DeBach 1974). Natural pest controls represent an impor­ tant ecosystem service (Cock et al. 2012), with an annual replacement value of an estimated $54 billion (Naylor and Ehrlich 1997). The first and perhaps the most spectacular success of applied biological control was the introduction of the vedalia beetle from Australia into California in 1888 to control the cottony‐cushion scale (Hagen and Franz 1973, Caltagirone and Doutt 1989). This outstanding success has led to many introductions of para­ sitoids and predaceous insects for biological control and the improvement of biological con­ trol techniques (Huffaker 1971, DeBach 1974, Caltagirone 1981, DeBach and Rosen 1991, van Driesche and Bellows 1996), although after many reckless insect importations, biological control is no longer recognized as a panacea (Hagen and Franz 1973); it even can pose threats to non‐target species (Samways 1997; Louda et  al. 1997, 2003; Boettner et  al. 2000; Follett and Duan 2000; Thomas et al. 2013) and elevate threats to human health (Pearson and Callaway 2006). Biological control, therefore, can be a double‐edged sword (Louda and Stiling 2004).

2.4 ­Insects and Advances in Science The natural sciences have found insects to be ideal for research (Wigglesworth 1976). Their study has produced major advances in our understanding of biomechanics, climate change, developmental biology, ecology, evolution, genetics, paleolimnology, and physiology. A few examples suffice to illustrate how the study of insects has advanced these areas of science, especially where insects “have done it first” (Akre et al. 1992).

2  The Importance of Insects

2.4.1 Biomechanics

Insects have evolved unique features in the ani­ mal world that are a surprise to experts in bio­ mechanics and bioengineering because many are recent inventions of humans. For example, insect cuticle, with its plywood‐like structure, is a laminated composite material. Such materials are now well known in engineering and are used where high strength and stiffness to weight ratios are required (Barth 1973). Manufactured plywood is fairly new, but insect cuticle has been around for some 400 million years (Grimaldi and Engel 2005). Furthermore, the insect exoskeleton contains areas of resilin protein, which tend to be associated with the locomotory (e.g., flight) system (Weis‐Fogh 1960). Resilin has been called “the most perfect rubber known” (Neville 1975) thanks to its high compliance (it deforms easily) and low tensile strength (Bennet‐Clark 1976). Although the origin of insect flight is still debated (Wootton and Ellington 1991), insects were certainly the first animals to evolve wings, evidently during the Late Devonian or Early Carboniferous (Grimaldi and Engel 2005). However, if Rhyniognatha hirsti Tillyard from the Early Devonian (Pragian) chert of the Old Red Sandstone of Scotland is a pterygote insect, wings might have evolved 80 my earlier (Engel and Grimaldi 2004). Thus, insect wings and flight capacity developed about 90 my before the earliest winged vertebrates (Grimaldi and Engel 2005), or perhaps even 170 my earlier (Engel and Grimaldi 2004). Not only did insects evolve active flight first, they remain unsurpassed in many aspects of aerodynamic performance and maneuverability (Dickinson et al. 1999). Although nobody knows how the smallest insects fly (Nachtigall 1989), the aerodynamic properties and design of cer­ tain insect wings have been perfected to such an extent that they are superior to the design of human‐made fixed‐wing aircraft in a number of respects (Nachtigall 1974). The structure of these organs and the way they are used are the envy of variable‐wing plane designers (Scudder

1976). Insect wings typically produce two to three times more lift than can be accounted for by conventional aerodynamics (Ellington 1999). Most insects rely on a leading‐edge vortex cre­ ated by dynamic stall during the downstroke to provide high lift forces (Ellington et  al. 1996, Ellington 1999). The wings of archaic Odonatoidea from the Middle Carboniferous, about 320 mya, show features analogous to the “smart” mechanics of modern dragonflies (Wootton et  al. 1998). These mechanisms act automatically in flight to depress the trailing edge of the wing and facilitate wing twisting in response to aerody­ namic loading, and suggest that these early insects were already becoming adapted for high‐­performance flight in association with a predatory habit. Modern dragonflies use “unsteady aerody­ namics,” a mode of flight not previously recog­ nized as feasible (Somps and Luttges 1985). In such flight, the forewings generate a small vor­ tex, which the hindwing can then capture to provide added lift. Hovering insects do not rely on quasi‐steady aerodynamics, but use rota­ tional lift mechanisms, involving concentrated vortex shedding from the leading edge during wing rotation (Ellington 1984). These discover­ ies have opened new possibilities in flight tech­ nology and have applications in designing not only planes but also features of turbine blades and racing cars. Collaborative research between engineers and specialists in insect flight is resulting in the development of micro‐air‐­ vehicles that are capable of industrial fault loca­ tion in enclosed situations (Wootton 2000). Furthermore, the microstructure of the lan­ terns of fireflies of the genus Photuris has pro­ vided insight into the optimum design of existing light‐emitting diodes (Bay et al. 2013). This has resulted in the production of more effi­ cient LED lights. Although many types of walking machines exist, engineers have not yet determined how best to make these machines handle unfamiliar situations. However, biologists with a detailed knowledge of insect walking and its control

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have linked with computer scientists to develop better robot designs, using computer models of insect locomotion (Pennisi 1991). 2.4.2 Genetics

Drosophila melanogaster Meigen, a tramp species of fruit fly, arguably is the best known eukaryotic organism (Grimaldi and Engel 2005). The Columbia Group of geneticists (T. H. Morgan, C. B. Bridges, H. J. Müller, and A. H. Sturtevant) helped to launch the field of modern genetics with their pioneering use of D. melanogaster in the “Fly Room” (Sturtevant 1965, Roberts 2006). They used the species to clarify or discover fundamental concepts such as crossing over, linkage, mutation, sex‐linked inheritance, and the linear arrangement of genes on chromosomes (DeSalle and Grimaldi 1991). Almost all significant basic concepts in transmission genetics were either first devel­ oped by Drosophila workers or conspicuously verified by them (Brown 1973). Drosophila played a major part in the investi­ gation of the nature and action of genes (Glass 1957), and the role of genes in the determina­ tion of sex was first deduced from the study of sex‐linked inheritance in the Lepidoptera by Doncaster and Raynor (1906). The laws of heredity, as worked out with these insects, pro­ vide one of the main pillars supporting the sci­ ence of genetics (Wigglesworth 1976). During the era of what Haldane (1932, 1964) called “bean‐bag genetics” came the demonstra­ tion that every feature governing the life of an organism, if inherited, was under genetic con­ trol. Such research has made Drosophila melanogaster a favorite species in laboratory research from cell biology to behavior, ecology, evolu­ tion, and physiology (Grimaldi and Engel 2005). This species was the preeminent model organ­ ism from 1970 to 1980 (Roberts 2006). Most of the early data on the genetic characteristics of central and marginal popula­ tions came from studies of chromosomal poly­ morphisms in various species of Drosophila (Brussard 1984). The genetic constitution of

colonizing individuals used to establish insect populations for biological control is relevant to their success, and depends on whether pop­ ulations of colonizers are drawn from the center or periphery of their range (Force 1967, Remington 1968). Research with house flies (Bryant et al. 1986) demonstrated the possibility of increased genetic variance after population bottlenecks (Carson 1990). Until this research, population bottle­ necks were usually considered to reduce genetic variance (Nei et al. 1975). After the discovery of transposable elements in corn (Zea mays L.) by Barbara McClintock in  the 1940s (Sherratt 1995), research on Drosophila first demonstrated the presence of transposable elements in animals (Cohen and Shapiro 1980). Of all the eukaryotic transposa­ ble elements, the most heavily exploited has been the Drosophila P element (Kaiser et  al. 1995). Use of transposable elements for insect pest control is now being investigated (Grigliatti et  al. 2007) in an effort to add to the current techniques of genetic control of insect pests (Davidson 1974). 2.4.3  Developmental Biology

Insects probably contain the greatest variety of developmental forms of any class of organisms (Kause 1960, Boswell and Mahowald 1985, Sander et  al. 1985). Eggs of insects are either indeterminate or determinate (Seidel 1924), and differ in their mechanism of pattern formations (Sander et al. 1985). Some of the earliest research on fate maps in determinate eggs were done by either small local mechanical or ultraviolet‐ radiation ablation experiments (Schubiger and Newman 1982) or by analyzing genetic mosaics in insects (Janning 1978). Determination, which is the process that results in cells being committed to specific developmental fates, has been well studied in holometabolous insects in their imaginal discs, first described by Lyonet (1762) in Lepidoptera, and later recognized to have developmental significance by Weismann (1864). Largely

2  The Importance of Insects

through the pioneering efforts of such scien­ tists as D. Bodenstein, B. Ephrussi, E. Hadorn, and C.  Stern, the developmental biology of imaginal discs has become an active field of investigation and a unique and favorable sys­ tem for the study of numerous problems in metazoan development (Oberlander 1985). Among these problems are pattern formation, positional information, transdetermination, and programmed cell death. In insects, morphogenesis gradients are pre­ sent in the embryo, where they influence the polarity and quality of body segments (Sander et al. 1985) and their appendages. The elucida­ tion of the segmental polarity genes, which control the primary segmental pattern in Drosophila, made a significant contribution to the development of the polar coordinate model of animal development (Bryant 1993, Roberts 2006). Homeosis, defined by Bateson (1894) as the replacement of the body part of one segment with the homologous body part of another seg­ ment, was pioneered by Bateson, with several examples drawn from insects. As with many other phenomena in insect development, home­ otic mutants have been studied most extensively in D. melanogaster (Gehring and Nöthiger 1973, Ouweneel 1975). Rapid advances have been made in under­ standing the genetic basis of development and pattern formation in animals (Patel 1994) as a  result of pioneer studies in Drosophila. Homologous genes are now known to serve similar developmental functions in a number of diverse organisms, with conservation of the homeobox sequence in evolution (Patel 1994). The homeobox genes, first identified by home­ otic mutations in Drosophila (Scott and Weiner 1984), act as markers of position, defining dif­ ferent fates along the anterior–posterior axis of animal embryos (Akam 1995). They are, thus, important regulators of embryonic develop­ ment, and have provided key indicators of the mysteries of evolution (Marx 1992). They indi­ cate that complex organizational changes, both functional and structural, can arise from few

genetic events (Hunkapiller et  al. 1982). The realization that nothing is lost in evolution, but instead is just not developed, has been sup­ ported by studies in D. melanogaster on the seg­ mental organization of the tail region in insects (Jürgens 1987). Although the strongest evidence for an intrin­ sic death program in animal cells originally came from genetic studies of the nematode Caenorhabditis elegans (Maupas) (Horvitz et al. 1982), research on Drosophila has substantially extended our understanding of how pro­ grammed cell death in development is executed and regulated (Raff 1994, White et  al. 1994). Defect mutants and homeotic mutants of Drosophila have been examined to determine to what extent morphological changes have been initiated by cell death and been brought about by subsequent modification (Lockshin 1985). Transdetermination, a phenomenon unique to insects and first documented by Hadorn (1968) with imaginal discs of Drosophila cul­ tured in vivo, reveals that there must be an underlying regulatory system for switching between alternative states of development (Shearn 1985). Further research with insects on this topic could provide a major step toward understanding the genetic programming of development. Sir John Lubbock (Lord Avebury), the famous banker, practical sociologist, and ama­ teur entomologist, pointed out (Lubbock 1873) the significance of metamorphosis in insects and paved the way for our current understand­ ing, emphasizing the difference between devel­ opment and adaptive changes (Wigglesworth 1976). We now realize that metamorphosis in holometabolous insects serves to free certain ectodermal cells from the task of forming functional cuticle, so that they can prepare for the formation of the specialized structures of  the future adult (Wigglesworth 1985). Epidermal cells, thus, have a unique triple capacity to form larval, pupal, or adult charac­ ters, and metamorphosis is no longer regarded as a reversion to embryonic development (Wigglesworth 1985).

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2.4.4 Evolution

Charles Darwin was fond of insects and referred to them extensively in his work and ideas on natural selection (Smith 1987). Insects, specifi­ cally the moth Biston betularia (L.), finally pro­ vided what Kettlewell (1959) called Darwin’s missing evidence, namely natural selection in action in the form of industrial melanism (Kettlewell 1961, 1973). The study of speciation was brought into the modern age and onto a firmer, more genetic basis by drosophilists during the 1930s and 1940s (Mallet 2006). A major event was the discovery of two populations of Drosophila that could not be differentiated by systematists, but which did not interbreed with each other, although they were fully fertile within each population (Ross 1973). Dobzhansky’s (1937) reproductive isola­ tion species concept, later incorporated into Mayr’s (1942) biological species concept, was based in large part on the discovery of pairs of sibling species in Drosophila. Sibling species (cryptic species) have since been discovered in most other groups of insects, such as black flies (Post et  al. 2007), butterflies (Bertrand et  al. 2014), and green lacewings (Bickham 1983), and provide fertile ground for speciation models. Sibling species, which are genetically close and almost morphologically identical, typically show strong reproductive isolation in the form of hybrid sterility, hybrid inviability, and assor­ tative mating (Mallet 2006). Recent advances in molecular and genetic understanding of Drosophila speciation genes have begun to open up our understanding of the genetic basis of hybrid inviability and sterility (Mallet 2006). The notion that prezygotic reproductive iso­ lation can be reinforced when allopatric taxa become sympatric, and that no single isolating mechanism is the “stuff of speciation,” was the result of studies on Drosophila (Coyne and Orr 1989). Drosophila research also provides no evidence for extensive reorganization of gene pools in speciation (Throckmorton 1977), and research on insects, together with studies in developmental and molecular biology, now

suggests that neither the genome nor the gene pool of species is highly coadapted (Bush and Howard 1986). Insects have been instrumental in demon­ strating that sympatric speciation can occur (Scudder 1974), with host–plant separation (Bush 1969, Huettel and Bush 1972), habitat specialization (Rice 1987, Rice and Salt 1988), or seasonal diversification (Tauber and Tauber 1981) often being important components. The power of disruptive selection was first investi­ gated in Drosophila (Thoday 1972), and the analysis of hybrid zones (Barton and Hewitt 1985) has been facilitated by studies of insects (Hewitt 1988, 1990). Allochronic speciation has been documented in crickets (Alexander 1968), and stasipatric speciation has been claimed from the study of morabine grasshoppers (Key 1968), but these speciation examples pose problems with parapatry and species interactions (Bull 1991). Founder‐flush and transilience theories of spe­ ciation were inspired largely by the endemic nature of Hawaiian Drosophila species (Carson 1970, 1975; Templeton 1981; Carson and Templeton 1984), and the molecular drive model of species evolution (Dover 1982) was derived from research on Drosophila genetics. Chromosomal mechanisms of speciation have been documented best in insects (White 1973, 1978), and insects are represented in examples of gynogenesis (Moore et  al. 1956, Sanderson 1960), a form of asexual reproduction that is similar to parthenogenesis but that requires stimulation by sperm, without contributing genetic material to the offspring. Studies of insects have been behind the con­ clusion that many different kinds of species exist as a result of different kinds of speciation processes (Scudder 1974, Foottit 1997). They provide a case for pluralism in species concepts (Mishler and Donoghue 1982). For evolution above the species level, or what Simpson (1953) called the major features of evo­ lution, insects have not made a major contribu­ tion recently. Early work by the famous Dutch naturalist Jan Swammerdam in about 1669,

2  The Importance of Insects

however, first gave a physiological description of insect metamorphosis, and a concept of “preformation” was foremost in evolutionary ideas in the 18th century, although as noted by Wigglesworth (1976), this latter notion was much abused. With respect to phylogeny, according to Wheeler et al. (2001), an epistemological revo­ lution was brought about by the publication of Hennig’s (1966) book, which is an English trans­ lation and revision of an earlier publication by  the German entomologist (Hennig 1950). Hennig (1966) used mostly insect examples in the explanation of his phylogenetic systematics, having earlier (Hennig 1965) briefly explained his methodology. Brundin (1966) was one of the first biologists to adopt this new methodology in his consideration of transantarctic relation­ ships of chironomid midges. Later, Hennig (1969, 1981) applied the method in his consid­ eration of insect phylogeny. It has now been generally adopted in discussions of the phylog­ eny of other animals and plants (Wiley 1981), and now prevails in considerations of insect phylogeny (Kristensen 1981) and both morpho­ logical and molecular data on the phylogeny of arthropods as a whole (Wheeler et  al. 1993, 2001; Boore et  al. 1994; Friedrich and Tautz 1995; Giribet et al. 2001; Nardi et al. 2003). 2.4.5 Physiology

Insects have been used for the study of the funda­ mental problems of physiology (Wigglesworth 1976). Today, the existence of cytochromes is common knowledge, but there are probably many biochemists who do not realize that the discovery of cytochromes was a product of the study of insect physiology (Wigglesworth 1976). Keilin (1925), while following the fate of hemo­ globin beyond the endoparasitic larval stage in the fly Gasterophilus intestinalis (DeGeer), was led to the discovery of cytochromes in flight mus­ cles of the adult free‐living insect (Kayser 1985). Wigglesworth (1976) noted that insect Malpighian tubules afford exceptional opportu­ nity for the study of the physiology of excretion,

owing to the ability to isolate individual tubules and have them function in vitro, as first demon­ strated by Ramsay (1955) in the stick insect Carausius morosus (Sinety). Bradley (1985) reviewed the structural diversity of Malpighian tubules in insects and showed them to have diverse functions. The Malpighian tubules of the larvae of the saltwater‐tolerant mosquito Aedes campestris Dyar and Knab can actively transport sulfate ions, an unusual function in animals (Maddrell and Phillips 1975). This sul­ fate transport in the Malpighian tubules of lar­ vae of Aedes taeniorhynchus (Wiedemann) is inducible and suggests that sulfate stress results in the synthesis and insertion of additional transport pumps into the Malpighian tubule membranes (Maddrell and Phillips 1978). Insect Malpighian tubules, in comparison with verte­ brate glomerula or other invertebrate tubules, are impermeable to organic molecules (Bradley 1985), although several insects can excrete nico­ tine independently of ion movement. However, transport systems for organic bases might not be universal in insects (Maddrell and Gardner 1976). The Malpighian tubules of the grasshop­ per Zonocerus variegatus (L.) have an inducible transport mechanism that actively removes the cardiac glycoside ouabain from the hemolymph (Rafaeli‐Bernstein and Mordue 1978). The isolated tubules of the large milkweed bug Oncopeltus fasciatus (Dallas) can excrete oua­ bain (Meredith et al. 1984). This excretory func­ tion is important for these insects, which feed on plants containing cardenolides. O. fasciatus also has ouabain‐resistant Na‐ and K‐ATPases (Moore and Scudder 1985). Weight for weight, the asynchronous flight muscles of insects generate more energy than any other tissue in the animal kingdom (Smith 1965). A unique feature of most insect flight muscles is that the fine ramifications of the tra­ cheal system, the tracheoles, penetrate deeply into the muscle fibers (Beenakkers et al. 1985). These flight muscles are among the most active tissues known. They have highly efficient fuel management and a remarkably high metabolic rate (Beenakkers et  al. 1984). In most insects,

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carbohydrate is the most important substance for flight, but many insects, particularly the Lepidoptera and Orthoptera, possess the capac­ ity to use lipids for flight, and in some insect species proline is used (Beenakkers et al. 1985). Insects and other terrestrial arthropods use several techniques to adapt to alpine and polar environments (Downes 1965, Ring 1981). The study of insects at low temperature (Lee and Denlinger 1991) has largely elucidated the phe­ nomena of cold hardiness, freeze‐tolerance, supercooling, and the role of antifreeze proteins (AFPs) and cryoprotectants. The polyhydric alcohol glycerol and other polyols such as man­ nitol, sorbitol, and threitol are responsible for most increases in supercooling in insects (Mullins 1985). AFPs from insects are far more potent than those from fish (Bower 1997). Some insect AFP cDNAs (Graham et al. 1997, Tyshenko et al. 1997) and genes (Guo et al. 2005, Qin and Walker 2006) have been isolated, and potential transfer to other hosts is now being investigated. However, neither transfer of fish AFP genes (Duncker et al. 1995) nor transfer of hyperactive spruce budworm AFP genes (Tyshenko and Walker 2004) to transgenic D. melanogaster has conferred cold tolerance to the recipient. 2.4.6 Ecology

Insects provide some of the best material for the ecologist (Wigglesworth 1976). The long‐ term research by Schwerdtfeger (1941) on German forest insects provided an example of the constancy of animal numbers, an essential concept in the development of Darwin’s theory of natural selection. Tamarin (1978) reviewed the major concepts and debates on population regulation in ecology, and showed that insects have had a major role. Many aspects of popula­ tion dynamics; population regulation by pre­ dators, parasites, or parasitoids; and the understanding  of density‐dependent factors, density‐­ independent factors, and key factor analysis (Clark et  al. 1967, Varley et  al. 1973) were developed through research on insects (Andrewartha and Birch 1973).

Crombie (1945) confirmed that Gause’s experimental results on interspecific competi­ tion with Paramecium also held true in the Metazoa by using a number of species of insects that lived in stored products. Chapman (1928) introduced the beetle Tribolium as a laboratory animal, and Park (1948), working with Tribolium castaneum (Herbst) and Tribolium confusum Jacquelin du Val, investi­ gated some of the complicating factors in inter­ specific competition, although the early results were compromised by the discovery that the pathogenic coccidian parasite Adelina tribolii Bhatia was a third party in the conflict. Park (1954) later showed that the results of competi­ tion in Adelina‐free cultures could be pre­ dicted from a comparison of the carrying capacity of the two species in single‐species cultures, depending on the temperature and humidity conditions, and that changing such conditions frequently could lead to indefinite coexistence. Comparable results could occur in many species pairs, particularly for short‐gen­ eration species such as insects (Hutchinson 1953). Nevertheless, Price (1984) noted that many elusive aspects of species competition were investigated in subsequent experiments with insects, many of which were reviewed by DeBach (1966) and Reitz and Trumble (2002). The term “ecological character displacement,” introduced by Brown and Wilson (1956), became a controversial theme in ecology and evolutionary biology, and continues to be a focus of much exciting research (Dayan and Simberloff 2005). Insects have provided examples in the eco­ logical literature of the existence of enemy‐free space (Atsatt 1981, Jeffries and Lawton 1984, Denno et al. 1990), and research on water mite parasitism of water boatmen (Scudder 1983, Smith 1988, Bennett and Scudder 1998) has shown how parasitism can be a cryptic determi­ nant of animal‐community structure (Minchella and Scott 1991). An invasive leafhopper, Homalodisca coagulata (Say), might be engi­ neering enemy‐free space in French Polynesia (Suttle and Hoddle 2006).

2  The Importance of Insects

Research on semiochemicals, whether pheromones concerned with interspecific com­ munication or allochemicals (allomones or kair­ omones) (Brown et  al. 1970) involved with interspecific communication, was pioneered using insects (Karlson and Butenandt 1959, Brown et  al. 1970, Whittaker and Feeny 1971, Duffey 1977, Price 1981, Rutowski 1981, Mayer and McLaughlin 1990). The term “pheromone” was proposed originally by Karlson and Lüscher (1959) for the first sex pheromone, bombykol, identified by Butenandt et  al. (1959) from the silkworm moth Bombyx mori (L.). Since the earliest observation of mate‐finding by Fabré (1910) and others, the power of female insects to lure males has astonished biologists (Phelan 1992). Probably no mate‐­communication system is better studied than that in the Lepidoptera (Phelan 1992). Sex‐pheromone components for about 80 compounds from more than 120 lepidopterous species have been discovered (Tamaki 1985), and they are known from many other groups of insects (Jacobson 1972). Yet, this sexual‐communication database has remained largely untapped by evolutionary biologists, outside the field of insect phero­ mones (Phelan 1992). The observation by B. Hüber in 1914 that alarm behavior in honeybee workers could be triggered by volatile sting‐derived components has been followed by discovery and research on  alarm pheromones in many other insects (Blum 1985). Aggregation pheromones occur in six  insect orders, although the majority have been discovered and studied in the Coleoptera, particularly the bark and timber beetles (Cur­ culionidae: Scolytinae) (Borden 1985). Other insect semiochemicals function as trail phero­ mones, spacing (epideictic) pheromones, and courtship pheromones, as well as in various interspecific communication situations (Haynes and Birch 1985, Roitberg and Mangel 1988). Sociality is the most striking and sophisti­ cated innovation of the insects (Grimaldi and Engel 2005), and semiochemicals are the glue that holds social insect colonies together (Winston 1992). The detailed structure and

function of these complex societies have amazed scientists and posed major problems in biology, such as the question of caste determination and kin selection. Caste determination and its con­ trol in ants, bees, termites, and wasps have been covered by Hardie and Lees (1985), and the biol­ ogy of these insects is well known (Wilson 1971). Kin selection is still the subject of much debate (Benson 1971, Eberhard 1975, Guilford 1985, Malcolm 1986). Insects have provided classic examples of commensalism, endosymbiosis, mimicry, mutu­ alism, and phoresy, although many examples, especially those of mimicry (Punnett 1915), have been based on subjective natural history observations rather than on experimentation (Malcolm 1990). When experiments are carried out, some of the classic examples have had to be reassessed (Ritland and Brower 1991). Ants and their relationship with Acacia (Janzen 1966) provide a good example of mutu­ alism, as do the insects that cultivate fungus gardens (Batra and Batra 1967). The well‐known fungus‐growing leaf‐cutter ants (Weber 1966, Martin 1970, Cherrett et  al. 1989), in an association that is some 50 million years old (Mueller et al. 1998), involve a third mutualist in the  system, namely the antibiotic‐producing Streptomyces bacteria (Currie et al. 1999). These leaf‐cutting ants (Atta spp.) evidently have an important ecological role as a result of their long‐distance transport redistribution and con­ centration of critical nutrients for plants grow­ ing near their nests (Sternberg et al. 2007). The food‐for‐protection association between ants and honey‐producing hemipterans is one of the most familiar examples of mutualism; these keystone interactions can have strong and per­ vasive effects on the communities in which they are embedded (Styrsky and Eubanks 2007). Insects are particularly prone to endosymbi­ otic associations (Henry 1967, Baumann et al. 1997), and have provided insights into the evolutionary biology, genetics, and physiol­ ogy of this intimate association. Many organ­ isms  also live ectosymbiotically with insects (Henry 1967).

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Insect Biodiversity: Science and Society

Phoresy among entomophagous insects is well documented (Clausen 1976). And the occurrence of midge and mosquito larvae in the pool of water held by the leaves of the carnivo­ rous pitcher plant, where they feed on decaying invertebrate carcasses, is a classic example of commensalism (Heard 1994). Because of their extreme mobility, insects have challenged many of the prevailing con­ cepts in zoogeography (Johnson and Bowden 1973), showing that species adapted to staying put are among the most successful travelers. Research on insect dispersal and migration (Johnson 1969) has shown the complex interre­ lations with agriculture, meteorology, medicine, physiology, and many other areas of general sci­ ence. The dispersal and movement of insect pests is a growing concern (Stinner et al. 1983; Wheeler and Hoebeke, this volume). Movement of organisms from one habitat to another can have profound effects on the structure and dynamics of food webs (Polis et al. 2004). Energy subsidies can either stabi­ lize or destabilize food webs, depending on the nature of the subsidy and what components of  the food web are subsidized. Dispersal influences food‐web structure, and studies of insect dispersal from this viewpoint could add to our understanding of community ecology (Thompson 2006). Insects have played a major part in the devel­ opment of ecological and island biogeography theory (Hafernik 1992). Much has been learned about the effects of fragmentation on insect populations and the movement of individuals between patches (Hunter 2002). Species living in highly fragmented landscapes often occur as metapopulations, and much of the literature on metapopulation dynamics has been the result of  studies on insects, particularly butterflies (Boughton 1999, Hanski 1999, Hanski and Singer 2001, Wahlberg et al. 2002, Hanski et al. 2006). Different population structures can have markedly different evolutionary outcomes (Barton and Whitlock 1997). The value of habi­ tat corridors also has been evaluated (Haddad 1999a, 1999b; Haddad and Baum 1999; Collinge

2000). Their function depends on environmen­ tal variation, landscape context, patch size, and species characteristics (Collinge 2000). Studies on insect–plant food webs have shown that habitat fragmentation can affect trophic pro­ cesses in highly complex food webs involving hundreds of species (Valladeres et  al. 2006). Research with butterflies also has shown that the surrounding matrix can significantly influ­ ence the effective isolation of habitat patches (Ricketts 2001). Because butterflies respond to subtle habitat changes, they have been sug­ gested as ecological indicators of endangered habitats (Arnold 1983), for which they could serve as umbrella species (Murphy et al. 1990). 2.4.7 Paleolimnology and Climate Change

Quaternary insect fossils are proving to be sen­ sitive indicators of past environments and cli­ mates (Elias 1994). Insect exoskeletons are found chiefly in anoxic sediments that contain abundant organic detritus. Lakes, ponds, and kettleholes serve as reservoirs that collect insects, and sediments that accumulate in these waters act rapidly to cover their remains, pre­ venting oxidation. Insect remains, therefore, have played a vital part in paleolimnological studies aimed at inferring and interpreting past environmental conditions (Smol and Glew 1992). Because insects in particular respond readily to changes in temperature more promptly and with greater intensity than do other compo­ nents of the terrestrial biota, they are providing evidence that major climatic changes in the past took place with unexpected suddenness, mov­ ing from glacial cold to interglacial warmth in decades rather than in millennia (Elias 1994). Such evidence is vital for current decision mak­ ing with respect to the management of ecosys­ tems (Smol 1992), and gives an indication of what might occur with climate change in the near future. Various life‐history and fitness traits, such as weight and survival of insect her­ bivores, probably will change as climate changes (Scherber et al. 2013).

2  The Importance of Insects

Crozier (2004), studying the sachem skipper Atalopedes campestris (Boisduval) in the Pacific Northwest, was the first to provide unequivocal data consistent with the hypothesis that current winter warming will drive butterfly range expan­ sion in North America. Ample evidence shows that insects are one of the first groups of living organism to respond to ongoing global climate change (Franco et  al. 2006, Wilson et  al. 2007). Predicting insect response is now an active area of investigation (Williams and Liebhold 1997, 2002; Sharma 2014). Understanding insect strate­ gies for survival under these circumstances, such as how they cope with new food sources (Thomas et al. 2001, Braschler and Hill 2007) and adjust to more acute temperature and humidity fluctua­ tions is still a challenge (Philogene 2006). Many species of tropical and widespread insects, such as Drosophila, will probably face proportional reductions in their distributions as climate change continues (Overgaard et  al. 2014). Research on butterflies in the United Kingdom has shown that many species fail to track recent climate warming because of a lack of suitable habitat (Hill et  al. 2002), leading to local extinctions at low‐latitude range boundaries of species (Franco et al. 2006). Other studies indicate that bumblebees are disap­ pearing from the southern areas of their ranges, although they are not expanding to new, more northern ranges owing to other biological factors (Kerr et  al. 2015). These distributional changes will have an impact on the crops and native plants that the bees pollinate. Sharma (2014) reviewed climate change effects on insects, with special reference to the projected impacts on crop production. In vol­ ume two of Insect Biodiversity: Science and Society, Gillespie et  al. review and discuss the impacts of global climate change on insect bio­ diversity in agroecosystems and the conse­ quences for human society.

2.5 ­Insects and the Public Insects have had a long connection with human­ kind. Primitive humans learned to obtain honey

by robbing the nests of bees in hollow trees or rock crevices by about 7000 bc (Townsend and Crane 1973). Archaeological evidence shows that the cultivation of the silkworm B. mori was begun before 4700 bc, and sericulture was an important part of peasant life in China between 4000 and 3000 bc (Konishi and Ito 1973). The notion that metamorphosis of the sacred scarab Scarabaeus sacer L. is a symbol of the resurrec­ tion of the dead, according to the Egyptians, might be of recent origin (Bodenheimer 1960), but the supposed health properties of this beetle were identified by at least 1550 bc (Harpaz 1973). Fumigation by burning toxic plants to kill insect pests dates from about 1200 bc (Konishi and Ito 1973). Insects have been in competition with humans for the products of our labor ever since cultiva­ tion of soil began (Wigglesworth 1976). Many members of the public – agriculturalists, health­ care professionals, homeowners, and natural resource personnel – no doubt regard insects as perfect pests (Scudder 1976). Some medical professions, however, find certain insects beneficial, even in modern medicine. Certain fly maggots, for example, are  a valuable, cost‐effective tool for treating wounds and ulcers that are unresponsive to conventional treatment and surgical interven­ tion (Mumcuoglo et  al. 1999). The saliva of hematophagous deer flies (Chrysops spp.) con­ tains a potent inhibitor of platelet aggregation (Grevelink et  al. 1993) previously unreported from arthropods and of potential use in medical therapeutics. Insect evidence can be paramount in estab­ lishing the postmortem interval for a decedent, as well as in providing additional information to investigators capable of deciphering the ento­ mological clues (Byrd and Castner 2001). Forensic entomologists, therefore, have found insects to be useful in criminal investigations (Catts and Goff 1992), and some criminal elements in our society have used insects, espe­ cially rare butterflies, in illegal trade. Educators and student participants in sci­ ence  fairs have found insects useful in simple

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Insect Biodiversity: Science and Society

experiments, although this practice is now discouraged by some animal‐rights activists. Wigglesworth (1976) pointed out that insects present desirable properties as objects for experimentation. They are tolerant of opera­ tion; they are so varied in form and habit that some species suited to the problem at hand can surely be found; and their small size makes it possible for the observer to be constantly aware of the whole, while focusing attention on the part (Wigglesworth 1976). As a result, insects are used in numerous studies of the living world (Kalmus 1948, Cummins et al. 1965), although in many jurisdictions, researchers and even field biologists working on insects must have animal‐ care certificates. Fishing enthusiasts have a special interest in insects. The sport and technique of fly fishing and fly tying primarily attempts to mimic the appearance and behavior of mayflies and other insects (McCafferty 1981), and real insects can also be used (Petersen 1956). Well‐known insect products used by humans include lac from the lac insect (Laccifer lacca Kerr.) and cochineal from Dactylopius coccus Costa (Bishopp 1952). Real silk from the silk moth B. mori must now compete with synthetic fibers (Bishopp 1952). In the past, species of the butterfly genus Morpho  –  with their striking iridescent blue color, which originates from the precisely spaced, overlapping projections on the ridges of their wing scales (I. Peterson 1995) – have been collected for jewelry to such an extent that they are now in danger of extinction (Scudder 1976). More recent efforts have promoted live jewelry using showy insects, mostly beetles. Humans are involved in food chains, and insects have been used as human food for cen­ turies in many cultures (Bodenheimer 1951; DeFoliart 1989, 1992). Some insects also are eaten by gourmands and treated as conversation pieces. Honeybees, mainly Apis mellifera L., remain the most economically valuable pollinator of crop monocultures worldwide (Klein et  al. 2007). When wild bees do not visit agricultural

fields, managed honeybees are often the only solution for farmers to ensure crop pollination, because they are cheap, convenient, and versa­ tile, although they are not the most effective pollinators on a per flower basis for some crops (Klein et al. 2007). Farmers in the United States pay bee keepers more than $30 million annually for the use of honeybees to pollinate crops val­ ued at $9 billion (Weiss 1989). Honey has valu­ able nutritional and other benefits (Buchmann and Repplier 2005, Simon et al. 2006). Beeswax has many modern uses in industry and the arts (Bishopp 1952), and even royal jelly has been promoted for its supposed health benefits (Crane 2003). The total value of crops in the United States resulting from pollinator activity in 1980 approached $20 billion, compared to the approximately $140 million worth of honey and beeswax produced in the United States (Levin 1983). These figures indicate that the activity of bee pollination is worth 143 times as much as the value of honey and beeswax, on which most beekeepers must make their living. That insects, especially honeybees, are valua­ ble in pollination (Vansell and Griggs 1952), is well known to the general public. The decline of bee populations in Europe and North America (Allen‐Wardell et al. 1998, Goddard and Taron 2001, Biesmeijer et  al. 2006) has raised alarm about pollinators that fertilize crops essential for the human food supply. Articles in the popu­ lar press (Bueckert 2007) point out that threats to pollinators include climate change, habitat destruction, human indifference, invasive spe­ cies, and pesticides. As a result, many gardeners are now interested in growing plants that attract butterflies and other insects, and even some municipal governments have ventured into this sphere in their parks and green spaces. Farmers and others are told that they should be less zeal­ ous about eliminating weeds around the bound­ aries of farmland, in ditches, or along utility rights of way (Bueckert 2007). The local gardener and nursery owner, as well as agriculturalists and foresters, now realize that  insects, both parasitoids and predators (Claussen 1952), can be used in natural

2  The Importance of Insects

biological control. Ladybird beetles are cultured for this purpose, are readily available, and seem to be released everywhere in the world (Caltagirone and Doutt 1989). However, users are not always aware that some of these ladybird beetles can be a major threat to native species (Staines et al. 1990, Howarth 1991, Elliott et al. 1996, Brown and Miller 1998, Cottrell and Yeargan 1999, Turnock et al. 2003). In intraguild predation, larger species are favored unless protected chemically (Sato and Dixon 2004). Gardeners also now know that carabid ground beetles are useful predators that can be affected negatively by indiscriminate use of insecticides. Insect books specially directed to gardeners are available (Cranshaw 2004). Butterfly farms and insectaries are used as public attractions, and insects can be used in wildlife education centers to educate the public on the living world and the need for biodiversity conservation. The inclusion of insects now under various endangered species legislation also has increased public awareness of this group of animals and the need for habitat con­ servation (Hafernik 1992). Butterflies in particular first induce many young people to become interested in collecting insects, leading many of them to become professional entomologists, interested in the outdoors and involved in the study of systematic entomology, ecology, and behavior (Michener 2007). Although many members of the public find insects abhorrent, others, using helpful and readily available field guides, such as those on butterflies (Glassberg 2001) and dragonflies (Dunkle 2000), have found insects of interest as a vocation. Insects are now becoming almost as popular as birds in this regard, and even a bird­ er’s bug book is available (Waldbauer 1998). Insects are now so popular with the public that publishers seem to be flooding the market with books on these animals. These books vary from encyclopedias (Resh and Cardé 2009) and solid accounts of biology (Wigglesworth 1964, Berenbaum 1995) to more popular books with varying slants (Hutchins 1966; Blaney 1976; d’Entrèves and Zunino 1976; Waldbauer 1996,

2003; Eisner 2003). The books by Berenbaum (1995), in particular, emphasize insects and their influence on human affairs. Butterflies are one of the few insect groups with a positive image among the average citizen (Hafernik 1992). The migratory monarch butterfly Danaus plexippus (L.) is perhaps the most well‐known and widely recognized butterfly, at least in North America (Nagano and Sakaii 1989), and its annual migra­ tion is considered one of the epic phenomena of the animal kingdom. Monarch wintering colo­ nies have been a tremendous attraction for tour­ ists, have improved local economies (Nagano and Sakaii 1989), and have engendered public interest in biodiversity conservation. Insect conservation is still in its infancy (Pyle et al. 1981), but the conservation of insects is of increasing public concern. The task for ento­ mologists is to decide how best this can be accomplished. Despite their ecological impor­ tance, their conservation has received little attention (Hafernik 1992), although recent reviews (Samways 1994, 2005, 2007a, 2007b; New 1995) might change this status.

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Valladares, G., A. Salvo and L. Cagnolo. 2006. Habitat fragmentation effects on trophic processes in insect‐plant food webs. Conservation Biology 20: 212–217. Van Driesche, R. G. and T. S. Bellows (eds). 1996. Biological Control. Chapman and Hall, New York. 539 pp. Vansell, G. H. and W. H. Griggs. 1952. Honey bees as agents of pollination. Pp. 88–107. In: Insects. The Yearbook of Agriculture 1952. United States Department of Agriculture, Washington, DC. Varley, G. C., G. R. Gradwell and M. P. Hassell. 1973. Insect Population Ecology: an Analytical Approach. Blackwell, Oxford. 212 pp. Vogel, S. and C. Westerkamp. 1991. Pollination: an integrating factor in biocenoses. Pp. 159–170. In A. Seitz and V. Loeschcke (eds). Species Conservation: a Population‐Biological Approach. Birkhäuser Verlag, Basel. Wahlberg, N., T. Klemetti, V. Selonen and I. Hanski. 2002. Metapopulation structure and movements in five species of checkerspot butterflies. Oecologia 130: 33–43. Waldbauer, G. 1996. Insects through the Seasons. Harvard University Press, Cambridge, Massachusetts. 289 pp. Waldbauer, G. 1998. The Birder’s Bug Book. Harvard University Press, Cambridge, Massachusetts. 290 pp. Waldbauer, G. 2003. What Good are Bugs? Insects in the Web of Life. Harvard University Press, Cambridge, Massachusetts. 366 pp. Wardle, D. A. 2002. Communities and Ecosystems: Linking the Aboveground and Belowground Components. Princeton University Press, Princeton, New Jersey. 392 pp. Watanabe, M. E. 1994. Pollination worries rise as honey bees decline. Science 265: 1170. Waterhouse, D. F. 1974. The biological control of dung. Scientific American 230 (4): 100–109. Weber, N. A. 1966. Fungus‐growing ants. Science 153: 587–604. Weis‐Fogh, T. 1960. A rubberlike protein in insect cuticle. Journal of Experimental Biology 37: 889–907.

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Weismann, A. 1864. Die nachembryonale Entwicklung der musciden nach Beobachtungen an Musca vomitoria und Sarcophaga cararia. Zeitschrift fur Wissenschaftliche Zoologie 14: 187–326. Weiss, R. 1989. New dancer in the hive. Science News 136: 282–283. Weisser, W. W. and E. Siemann. 2004. The various effects of insects on ecosystem functioning. Pp. 3–24. In W. W. Weisser and E. Siemann (eds). Insects and Ecosystem Function. Springer‐ Verlag, Berlin Heidelberg. Wheeler, Q. D. 1990. Insect diversity and cladistic constraints. Annals of the Entomological Society of America 83: 1031–1047. Wheeler, W. C., P. Cartwright and C. Y. Hayashi. 1993. Arthropod phylogeny: a combined approach. Cladistics 9: 1–39. Wheeler, W. C., M. Whiting, Q. D. Wheeler and J. M. Carpenter. 2001. The phylogeny of the extant hexapod orders. Cladistics 17: 113–169. White, D., Jr., K. C. Kendall and H. D. Picton. 1998. Grizzly bear feeding activity at alpine army cutworm moth aggregation sites in northwest Montana. Canadian Journal of Zoology 76: 221–227. White, K., M. E. Grether, J. M. Abrams, L. Young, K. Farrell and H. Steller. 1994. Genetic control of programmed cell death in Drosophila. Science 264: 677–683. White, M. J. D. 1973. Animal Cytology and Evolution. 3rd edition. Cambridge University Press Cambridge. 961 pp. White, M. J. D. 1978. Modes of Speciation. W. H. Freeman and Co., San Francisco, California. 455 pp. Whittaker, R. H. and P. P. Feeny. 1971. Allelochemics: chemical interaction between species. Science 171: 757–770. Wiebes, J. T. 1979. Co‐evolution of figs and their pollinators. Annual Review of Ecology and Systematics 10: 1–12. Wiegert, R. G. and F. L. Evans. 1967. Investigations of secondary productivity in grasslands. Pp. 499–518. In K. Petrusewicz (ed). Secondary Productivity in Terrestrial

Ecosystems. Institute of Ecology, Polish Academy of Science, Warsaw. Wigglesworth, V. B. 1964. The Life of Insects. Weidenfeld and Nicholson, London. 360 pp. Wigglesworth, V. B. 1976. Insects and the Life of Man. Collected Essays in Pure Science and Applied Biology. Chapman and Hall, London. 217 pp. Wiggleworth, V. B. 1985. Historical perspective. P. 1024. In G. A. Kerkut and L. I. Gilbert (eds). Comprehensive Insect Physiology, Biochemistry and Pharmacology. Volume 7. Endocrinology I. Pergamon Press, Oxford. Wiley, E. O. 1981. Phylogenetics: the Theory and Practice of Phylogenetic Systematics. John Wiley and Sons, New York. 439 pp. Williams, D. W. and A. M. Liebhold. 1997. Latitudinal shifts in spruce budworm (Lepidoptera: Tortricidae) outbreaks and spruce‐fir forest distributions with climate change. Acta Phytopathologica et Entomologica Hungarica 32: 205–215. Williams, D. W. and A. M. Liebhold. 2002. Climate change and the outbreak ranges of two North American bark beetles. Agricultural and Forest Entomology 4: 87–99. Wilson, E. O. 1971. The Insect Societies. Belknap Press, Cambridge, Massachusetts. 548 pp. Wilson, E. O. 1987. The little things that run the world (the importance and conservation of invertebrates). Conservation Biology 1: 344–346. Wilson, E. O. 1992. The Diversity of Life. W. W. Norton, New York. 424 pp. Wilson, R. J., Z. G. Davies and C. D. Thomas. 2007. Insects and climate change: processes, patterns and implications for conservation. Pp. 245–279. In A. J. A. Stewart, T. R. New and O. T. Lewis (eds). Insect Conservation Biology. CAB International, Wallingford, United Kingdom. Winston, M. L. 1992. Semiochemicals and insect sociality. Pp. 315–333. In B. D. Roitberg and M. D. Isman (eds). Insect Chemical Ecology: an Evolutionary Approach. Chapman and Hall, London.

2  The Importance of Insects

Wootton, R. 2000. From insects to microvehicles. Nature 403: 144–145. Wootton, R. J. and C. P. Ellington. 1991. Biomechanics and the origin of insect flight. Pp. 99–112. In J. M. V. Rayner and R. J. Wootton (eds). Biomechanics in Evolution. Cambridge University Press, Cambridge.

Wootton, R. J., J. Kukalova‐Peck, D. J. S. Newman and J. Muzon. 1998. Smart engineering in the Mid‐Carboniferous: How well could Paleozoic dragonflies fly? Science 282: 749–751. Zinsser, H. 1934. Rats, Lice and History. Routledge, London. 301 pp.

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Part I Insect Biodiversity: Regional Examples

47

3 Insect Biodiversity in the Nearctic Region Hugh V. Danks1 and Andrew B. T. Smith2 1 2

Retired. Biological Survey of Canada, Canadian Museum of Nature, Ottawa, Ontario, Canada Research Division, Canadian Museum of Nature, Ottawa, Ontario, Canada

The Nearctic region, which occupies an area of nearly 20 million km2 (Fig. 3.1), includes many different environments inhabited by insects, ranging from arctic tundra to lush forests. Published and unpublished information and extrapolations and corroborations by specialists suggest that more than 147,000 species of insects occur in the region, but only about 65% of the species have been formally described in the scientific literature. Only about 6% of the species are estimated to have been described in the immature stages (Kosztarab and Schaefer 1990a). The state of knowledge varies widely among different groups; families that contain species of economic importance are better known. High Arctic regions are the least rich, and southern areas (especially northern Mexico, Arizona, Florida, and Texas) contain the greatest percentage of the fauna. The Nearctic region has lower insect biodiversity relative to other biogeographical realms and is most similar faunistically to the Palearctic region, with many overlapping taxa at the lower taxonomic levels (genera and species). The fauna overlaps significantly with that of the Neotropical region at the generic level. Basic taxonomic research on Nearctic insects is more advanced than for most other regions, but is still in the discovery and development stages for the vast majority of insect taxa. Most Nearctic insect species are

known only from a basic description and ­antiquated distributional records or are completely unknown to science. Only a small percentage of Nearctic insect taxa have been given a modern and thorough taxonomic treatment to describe and diagnose them properly, map out their distributions through space and time, and assess their evolutionary relationships with other taxa. This chapter examines the biodiversity of insects in the Nearctic region, based on extant species, and the state of knowledge about them. Basic information on the numbers of species in this region comes from educated book‐keeping exercises; these estimated numbers depend on fewer assumptions than are necessary to make similar estimates in tropical regions of much greater biodiversity, so no considerable efforts are made here to refine the estimates in detail. Rather, some attempt is made to synthesize and interpret the general patterns that emerge. The Nearctic region comprises the northern part of the New World. The core of the fauna lives in North America, but Nearctic faunal elements occupy the mountains of Mexico and Central America, at least as far south as the montane pine‐oak forests of Honduras and northern Nicaragua (Halffter 1974, 1987, 2003). The nucleus of northern, more‐or‐less cold‐ adapted forms in North America is ­supplemented

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

48

Insect Biodiversity: Science and Society

0

1

2

3

4 5 7 9 10

6 8 11

Figure 3.1  Ecological biomes of the Nearctic realm, adapted from data available from the World Wildlife Fund at http://www.worldwildlife.org/biomes, as described by Olson et al. (2001). 0, permanent ice; 1, tundra; 2, boreal forest; 3, moist temperate forest; 4, temperate grasslands; 5, temperate broad‐leaf and mixed forest; 6, temperate coniferous forest (southeast); 7, xeric shrublands and deserts; 8, subtropical grasslands (Gulf coastal grasslands); 9, temperate grasslands (Central California); 10, Mediterranean (California chaparral and woodlands); 11, warm temperate evergreen (oak‐pine) forest.

by many forms of subtropical affinity, especially in the southern United States. Additional species occur in the Mexican highlands, and addition of these taxa would increase the numbers of species reported from the Nearctic region. However, detailed faunal data are adequate only for North America (north of Mexico; henceforth North America). Therefore, most of the information presented below comes from this somewhat smaller area.

The Nearctic fauna is closely linked with that of the adjacent Palearctic fauna, from which it has received many components, especially in the north. The amount of overlap varies by taxon; a recent study of Holarctic spiders found that of 13,800 species, about 1% naturally occurred in both the Palearctic and Nearctic regions (Marusik and Koponen 2005). Conversely, less than 0.001% of scarab beetles have a n ­ atural distribution across the two realms

3  Insect Biodiversity in the Nearctic Region

(based on Gordon and Skelley 2007). In the south, the Nearctic region has received elements from the adjacent Neotropical fauna, but it also has contributed significantly to the Neotropical fauna. North America is so large that conditions change greatly from south to north and from west to east, spanning about 58 degrees of latitude and more than 105 degrees of longitude. Temperatures fall toward the north, and summer temperatures are higher and winter temperatures  lower in the middle of the continent. Consequently, North America includes insect‐ inhabited environments that range in mean July temperatures from below 5 °C (Canadian High Arctic) to 33 °C (Phoenix, Arizona) and in mean January temperatures from less than −30 °C (High Arctic) to about 20 °C (southern Florida). Regions vary in mean annual rainfall from less than 100 mm or 200 mm (polar deserts; southwestern deserts, e.g., Reno, Nevada) to 2000– 3000 mm along the northwest coast (e.g., Yakutat, Alaska: 3348 mm) and northern Cordillera (e.g., Prince Rupert: 2399 mm) (Bryson and Hare 1974). Correspondingly, habitats range from hot desert and cold arctic fellfield to lush coastal temperate rainforest. The many different vegetation formations in this area have been classified or categorized in several different ways (e.g., Taktajan 1986). The current Nearctic fauna also is influenced by history (Matthews 1979). Northern North America was glaciated in Pleistocene times, and the faunas of large areas in the northern part of the continent were exterminated by ice sheets 1–2 km thick, which receded only 10,000– 15,000 years ago. More recently, invasive species have become a significant component of the fauna (Lindroth 1957, Turnbull 1979, Pimentel 2002, Foottit et al. 2006), with some effects on native species. Reductions also have occurred, some attributable to long‐term habitat changes and some attributable to human activities. Nearctic biodiversity is low relative to other biogeographic realms. For example, 1808 Nearctic scarab beetles are known (Smith 2009). This total is similar to that for Europe (2318),

but is approximately four times less than the total for the entire Palearctic region (Löbl and Smetana 2006). The greater species richness in the Palearctic region is due mainly to the much larger land area with a greater variety of ­ecozones. Nevertheless, a tremendous amount of insect biodiversity exists in the Nearctic region, including endemic families such as the  Pleocomidae and Diphyllostomatidae (Coleoptera), with low overlap, at the species and genus levels, with insects in other realms.

3.1 ­Influence of Insect Biodiversity on Society in the Nearctic Region The importance of entomology and the study of insect biodiversity emerged in North America during the 1800s. One of the main driving forces behind this emergence was the unprecedented expansion of agriculture in the eastern half of the continent. Many native and invasive pest insects were destroying crops, which led to a great thirst for knowledge about these species. Naturalists and farmers realized that knowledge of the natural history, life cycles, and biodiversity of insects were crucial to controlling pests. These challenges are still faced today, with globalization and climate change bringing new pest species into the Nearctic with ever‐increasing frequency. A major problem faced by early entomologists in North America was that all of the entomological expertise, collections, and libraries were in Europe and practically inaccessible to those in the New World. Early pioneers in North American entomology, such as Thomas Say (1787–1834), began publishing and establishing collections in North America (Stroud 1992). Entomological research published in North America began to proliferate in later decades as natural history societies and collections sprang up across the United States and Canada (Spencer 1964, Barnes 1985). In the 20th century, major institutions such as the Smithsonian Institution, California Academy of Sciences, Canadian National Collection of Insects,

49

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Insect Biodiversity: Science and Society

Arachnids and Nematodes, American Museum of Natural History, Harvard University Museum  of Comparative Zoology, and others came to prominence for their leading‐edge collections and research programs. Even though North America hosts a large proportion of the most eminent and active insect systematics programs and collections, major challenges still exist in describing the insect biodiversity of the Nearctic region. A sobering number of Nearctic insect species are still unknown to science  –  an estimated 50,000 Nearctic insect species (35%) are undescribed (Table 3.1). The underfunding of taxonomy and biodiversity research has been well documented and has affected the ability of the scientific community to get the job done – even in the Nearctic region, which has arguably been the hotspot for taxonomy and biodiversity research since the Second World War. Other factors have confounded efforts to describe the insect fauna of the Nearctic region. Many Nearctic species were described in the Victorian era, with type material deposited in European museums, and modern taxonomy often is inhibited by the difficult task of tracking down old type material. Poor record keeping, lost or destroyed collections, poor specimen labeling, specimen exchange without documentation, theft, and chronic underfunding of natural history collections are all impediments. The limited knowledge of the taxonomy of many groups causes problems even with basic characterizations and estimates of biodiversity. Species diversity of many poorly known groups is far greater than numbers found in the scientific literature because large proportions of the fauna are unknown to science. Newton et  al. (2000), for example, noted that the number of species of Staphylinidae beetles in North America increased by more than 700 between 1963 and 2000, a rise of about 17% in 37 years. Likewise, Grissell (1999) found that new species of Nearctic Hymenoptera were being described at a rate of at least 1500 per decade toward the second half of the 20th century. This rate peaked in the 1960s, when more than 2500 new species

of Hymenoptera were described from the Nearctic. Limited taxonomic knowledge also has led to the opposite problem – overestimations of species diversity have occurred in groups where careless or sloppy taxonomic work has resulted in species being described multiple times. Perhaps the most stunning examples of this were courtesy of Thomas Lincoln Casey (1831–96). Subsequent workers discovered that more than 90% of the so‐called species of carabid beetles Casey described from North America were previously described (Lindroth 1969). Casey described Tomarus gibbosus (De Geer), a common and widespread species of scarab beetle, 23 times (Saylor 1946)! The limited knowledge of the taxonomy of many groups can cause both overestimations and underestimations in species diversity, further undermining our abilities to have even basic levels of understanding of biodiversity for most of the truly megadiverse groups of organisms. Because taxonomy and biodiversity research are the foundation of other biological sciences, the paucity of basic knowledge of Nearctic insect biodiversity has a profound effect on other endeavors.

3.2 ­Insect Conservation Conservation of natural habitats and protection of species at risk are strong desires of people across North America. However, the use of insects in conservation studies and the recognition of insect species at risk have barely begun. Bossart and Carlton (2002) and Spector (2006) presented summaries indicating that insects are better than any other group of organisms as ecological indicators and in monitoring biotic changes in the environment. However, they pointed out that only a tiny fraction of insect diversity from only a few select taxa have been used for this purpose (notably dragonflies, butterflies, and selected groups of moths and beetles). Population studies of British Lepidoptera have demonstrated that insects are effective as a means of detecting biodiversity declines

10 3 2 0 0 513

578

66

41

20

13

23

Plecoptera

Blattodea

Isoptera*

Mantodea

Notoptera

Dermaptera

59

5,105

310

Neuroptera

1

43

21

Megaloptera

Raphidioptera

20

700

109

Mallophaga*

Strepsiptera

110

85

0

655

68

257

76

Psocoptera

233

1

Anoplura*

10,804

700

Hemiptera

Thysanoptera

5

13

3

Embiidina

Zoraptera

5

1,804

31

Orthoptera

Phasmatodea

0

2

555

415

Ephemeroptera

20

23

Estimated number of species unknown

Odonata

35

30

Microcoryphia

Thysanura

Number of species known

Order

Table 3.1  Census of Nearctic insects.

395

21

44

129

1,355

144

367

933

15,909

8

14

36

2,317

23

13

22

44

76

578

417

614

50

58

Estimated total number of species

64

2

30

6

1

35

10

35

1,470

0

0

0

360

0

2

0

0

8

232

355

461

6

7

Number of species with immatures described

78

100

98

84

52

53

70

75

68

37

93

86

78

100

100

91

93

87

100

>99

90

60

60

Adults

16

10

68

5

(Continued)

0.05); thus, our sampling regime by fogging was not affecting faunal balance. To obtain a preliminary estimate of beetle richness in our plots, we chose 300 samples from Piraña, as well as another 300 like samples at the control site, Tiputini. We found that 15,126 specimens of 14 family‐group beetle taxa represented 2010 morphospecies. A selection of these families is illustrated in Fig. 4.12. Based on species‐accumulation curve estimates (Erwin et al. 2005), a consistent set of patterns emerged in the data for the family‐group beetle taxa thus far investigated. In these taxa, even with the rigorous sampling regime, more samples than 600 are needed for us to know the universe of canopy and understory species in the local area, and certainly more than 300 samples at one site, even for the less‐diverse families. The exception among these family‐group taxa were the otidocephaline Curculionidae (Fig. 4.12), a small taxon of specialized weevils;

79

80

Insect Biodiversity: Science and Society Arachnida 12.20%

Blattaria 0.58% Orthoptera 0.68% Mantodea 0.01% Phasmatodea 0.02%

Diptera 33.00%

Psocoptera 2.56% Heteroptera 2.76%

Homoptera 0.90%

Hymenoptera 17.45%

Coleoptera 18.73% Lepidoptera 1.10%

Figure 4.11  Adult arthropod target‐taxa abundances for the Piraña (Onkone Gare) 1994–96 canopy samples.

combining 300 samples from both sites for a total of 600 proved adequate to nearly reach an asymptote for the species‐accumulation curve for the area. The Carabidae (Fig. 4.12) at Piraña were not adequately sampled with 900 samples; however, the 300 samples of carabids that have been processed thus far from Tiputini provided enough additional species for a species-accumulation curve to reach an asymptote for the region’s canopy species. The ground fauna is also species rich, and we are now assessing that fauna. When these two family‐group taxa reaching near asymptote were analyzed for complementarity between the two sites, the values were CI = 0.29 for the otidocephaline Curculionidae and CI = 0.69 for the Carabidae. For the rest of the families examined, at least 300 or more samples will need to be added to the database for the species‐accumulation curve to reach an asymptote. Thus, observed and predicted numbers of morphospecies (Fig. 4.12) likely will increase with additional collecting at Tiputini. In addition, some taxa already have produced more morphospecies to date than

were predicted from previous accumulation curve estimates (Fig. 4.12, Erwin et  al. 2005), whereas richness for other taxa remains lower than estimated. This discrepancy reflects the varying degree of taxonomic treatment by specialists in each group. The tumbling flower beetles of the family Mordellidae (Fig. 4.12) is an example of a group that is not particularly well known from the Neotropics, but has high morphospecies richness in the canopy. This situation demonstrates the importance of samples taken for applied conservation purposes as a significant new source of material for basic systematics research, and highlights the need for proper vouchering and databasing of individual specimens in ecological studies.

4.6 ­Morphospecies Richness to Biodiversity Estimating morphospecies richness in an ­ecosystem such as the Amazon is a necessary first step toward understanding its biodiversity

4  Amazonian Rainforests

e b d a c f

j

g

5 mm

h

i

k

Figure 4.12  Coleoptera taxa examined in Yasuni from 1994 to 2006. Images were taken with the EntoVision extended focus photography system (Alticinae and Cleridae not figured). For each taxon, the number of observed morphospecies (as of 2008) is listed, as well as predicted numbers of species based on accumulation curves and ICE (incidence‐based coverage estimator) calculations (Erwin et al. 2005). (See color plate section for the color representation of this figure.)

­ atterns. As our taxonomic resolution increases p and the technology to map patterns of richness and abundance data at the specimen level becomes more sophisticated, our ability to characterize assembly rules for tropical forests will

strengthen. For example, we can use distribution patterns to hypothesize which species are tourists and which are true canopy dwellers. Fig.  4.13 illustrates this point for the family Mordellidae, which we use as a case study.

81

Insect Biodiversity: Science and Society Mordellini

Mordellistenini

1 mm Glipostenoda

Mordellistena

Mordella

# individuals in 900 samples

82

250

250

(b)

200

200 150

150

100

100

(a)

50

50

Mordella Mordellistena Gliposetnoda

0

Figure 4.13  Histograms (a) showing morphospecies distribution curves for six Coleoptera groups from the 900 canopy samples collected from 1994 to 1996 from the Piraña (OG) plot (Otidocephalinae and Entiminae = Curculionidae; Strongyliini = Tenebrionidae). The shape of the curve for the Mordellidae (b) suggests oligarchic dominance by six morphospecies in three genera. These morphospecies, represented by numerical codes (c), were present in abundances of greater than 50 individuals in 900 samples. Further research and incorporation of new technologies will increase taxonomic resolution and put morphospecies into phylogenetic context (d). Images were taken with the EntoVision extended‐focus photography system.

0 Strongyliini Entiminae

004, 007, 021, 028, 038, 164

Canopy biorichness estimates (c)

Ceratocanthidae Otidocephalini

alpha-taxonomy DNA barcoding phylogenetic revisions updated classifications new keys geodatabases

(d)

Erotylidae Mordellidae

Mordellini Mordelistenini

Canopy biodiversity studies

Worldwide, about 1500 total species have been described, with 205 known from North America (Jackman and Lu 2002). Compared with other phytophagous beetle clades, little is known about the family Mordellidae in the Neotropics. North American mordellids are broadly classified as pollen feeders, especially of Apiaceae and Asteraceae plants, as adults, whereas the larvae are endophagous feeders of woody and herbaceous stems, decaying wood, and fungi (Jackman and Lu 2002). Two subfamilies and five tribes currently are described worldwide, but their phylogenetic relationships are not understood. In temperate zones, larvae in the tribe Mordellini bore into woody host plants, whereas larvae in the tribe Mordellistini use herbaceous hosts (Jackman and Lu 2002). A third tribe, the Conaliini, is found in the Neotropics, but the life

histories of adults and larvae are not well characterized. The morphospecies‐distribution curve for the Mordellidae (Fig. 4.13a) shows a pattern of few abundant taxa, with a long tail representing doubletons and singletons. To understand the mechanism driving this pattern, we should know how the abundant and rare species are related to each other and what life‐history characteristics they share (either via similar ways of life or shared recent ancestry). The utility of this approach has been shown for comparing physiological traits in aquatic insects (Buchwalter et al. 2008). Preliminary examination of the morphospecies of the Mordellidae collected from Piraña from 1994 to 1996 suggests that an oligarchy of dominant species exists (Fig. 4.13b–d); six morphospecies were found in numbers greater than

4  Amazonian Rainforests

50 in the 900 total samples, as well as a large number of rare species. When we put the six abundant morphospecies numbers into phylogenetic context, we found that they fitted into only three genera in two tribes. The tribe Conaliini also is known from Amazonia, but conaliine morphospecies were rare. Little is known about the life histories of adult and larval Mordellidae in the Amazonian canopy, so we cannot say what processes are driving this pattern other than to suggest that some of the rare taxa probably are understory species that were captured as canopy tourists. We do know, however, that the Mordellini and Mordellistenini were dominant in the canopy samples from the Piraña plot from 1994 to 1996. Morphospecies designations need to be confirmed and valid species names applied before accurate statistics can be calculated, but genus‐level keys are available only for the North American fauna. Work is underway to describe the putative common oligarchy morphospecies and, in the process, update the genus‐level classifications and keys. Histogram curves of other representative beetle groups (Fig. 4.13a) show different lineages with varying patterns of species distributions, as we would expect. These patterns might reflect different life histories and ecosystem requirements, or they could be artifacts of varying taxonomic scrutiny. However, the general pattern we see among those families that have been identified to morphospecies is that many rare species are in the canopy samples. Collections in the understory ecosystem in these plots will reveal whether the rare canopy taxa are abundant elsewhere, and whether the Mordellidae fauna is stratified vertically. We know little in general about what the overlap is between ground and canopy faunas, and this relationship can differ even among beetle subfamilies. For example, the beetle family Carabidae has distinct canopy fauna (i.e., arboreal species) and distinct ground fauna (i.e., terrestrial species) (Erwin 1991b). Of the nearly 500 species recorded thus far from the canopy of our two plots, only a dozen or so are terrestrial‐true species, the so‐called canopy tourists.

Amazonian biodiversity cannot be generalized until we know how much overlap occurs at both large and small spatial scales. Does the roughly 25% overlap in tree species between Piraña and Tiputini predict a certain amount of overlap between the insect communities? How does the degree of overlap differ among insect lineages? The above case study demonstrates that for many Neotropical insect groups, phylogenetic relationships, classifications, and keys at the genus level need to be revised before we can reliably assign valid names or associate males and females to confirm that morphospecies designations are accurate. A team of taxonomists is already doing this research with the specimens from these two hectare plots. Their contribution to increasing taxonomic resolution will allow us to compare more accurately pre‐ and post‐road building canopy richness between the control (Tiputini) and impact (Piraña) plots. Thus, advancing taxonomic knowledge will enable us to test whether canopy samples taken 20 years after road building show the same relative species abundances over time, and whether the distributions of species and genera among transects have changed.

4.7 ­Beetles: Life Attributes Have Led to Contemporary Hyperdiversity True beetles appear for the first time in the Triassic (ca. 240 mya). A marked radiation occurred in the Jurassic (210 to 145 mya), with the appearance of several families still in existence. Then, in the Cretaceous (145 to 65 mya), an incredible radiation occurred in parallel with the spread of angiosperm plants. Across a time span of 100 million years, beetles invaded all sorts of biotopes and habitats, including deep soil, caves, freshwater, and forest canopies (Fig.  4.14). Table 4.4 depicts the guilds represented in Neotropical rainforests (Lawrence and Britton 1994). To comprehend the true nature of Neotropical beetle diversity, a selection of the more hyperdiverse guilds will need to be explored in depth across the commonest

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Number of species

Arboreal Pulses

Canopy Super Specialists

Undercanopy Specialists + Climate Specialists

+ Climate Specialists

Forest Floor Specialists 90

0

90

Latitudinal and Altitudinal Pulses High Altitude Super Specialists

High Altitude Super Specialists

Tu Sp ndr ec a S ia up lis e ts r

Up

lan

d

Sp

ec

ial

l Up

s

S

Steppe / Desert Super Specialists Cave Specialists + Climate Specialists Forest Floor Specialists

Steppe / Desert Super Specialists Cave Specialists + Climate Specialists Forest Floor Specialists Cave Specialists

d

an

ist

ts

lis

ia

c pe

Fossorial Fossorial Specialists

90

r pe Su ts ra alis nd ci Tu Spe

Altitude

84

Waterside Generalists (highly vagile dispersants)

Cave Specialists

0

90

TIME

Figure 4.14  Taxon pulse model (Erwin 1979, 1985). Table 4.4  Beetle guilds. Microhabitat

Basic food sources

Guilds

Living vegetative surfaces

Leaves, flowers, cones, seeds, pods

Herbivores, predators, fungivores, pollinavores

Bark and wood surfaces

Wood, detritus

Borers, predators, fungivores, scavengers

Herbaceous plant tissues Stems, gall, and leaf interiors, roots,

Borers, herbivores, predators, fungivores

Leaf litter, ground debris Dead vegetation, rotting wood, decaying flowers and fruits

Predators, fungivores, scavengers, detritivores, seed‐predators

Animal nests

Dung, carrion, nest construction materials

Predators, fungivores, detritivores, scavengers

Caves

Carrion, algae

Predators, detritivores, scavengers

Soil

Worms, nematodes, bacteria, etc.

Predators, detritivores, scavengers

Fungi

Fruiting bodies, mycelia

Fungivores, predators,

Carrion

Carrion

Predators, detritivores, scavengers

Dung

Pass‐throughs

Predators, fungivores, scavengers, detritivores, seed‐predators

Littoral zone

Algae, debris, carrion, herbaceous plant tissues Predators, detritivores, scavengers

Lentic zones

Aquatic plants, detritus

Predators, detritivores, scavengers

4  Amazonian Rainforests

Amazonian biotopes and habitats in the Basin and its surroundings. New evidence, methods, and technology (McKenna and Farrell 2006) seem to support the taxon pulse model (Erwin 1979, 1985; Fig. 4.14) in demonstrating downtimes in the evolution of radiating beetles alternating with surge times. If this evolutionary process is connected to common regional Critical‐Zone events, and is thus synchronous across family‐group taxa, patterns can be discovered, processes discerned, hypotheses tested, and predictions made. If no connection exists to such common events, and the evolutionary process is asynchronous across family‐ group taxa, chaos theory must be brought to bear for explanatory insights.

4.8 ­Summary and Guide to Future Research, or “Taking a Small Step into the Biodiversity Vortex” A faunistic and floristic inventory can be an important and necessary tool for planning and creating protected areas (Fig. 4.5). Such inventories establish the basic information for monitoring community dynamics in space and time. Our study provides methodological information that could assist in the design and creation of protocols for entomofauna inventories in the Amazonian terra firme forests and elsewhere. We have demonstrated that it is possible to adequately sample insect family‐group taxa for a local area in a relatively short time, inexpensively, even in an area of incredible biodiversity. A series of fogging plots sampled rigorously across a region at various floristically determined locales, as in the case of Piraña and Tiputini, might better describe the apparent mosaic distribution of canopy and understory (e.g., in plants by Tuomisto et al. 2003, in birds by Terborgh et  al. 1990 and Blake 2007). To complement the fogging regime and sample for all terrestrial arthropod species and other organisms, larger and more diversely sampled

plots will be necessary. Geodatabasing and DNA barcoding will help to streamline future canopy‐sampling efforts. The results of canopy sampling from 1994 to 1996 hint at a variable degree of beetle‐species turnover across feeding guilds and across a forest mosaic within short distances. The distribution of beetle species in the Western Amazon Basin likely is arrayed in a mosaic or discontinuous pattern rather than being evenly distributed across the local landscape. How that pattern is shaped by the distribution of trees or whether it constitutes an oligarchy remains to be tested. Pitman et  al. (2001) predicted that the tree oligarchy pattern was driven by varying degrees of habitat specialization, particularly to soil type. With our present knowledge, we cannot say whether subtle forest, soil, or climatic differences, or perhaps something historical, accounts for the patterns we observed in species turnover or morphospecies richness. However, we predict that a central ecological factor driving beetle diversity patterns in Amazonian rainforest canopies is the level of tree‐host specificity (either as food or habitat) of adult and immature stages. If we accept the oligarchy hypothesis that the same suites of tree species and genera are found consistently throughout Amazonia at densities of at least one individual per hectare, then we predict that beetle lineages associated with those trees also are found in oligarchic hierarchies of taxa, probably at the level of genus or tribe. The taxonomic data further suggest that, over evolutionary time, beetle‐radiation patterns have been shaped by taxon pulses. Biodiversity research lies at the crossroads of taxonomy, ecology, and evolutionary biology. We need to combine experimental research on ecological and evolutionary mechanisms with taxonomic survey data to make more precise estimates of insect richness in Neotropical forests. Lists of morphospecies compiled via cursory observation of morphological characters or via DNA‐sequence variations are merely estimates of biorichness unless they are put into evolutionary context: that is, given names and classified. Biodiversity research requires

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­ hylogenetic perspective. Testing the oligarchy p hypothesis, or any hypothesis of insect community structure, is not possible without more alpha‐taxonomic work on Neotropical phytophagous insects. Proper use of molecular tools and geospatial databasing of museum‐ vouchered specimens along with sound alpha‐ taxonomy will allow the next generation of biodiversity scientists to monitor the effects of disturbances on Amazonian rainforests.

­Acknowledgments The following (in order of the number of times of participation) are those who treaded into the forest at 0300 hours to set up collection sheets and clear paths for operations, a truly dedicated bunch. First team (also includes substantial specimen sorting): Pablo E. Araujo, Ma. Cleopatra Pimienta, Sandra Enríquez, Fabian Bersosa, Ruben Carranco, María Teresa Lasso, Vladimir Carvajal, Ana Maria Ortega, Paulina Rosero, Andrea Lucky, Sarah Weigel, and Valeria Granda. Sometimes or one‐time field assistants (in alphabetical order): Mila Coca Alba, Gillian Bowser, Franklin, Paulo Guerra, Henry, Peter Hibbs, Amber Jonker, Pella Larsson, Keeta DeStefano Lewis, Jennifer Lucky, Ana Mariscal, Marinez Marques, Mayer, Raul F. Medina, Wendy Moore, Karen Ober, Monica O’Chaney, Kristina Pfannes, Mike G. Pogue, Wendy Porras, Theresia Radtke, Jennifer Rogan, Leah Russin, Mercedes Salgado, Linda Sims, Dawn Southard, George L. Venable, Joe Wagner Jr., and Winare. The following individuals provided all those important things in the museum that allowed production (in alphabetical order): Ma. Cleopatra Pimienta, Valeria Aschero, Gary H. Hevel, Jonathan Mawdsley, Mike G. Pogue, Linda Sims, Warren Steiner, George L. Venable, and Carol Youmans. Technical assistance: Grace P. Servat for assistance with the Sigma Plot program for graphing our results; Valeria Aschero for developing the initial GIS system for the Mordellidae; Rob Colwell for assistance with the EstimateS program; Karie Darrow for digital

image preparation; Charles Bellamy, Mary Liz Jameson, Paul Johnson, Jonathan Mawdsley, Brett Ratcliff, Paul Skelly, and Warren Steiner for generic determinations of some beetles used in our study. Grants: the following provided the essential funding to the National Museum of Natural History that allowed our study to happen: the Neotropical Lowland Research Project (Richard Vari, PI), the Department of Entomology, and the Casey Fund (Entomology). Field support from Ecuambiente Consulting Group SA in Quito, Ecuador, allowed the participation of several Ecuadorian students at Piraña Station, as well as logistics.

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Centro de Biodiversidad y Ambiente, Ecuador. 115 pp. Pitman, N. C. A., J. W. Terborgh, M. R. Silman, P. Nunez, D. A. Neill, C. E. Ceron, W. A. Palacios and M. Aulestia. 2001. Dominance and distribution of tree species in upper Amazonian terra firme forests. Ecology 82: 2101–2117. Pokon, R., V. Novotny and G. A. Samuelson. 2005. Host specialization and species richness of root‐feeding chrysomelid larvae (Chrysomelidae, Coleoptera) in a New Guinea rain forest. Journal of Tropical Ecology 21: 595–604. Porter, C. C. 1967. A revision of the South American species of Trachysphyrus (Hymenoptera: Ichneumonidae). Memoirs of the American Entomological Institute 10: 1–368. Price, P. W. 2003. Macroevolutionary Theory on Macroecological Patterns. Cambridge University Press, Cambridge, United Kingdom. 302 pp. Salo, M. and A. Pyhala. 2007. Exploring the gap between conservation science and protected area establishment in the Allpahuayo‐ Mishana National Reserve (Peruvian Amazonia). Environmental Conservation 34: 23–32. Samways, M. E. 2009. Reconciling ethical and scientific issues for insect conservation. Pp. 547–559. In R. G. Foottit and P. H. Adler (eds). Insect Biodiversity: Science and Society. Wiley‐Blackwell Publishing, Chichester, United Kingdom. Schulman, L., K. Ruokolainen, L. Junikka, I. E. Saaksjarvi, M. Salo, S. K. Juvonen, J. Salo and M. Higgins. 2007. Amazonian biodiversity and protected areas: do they meet? Biodiversity and Conservation 16: 3011–3051. Spangler, P. J. and S. Santiago. 1987. A revision of the Neotropical aquatic beetle genera Disersus, Pseudodisersus, and Potamophilops (Coleoptera: Elmidae). Smithsonian Contributions to Zoology 446: 1–40. Staines, C. L. and C. Garcia‐Robledo. 2014. The genus Cephaloleia Chevrolat, 1836

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(Coleoptera, Chrysomelidae, Casidinae). ZooKeys 436: 1–355. Terborgh, J., S. K. Robinson, T. A. Parker, C. A. Munn and N. Pierpont. 1990. Structure and organization of an Amazonian forest bird community. Ecological Monographs 60: 213–238. Tuomisto, H., K. Ruokolainen and M. Yli‐Halla. 2003. Dispersal, environment, and floristic variation of western Amazonian forests. Science 299: 241–244.

Valencia, R., R. B. Foster, G. Villa, R. Condit, J. C. Svenning, C. Hernandez, K. Romoleroux, E. Losos, E. Magard and H. Balslev. 2004. Tree species distributions and local habitat variation in the Amazon: large forest plot in eastern Ecuador. Journal of Ecology 92: 214–229. Weiblen, G. D., C. O. Webb, V. Novotny, Y. Basset and S. E. Miller. 2006. Phylogenetic dispersion of host use in a tropical insect herbivore community. Ecology 87: S62–S75.

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5 Insect Biodiversity in the Afrotropical Region Clarke H. Scholtz and Mervyn W. Mansell Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa

The Afrotropical region is renowned for its charismatic megafauna and diverse botanical wealth, but these aspects are overshadowed by the sheer diversity of insects that occupy the continent of Africa and its associated islands. The entomofauna of this zoological realm presents enormous challenges to scientists because of the profusion of insect taxa that have evolved in the multitude of ecological systems of the region and because of historical and sociopolitical issues that afflict the continent. Insects and other invertebrates drive the ecosystems on which the megafauna and flora and, ultimately, humans depend. Vertebrate animals depend on ecosystems for survival, and terrestrial ecosystems depend on insects for their establishment and maintenance. Insects provide numerous primary environmental services, from recycling nutrients to pollination, besides their fundamental contribution to the food resources of many vertebrate animals. Insects, consequently, should be at the core of any country’s commitment to the International Convention on Biodiversity. Africa’s rich biodiversity, however, is not matched by its economic wealth, as it has the dubious distinction of being home to most of the world’s poorest nations. A discussion of insect biodiversity science, consequently, should be seen in this context. The few studies undertaken so far on African insect biodiversity (e.g.,

Miller and Rogo 2001) have arrived at similar conclusions: species numbers are vast but not accurately known; insect habitats are fast declining; few African countries house insect collections or employ taxonomists (Table 5.1); and if collections of African insects exist, they are housed in foreign museums, either those of the ex-colonial powers, mostly in Europe, or those based on more recent collections such as some in the United States (Table 5.2). No collections have been returned to the countries from which the insects were collected, but some foreign countries, such as Belgium, that have African collections are preparing to repatriate the information. We believe that before poor countries start to recognize the importance of insect biodiversity studies, they need to be convinced of the material benefit of such research. Insects have direct, easily understandable value, as well as less tangible value, in poor countries. Examples of insects with direct value are those harvested for food (e.g., mopane caterpillars in large parts of southern Africa, termite alates and locusts over much of the continent, and Ephemeroptera in the Rift Valley lake systems) and those that produce useful products (e.g., honey and silk from native silk worms). Examples of insects with less tangible value include pollinators, pest-control agents, and biodegraders in the form of dung beetles, termites, and flies. Furthermore, insects are

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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Table 5.1  Major entomological collections in the Afrotropical region (based on Miller and Rogo 2001). Country

City

Institution

Angola

Dundo

Museu do Dundo

Kenya

Nairobi

National Museums of Kenya

Mozambique

Maputo

Museum Nacionale de Mozambique

Namibia

Windhoek

State Museum of Namibia

Senegal

Dakar

Institut Fondamental d’Afrique Noire

South Africa

Cape Town

Iziko Museums

South Africa

Grahamstown

Albany Museum

South Africa

Pietemaritzburg

Natal Museum

South Africa

Pretoria

Plant Protection Research Institute

South Africa

Pretoria

Transvaal Museum

Uganda

Kampala

Kawanda Research Station

Zimbabwe

Bulawayo

Natural History Museum

Table 5.2  Some major entomological collections of Afrotropical insects outside Africa (based on Miller and Rogo 2001). Country

City

Institution

Austria

Vienna

Naturhistorisches Museum Wien

Belgium

Brussels

Institut Royal des Sciences Naturelles

Belgium

Tervuren

Royal Museum of Central Africa

Denmark

Copenhagen

Copenhagen Museum

France

Paris

Museum National d’Histoire Naturelle

Germany

Berlin

Museum für Naturkunde der Humboldt-Universität

Germany

Munich

Staatssammlungen der Bayerischen Staates

Hungary

Budapest

National Museum

Italy

Florence

Centro di Studio per la Faunistica ed Ecologia Tropicali

Spain

Barcelona

Barcelona Museum

Sweden

Lund

Lund University Museum

Sweden

Stockholm

Naturhistoriska Riksmuseet

United Kingdom

London

The Natural History Museum

United Kingdom

Oxford

Hope Museum

United States

Chicago

Field Museum

United States

New York

American Museum of Natural History

United States

Pittsburgh

Carnegie Museum

United States

San Francisco

California Academy of Science

United States

Washington

Smithsonian Institution

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crucial elements of the food chain for fish, the most important source of animal protein for humans in large parts of Africa. By contrast, some insects have negative effects as vectors of disease agents and as agricultural pests, and these taxa also require further study and monitoring. Miller and Rogo (2001) reviewed some of the aspects of insect biodiversity science in an excellent synthesis of African and Afrotropical insect diversity. They set the scene by highlighting the richness of insects in the region (more than 100,000 described species) and their potential for sustainable use if comprehensively understood and documented. They also provided a detailed background to current and historical resources, including a list of institutions in Africa, Europe, and the United States that hold collections of Afrotropical insects. They emphasized the difficulty of locating specimens and literature references, and provided a preliminary list of resources where such information could be obtained. Most importantly, they highlighted a series of challenges that face insect biodiversity science in Africa, which they had identified in an earlier study (Miller et al. 2000). Miller et  al. (2000) proposed a biodiversity plan for Africa, with three main components: (i)  an information-management program to organize and make available the large volume of data that already exists but is not generally accessible; (ii) a series of field projects to evaluate the use of insects as indicator organisms and to quantify their roles in ecosystem processes; and (iii) training and participatory technology transfer. To these, we add two more components: (iv) an emphasis on Africa as the center of biodiversity of many higher insect taxa, with examples of sentinel groups; and (v) the identification of insects with potential to become major, Africa-wide pests, and training appropriate taxonomists to identify them. We will develop these points further. The purpose of the current chapter is not to repeat the information provided by Miller et al. (2000), but to try to address some of the questions they raised and challenges they identified,

and to add new insights into African b ­ iodiversity science by means of insect groups with which we are familiar.

5.1 ­What Do We Know about Afrotropical Insects? All insect orders are present in Africa. The recently described order Mantophasmatodea (Klass et al. 2002), whose extant representatives are known only from Africa, was reclassified with the Grylloblattodea, and both are now considered suborders in the order Notoptera (Arillo and Engel 2006), eliminating the once-unique African order. Despite the insect richness, few taxa have been collected extensively and even fewer have been studied comprehensively; those that have been studied have mostly been studied outside Africa. South Africa is the one exception, with reasonable collections and a history of taxonomic research. Table 5.1 provides a list of African museums with reasonably well-maintained and well-curated collections. This situation, however, reflects the poor state of affairs; only eight countries, of more than 50, have museums housing insect collections. It is a barometer of the state of insect taxonomic exploration in Africa.

5.2 ­An InformationManagement Program The most immediate challenge to understanding and applying Africa’s insect biodiversity lies in documenting new data, including the description of species, and in the collation of taxonomic and biological data in existing historical resources and their coordination with preserved specimens in institutions scattered throughout the world. This major issue was raised by Miller and Rogo (2001) when they posed the question: “But how can these resources be unlocked to make information readily available for use?” An attainable solution now exists to this challenge.

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Vast amounts of African specimen-related data are incarcerated in the biological collections of the world, but the information has been difficult to access because of logistical and physical constraints. These constraints include the disparate nature of collections and the time and expense involved in visiting different museums in many parts of the globe. The challenge lies in the development of a system to assemble and collate data from many sources, with the simultaneous incorporation of burgeoning new information. Until now, conventional filing systems, such as card catalogs and accession registers, were unable to accommodate the vast amount of potential data or its collation across multiple platforms  –  from specimen data to taxonomy, historical literature references, geographical distributions, phenology, host plants, molecular data, and graphics, to name but a few relevant parameters. Electronic computerization did not initially resolve these issues because complex and expensive programming put these resources beyond the reach of most biologists, and personal computers were initially compromised by software limitations. The advent of relational databases, based on mathematical concepts (Codd 1970), has now placed powerful resources within reach of all biologists. Relational database management systems (RDBMSs), such as Microsoft Access and My SQL, enable biologists to design systems to record and collate vast amounts of taxonomic and other data within highly flexible and adaptable applications that are universally standard and easily understood. Relational databases, consequently, have become the cornerstones of sound curatorial practice, information exchange, and dissemination in many museums and collections, and considerable advances have been made in this field. The advantages of virtual, electronically collated collections data are obvious, as numerous products can be generated that advance the relevance of museum collections and justify their continued accrual and maintenance. Products that can be generated from well-designed and integrated relational databases include faunal inventories, distribu-

tional data for conservation applications and environmental impact assessments, geographical information system (GIS) modeling (e.g., climate change modeling, conservation-area selection, and mapping of biodiversity hotspots and endemicity), host-plant associations and disease vectors for application in agriculture, and development of web-based products, as well as printed catalogs and capacity building (e.g., student training). Added advantages include large amounts of instantly available, integrated data and electronic databases that are also virtual collections of specimens, providing a backup of the collection in case of disaster. The establishment of the Global Biodiversity Information Facility (GBIF), Species 2000, and other international initiatives has brought databasing into sharp focus because the electronic recording of specimen and taxonomic data are fundamental to the objectives of these international programs. Database activities in the African context are sporadic or non-existent, and many institutions are hesitant to embark on programs because of the perceived enormity of the task or reluctance to provide public access to their data. A general misconception is that specimen data in collections are a marketable resource that belongs strictly to a particular institution. This attitude is a major impediment to documentation of the African insect fauna because such data remain beyond the mainstream flow of biodiversity information and are essentially irrelevant and increasingly difficult to justify in terms of maintenance expenses. This parochial attitude is further negated by current accessibility to substantial funding for the electronic recording of museum specimens from GBIF and the South African Node of GBIF, the South African Biodiversity Information Facility (SABIF). In addition, a major participant in the enhancement of electronic documentation of Africa’s biodiversity resources has now emerged in the form of the Seattle-based JRS Biodiversity Foundation. The initial focus of JRS on documentation of African biodiversity is greatly enhancing and

5  Insect Biodiversity in the Afrotropical Region

a­ccelerating the ­electronic recording of data that have long been inaccessible in numerous collections in Africa and Europe. This documentation support is, in turn, leading to further enhancement of data beyond the initial and essential exercise of data-capture. These enhancements include areas such as molecular analysis, GIS modelling and the application of the data to biodiversity training and information dissemination through web pages. The South African National Collections of Insects and Arachnids of the Agricultural Research Council (ARC) and the University of Pretoria are among the leading institutions in Africa with regard to progress in the databasing of invertebrate collections. The most extensive data set, although not strictly of insects, is the African Arachnid Database (AFRAD), which now includes more than 6000 taxonomic records that can be viewed on the ARC website. This initiative also has attracted substantial funding and is a collaborative program with the newly established South African National Biodiversity Institute (SANBI). Substantial progress also has been made in the electronic recording of the insect collections, with comprehensive data sets available for African Tephritidae (fruit flies), isopterans (termites), Megaloptera (alderflies and fishflies), and Neuroptera (lacewings and relatives), and steadily increasing electronic documentation of  other groups including Scarabaeoidea (Coleoptera), Sternorrhyncha (Hemiptera), Thysanoptera, and Apoidea and Chalcidoidea (Hymenoptera). The Scarabaeoidea, Apoidea, and Neuroptera, in particular, have been major beneficiaries of JRS support, which far outweighs local funding resources for electronic data recording. In this respect, support from JRS is now a major factor in the documentation of these three groups. The Neuroptera data set can be used as an example of the manner in which data are recorded, collated, and disseminated for application in fields including biological control and pollination biology (agriculture), conservation biology, and biogeography, as well as

fundamental scientific research. This database ­comprises several discrete databases – ­specimens, taxonomy, localities, institutions, persons, and bibliographies  –  that are interlinked through key fields. This arrangement facilitates simultaneous queries across multiple platforms that are designed to answer specific questions. The database also accommodates hyperlinks to graphics and to PDF files of associated literature, ensuring that all historical and current resources pertaining to specimens (in all museums), taxonomy, and literature, as well as associated persons and graphics, can be accommodated in one reference source. This information can be translated directly into searchable web-based products and electronic and paper catalogs. The intended first product is a Catalogue of Lacewings (Neuroptera) of the Afrotropical Region, accessible through the GBIF portal. This was a GBIF-funded initiative, and the results also will be published in hard-copy through SANBI. The JRS funding is contributing significantly to enhancing this initiative and to the development of web pages pertaining to the Scarabaeoidea. Another of the constraints that a database program is designed to address is the compilation of catalogs of additional insect groups. Such catalogs form the basis of research on all biological organisms. At present, only two comprehensive catalogs are available for entire orders of Afrotropical insects. The first, Catalogue of Diptera of the Afrotropical Region (Crosskey 1980), is now more than 35  years out of date and not available in electronic format. The second, Catalogue of Lacewings (Neuroptera) of the Afrotropical Region, is currently only available in electronic format. The advantages of electronic catalogs are that they accommodate continual updates, so the data remain current. The advent of GBIF and SABIF, and now JRS, has provided further incentives and facilities to produce such catalogs. Compilation of catalogs requires a distillation of all published information on a particular taxon and a realistic, current assessment

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of the status and extent of knowledge of a ­particular group, often with remarkable consequences. In the compilation of the Afrotropical lacewing catalog, the number of valid species of Neuroptera described from the Afrotropics has decreased considerably. For example, in the Chrysopidae, one of the largest families of Neuroptera, 286 species have been described, but only 183 of these names are valid, reducing the number of described, valid species by 103 (36%, or more than one-third). Sixty-seven of these synonyms were created by a single author, the Spanish cleric Longinos Navás (1858–1938). The legacy of Navás and several other early authors of Afrotropical lacewings left a trail of taxonomic confusion that continues to impede progress toward an accurate assessment of the Neuroptera of this region. The number of taxonomic names lost to synonymy will be offset by new discoveries, but before most of these descriptions are possible, all existing names have to be checked thoroughly against type specimens, many of which have been destroyed, lost, or deposited in obscure collections. These constraints limit real progress and affect many other insect groups as well. On the positive side, the advent of electronic web documentation of lacewing taxa and literature, particularly by John D. Oswald of Texas A&M University (http://lacewing. tamu.edu/SpeciesCatalog/References) has greatly facilitated research on lacewings by concentrating all literature and taxonomic names into convenient reference sources. This project has been a major contribution to research on Afrotropical lacewings, further emphasizing the need to encourage sound taxonomic procedures and ongoing electronic documentation and dissemination. The prevailing situation for the lacewings substantiates claims by Scholtz and Chown (1995) that total insect numbers for southern Africa (but extrapolated to the whole of Africa) are unlikely to change significantly over what is currently known because synonymy more or less compensates for new species described.

5.3 ­The Role of Insects in Ecosystem Processes and as Indicators of Environmental Quality – Dung Beetles as a Case Study The principal importance of dung beetles lies in their maintenance of pasture health by burying dung, which has the effect of removing surface wastes, recycling the constituent nutrients, and reducing exposure of livestock to internal parasites. Negative environmental effects that result from a lack of dung beetles were seen in Australia before the introduction of dung beetles adapted to cattle dung. These effects included the loss of grass cover due to the persistence of unburied dung pads, the growth of unpalatable grass around these pads, the leaching of nutrients in surface rainwater runoff, and the buildup of large populations of dung-breeding flies (Waterhouse 1974). Much of the traditional farming in most of Africa is of a subsistence nature, based on small areas of planted crops per household and on livestock including camels, cattle, donkeys, goats, horses, pigs, and sheep, which graze on communal land by day and are penned at night. Human sewage is often deposited near villages and is removed by dogs, pigs, and dung beetles. Cattle are conservatively estimated to number about 100 million in Africa, while small livestock such as sheep and goats probably number three times more. Considerably smaller numbers of beasts of burden are found, mainly in regions with a long tradition of association between them and their owners. All of these animals, however, produce dung. Camel and cattle dung is collected, usually during the dry season, from the field or from the pens where the animals spend the night. It is dried and used as fuel for fires in regions where trees have been destroyed and, in rehydrated form, as building material. In some areas, dung from accumulations in livestock pens is used as fertilizer in crop fields. Although the total quantities of dung produced or the amount used for fuel,

5  Insect Biodiversity in the Afrotropical Region

mortar, or fertilizer is impossible to estimate, a safe estimate is that the dung produced by day while the animals are out grazing contributes about half the total. Because we have a reasonable estimate of cattle and small livestock numbers in Africa, and the amount of dung they produce is known, we can calculate the amount of dung available to dung beetles for feeding and breeding, activities that greatly enhance soil nitrogen, soil porosity, and water penetration (Losey and Vaughan 2006). Cattle produce, on average, about 9000 kg of dung per animal each year. If we assume that half of this dung is collected and used for fuel, mortar, and fertilizer, about 4500 kg per animal remains on the ground. If this amount is multiplied by 100 million cattle, we are presented with the staggering amount of 450 million metric tons of dung deposited on the continent per year. Sheep and goats each produce about 900 kg of dung per year, and if the same algorithm based on a number of about 30 million small livestock units is applied for calculating the amount returned to the soil, the total amount is about 135 million metric tons. Add to this the dung produced by humans, as well as their pigs, dogs, and beasts of burden, and the total is immense. Indicators of environmental quality in agroecosystems have received considerable attention in recent years (Riley 2001). Although an acceptable framework for their application is still lacking due to various degrees of incompatibility among different systems, the use of indicators remains desirable as a basis for managing agroecosystems. Here we describe and review the role of the scarabaeine (Scarabaeidae: Scarabaeinae) dung beetles as agricultural indicators. One of the uses of dung beetles as indicators is the defining of biogeographical regions and faunal distribution centers to facilitate and validate comparisons among species assemblages in natural and intensively farmed systems. This approach has been conducted in some detail in South Africa (Davis 1993; Davis et  al. 1999, 2002a, 2004; Davis and Scholtz 2004). A second

use of dung beetles is the characterization of pasturage from natural to heterogeneous to completely transformed (Davis et al. 2004). In a review of terrestrial insects as bioindicators, McGeoch (1998) recommended a ninestep protocol for assessing the value of the insect group. These nine steps can be reduced to three steps, assessing (i) the category (biodiversity, ecological, or environmental) and scale (regional or local) of indication, (ii) the specific objectives of the application, and (iii) the data collection and rigorous statistical testing of the group to ensure that it fulfills the study objectives and permits well-supported decision making. Scarabaeine dung beetles are an obvious choice as indicators because they are an integral part of livestock pasture ecology in the warmer, moister climatic regions where they are centered. These regions are situated within the 45 ° latitudinal limits in areas receiving more than 250 mm of annual rainfall and subject to mean annual temperatures greater than 15 °C. The rainfall limit for dung beetles is also roughly the limit for the growth of pasturage suitable for cattle, although small livestock survive in drier areas. 5.3.1  Dung Beetles as Indicators of Regional Biodiversity

Biogeographical differences among regions can be defined by comparing data on species richness, taxonomic composition, and speciesabundance structures of local assemblages (Davis 1997; Davis et  al. 1999, 2002a, 2004). Such differences are usually related to climatic factors, although edaphic and vegetational characteristics also vary at a regional scale: for example, in rainforests, winter-rainfall shrublands, and deep desert sands. Whereas vegetation largely depends on climate, edaphic factors can be independent of climate. Analysis of such data permits one to determine natural regional boundaries, define the distribution centers of groups of species, and identify centers of endemism.

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A global comparison of 46 widely separated local faunas provides insight into some subcontinental patterns (Davis et al. 2002b). Parsimony analysis of endemism, using these data, suggests subcontinental centering according to ecoclimatic zones, primarily forest, woody savanna, highland grass, and arid or winter-rainfall climate. 5.3.2  Dung Beetles as Indicators of Habitat Transformation

Dung beetles are useful indicators of effects related to local transformation from natural habitat to farmland. The consequences are related primarily to modification of natural vegetation (Estrada and Coates-Estrada 2002, Halffter and Arellano 2002) and the loss of indigenous mammals, particularly large monogastric species that void large fibrous droppings. To conserve local biodiversity in a heterogeneous environment, sufficiently large fragments must remain to support specialists, to maximize species richness, and to maintain pasture health. However, the reality is a heterogeneous system comprising reserves, naturally farmed patches, and intensively farmed areas in various proportions. Relative naturalness can be categorized by surveying differences in dungbeetle assemblages between reserves and natural to disturbed farm habitats.

5.4 ­Africa-Wide Pests and Training Appropriate Taxonomists – Fruit Flies as a Case Study Insect pests account for about 50% of crop losses in Africa, from plant establishment through plant growth, crop maturation, and storage. Fruit flies are some of the world’s most devastating crop pests, causing millions of dollars in production loss each year. In Africa, many species attack fruits, vegetables, and native hosts. These pests include at least 12 species that are endemic to Africa, including the

world’s worst fruit pest, Ceratitis capitata, the Mediterranean fruit fly or medfly. Fruit flies not only constrain fruit export from Africa, but also cause extensive crop losses that severely affect sustainable rural livelihoods and food security in many impoverished regions of Africa. Four species of Asian fruit flies have invaded Africa and are of particular concern.  Bactrocera dorsalis (formerly Bactrocera invadens) and Bactrocera cucurbitae are now widespread in Africa and are devastating pests that attack a wide variety of fruit and vegetable crops, including citrus, guava, mango, and tomato, as well as a large number of indigenous hosts. Of the other two invasive species, Bactrocera zonata (peach fly) is currently known only from Egypt and Mauritius, and Bactrocera latifrons (solanum fly) was recently detected in Tanzania and Kenya. The African Fruit Fly Initiative (AFFI) was established at the International Centre of Insect Physiology and Ecology (ICIPE), Nairobi, Kenya, to address the above concerns (Ekesi and Billah 2007). The program is designed to cover a number of aspects, including surveys and monitoring, development of control methods, training of scientists and agricultural personnel in the identification and management of fruit flies, and information and support for small-scale farmers. During the initial phases, traps and lures were provided to several countries, especially the East African community of Kenya, Tanzania, Uganda, and Zanzibar. This initial survey was responsible for the first detection in Africa of the highly invasive B. dorsalis (Lux et al. 2003), subsequently described as a new species, B. invadens (Drew et  al. 2005), but recently synonymized with B. dorsalis by Schutze et  al. (2015). The invasion has resulted in a pest that is proving far more destructive and invasive than is C. capitata, and is now cause for major concern from quarantine and food security perspectives. These invasive species are comprehensively documented by De Meyer et al. (2014) in an active website hosted by the Royal Museum for Central Africa, Tervuren, Belgium. Training courses also have been

5  Insect Biodiversity in the Afrotropical Region

­rovided by the AFFI, and a comprehensive p manual entitled A Field Guide to the Manage­ ment of Economically Important Tephritid Fruit Flies in Africa has emanated from the program (Ekesi and Billah 2007). Surveys to detect and monitor fruit flies are now in progress in Africa. These have been initiated by the United States Department of Agriculture Animal and Plant Health Inspection Service (USDA-APHIS) Pretoria office and Trademark Southern Africa (TMSA), which have provided financial and technical support. Few professionally competent taxonomists, however, are available to provide identifications of flies detected in these surveys. With one exception, Africa depends on specialists in Britain and Europe for taxonomic expertise to underpin fruit fly research on the continent. Training of tephritid taxonomists beyond the parataxonomic level is, consequently, an urgent priority for fruit fly research and management in Africa. Apart from the countries surveyed by the AFFI, Benin, Botswana, Ethiopia, Malawi, Mozambique, Namibia, Senegal, South Africa, Swaziland, Zambia, and Zimbabwe now conduct regular monitoring programs mostly supported by USDA-APHIS and TMSA. Urgent attention now is focused on the invasive species, in particular B. dorsalis. This species is destined to have a major effect on fruit and vegetable production in Africa and ultimately on sustained agricultural production on the continent. Ideally, intensive continent-wide programs should be launched to monitor the spread of this and other pest species and to inform agricultural authorities of its presence and threat to their countries. Once again, the AFFI has been proactive in this regard, with a major proposal for funding having been submitted to the Food and Agriculture Organization of the United Nations to deal with the threat posed by the invasive species. 5.4.1  Invasive Species of Concern in Africa

Bactrocera dorsalis (Hendel) (= B. invadens), the invader fly, is native to Sri Lanka, but recently

invaded Africa and spread rapidly across the continent and the Comores Islands. Since its first detection in Kenya in 1993 (Lux et  al. 2003), B. dorsalis has spread to most countries in Africa and infests at least 31 host plants. Bactrocera dorsalis belongs to a complex of superficially similar Oriental species. Three members of this “dorsalis” complex are serious to extremely devastating pests, whereas other members of the complex are fairly benign. Distinguishing the species requires the services of an experienced taxonomist. Bactrocera dor­ salis attacks a wide range of hosts, including citrus, guava, mango, papaya, and the wild hosts Strychnos and especially marula (Sclero­ carya birrea). It also infests cashew nuts. The potentially wide host range also makes it a dangerous invasive species, further exacerbated by its aggressive behavior, whereby indigenous species are displaced and multiple ovipositions can occur in one fruit. Males are attracted to methyl eugenol. Bactrocera cucurbitae (Coquillett), the melon fly, is native to Asia, but has been introduced into Africa and is currently known from Egypt, Kenya, Malawi, Senegal, Tanzania, and Zambia, as well as Mauritius and Réunion. Bactrocera cucurbitae is a serious pest of the Cucurbitaceae, but has been reared from more than 125 species of plants, including many non-cucurbits such as avocado, beans, fig, granadilla, jackfruit, mango, papaya, peach, quince, tomato, and tree tomato. The potentially wide host range makes this invasive species a dangerous pest. Males are attracted to cue lure. Bactrocera (Bactrocera) zonata (Saunders), the peach fruit fly, has extended its range from Asia and is currently known from Egypt and Mauritius in the Afrotropical region. It attacks many crops including apple, bitter gourd, citrus, date palm, guava, mango, papaya, peach, pomegranate, quince, tropical almond, and watermelon. The wide host range and the danger of the species spreading southward from Egypt make it a serious potentially invasive species in Africa. Males are attracted to methyl eugenol.

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Bactrocera (Bactrocera) latifrons (Hendel), the solanum fruit fly, only recently has been detected in Tanzania, on eggplant, and is currently known only from Tanzania. Two species, B. dorsalis and B. zonata, are morphologically similar to, and easily confused with, B. latifrons. An adventive population of B. latifrons is known from Hawaii, and the species also is known from China, India, Laos, Malaysia, Pakistan, Sri Lanka, Taiwan, and Thailand. It is mainly a pest of solanaceous crops, but the known host list includes Baccaurea motleyana (rambai), Capsicum annuum (chilli), Lycopersicon escu­ lentum (tomato), Lycopersicon pimpinellifolium (currant tomato), Malus domestica (apple), Solanum incanum, Solanum melongena (eggplant), Solanum nigrum (black nightshade), Solanum sisymbriifolium, and Solanum torvum (terongan). A new lure, latilure, has been developed as an attractant of this fly. 5.4.2  African Indigenous Fruit Flies of Economic Importance

Ceratitis (Ceratitis) capitata (Wiedemann), the Mediterranean fruit fly or medfly, is native to Africa and has become one of the world’s most notorious crop pests. It has spread into many parts of the world, and adventive populations occur in all continental regions except tropical Asia and North America, where it has been eradicated several times. Millions of dollars are spent annually in preventing establishment in North America. It is also present on most Indian Ocean islands and on Hawaii. The species has an extensive host range (White and ElsonHarris 1992) and is particularly injurious to tropical and subtropical fruits. Males are readily attracted to trimedlure and terpinyl acetate. Ceratitis (Pterandrus) rosa Karsch, the Natal fruit fly, is a major pest species that can be as devastating as the medfly in areas where it occurs. It is native to southern and eastern Africa, extending as far north as southern Kenya. Adventive populations exist in Mauritius and Réunion. It is also a major pest of tropical and subtropical fruits. White and Elson-Harris

(1992) provided an extensive host list. Males are attracted to trimedlure and terpinyl acetate. Ceratitis (Pterandrus) fasciventris Bezzi previously has been confused with C. rosa, and many country records for the Natal fruit fly are actually of this species. It replaces C. rosa in western Kenya, across to western Africa, and has a similar host range. Males are attracted to trimedlure and terpinyl acetate. Ceratitis (Pterandrus) anonae Graham is a western African species with an extensive host range (White and Elson-Harris 1992). No effective lure is available for this species. Ceratitis (Ceratalaspis) cosyra (Walker), the marula fruit fly, is widespread in eastern Africa, as is its native host, marula. The marula fruit fly has a more limited host range than do other Ceratitis species, but it is, nonetheless, a serious pest of mango. It is attracted to terpinyl acetate but not trimedlure. The above Ceratitis species have a vast collective range of cultivated and wild hosts. They are all serious pests of mango and other tropical and subtropical fruits. Mango is a sentinel crop in Africa, both in terms of export potential and sustainable livelihoods, and many rural families depend on this fruit as an essential component of their diet. These Ceratitis pests, now exacerbated by the invasive species, are a constraint to agricultural development and food security in Africa. A number of African Dacus species, including Dacus (Dacus) bivittatus (Bigot) (pumpkin fly), Dacus (Didacus) ciliatus Loew (lesser pumpkin fly), Dacus (Didacus) frontalis Becker, and Dacus (Didacus) vertebratus Bezzi (jointed pumpkin fly), infest a wide range of the Cucurbitaceae. They are more limited in their host ranges than are the Ceratitis species, but they, nonetheless, have a similar effect on rural agriculture and food security. Cucurbitaceae are widely cultivated and are an important dietary component in many African countries, and are used extensively as container gourds in many rural households. Bactrocera (Daculus) oleae (Gmelin), the olive fly, is a unique pest because of its stenophagous

5  Insect Biodiversity in the Afrotropical Region

host range, which is limited to olives (Olea). It is widely distributed in Africa and has spread throughout the olive zone of the Mediterranean. The larvae not only affect the quality of table olives, but also can reduce the quality of the oil if the fruits are stored for a long period (White and Elson-Harris 1992). Trirhithrum nigerrimum (Bezzi) and Trirhithrum coffeae Bezzi, the coffee flies, are also widespread in Africa and are major pests of coffee, constraining the cultivation and export of coffee from the continent. They consequently impede the generation of export revenue in several coffee-producing African countries.

5.5 ­Sentinel Groups The Afrotropical region is the second most species-rich zoogeographical region in the world (Cowling and Hilton-Taylor 1994). Despite this level of focused biodiversity, exploration for insects has been almost minimal for most countries, and few invertebrate groups are well known across the entire region. The only available catalogs encompassing complete orders of Afrotropical insects are for the Diptera and Neuroptera. The Catalogue of Diptera of the Afrotropical Region (Crosskey 1980) was not based on dedicated surveys for Diptera throughout the region, but rather on serendipitous collection records and publications. The Catalogue of Lacewings (Neuroptera) of the Afrotropical Region suffers from the same deficiencies as the Diptera catalog, with regard to most African countries, although a dedicated long-term survey for lacewings has been carried out in the southern African subregion as part of the Southern African Lacewing Monitoring Programme (Mansell 2002). Further comprehensive collecting was done during the Belgian colonial period in what is now the Democratic Republic of Congo, and these extensive collections are housed in the unique Royal Museum for Central Africa in Tervuren, Belgium, an invaluable resource for the study of Afrotropical lacewings and other African insects. Sporadic

contributions were made during the colonial era of many African countries, but all material from these collections is deposited in museums in Europe and can be accessed only at great expense by scientists from Africa. Besides Tervuren, museums that hold significant collections of African lacewings include The Natural History Museum, London; Museum National d’Histoire Naturelle, Paris; Naturhistorisches Museum, Vienna; Humboldt University Museum, Berlin; Copenhagen Museum; Lund University Museum; and Barcelona Museum. Crucial collections were destroyed along with the Hamburg Museum during the Second World War. Several of these collections, which house critical type material, were also inaccessible to South African scientists for several decades, for political reasons, which severely hampered progress in the documentation of Afrotropical insects. 5.5.1 Neuroptera

The orders Neuroptera and Megaloptera are comparatively well known in the Afrotropical region, especially in the southern African subregion, and can be used as an example to highlight further key issues in the exploration of Afrotropical insects. Thirteen of the 18 families of Neuroptera and both families of Megaloptera occur in the Afrotropics; however, the Megaloptera occur only in South Africa and Madagascar. The Afrotropical region is the richest zoogeographical region in the world for these insects, and the southern African subregion is especially rich: all 15 families are represented in the area south of the Zambezi and Cunene Rivers. The Neuropterida fauna of this area, and of South Africa in particular, manifests distinct geographical trends. An eastern fauna comprises taxa that occur in central and eastern Africa and extend their geographical range along the eastern tropical corridor into South Africa. The western fauna occupies the Cape Provinces of South Africa, Namibia, and western Botswana, with almost 90% of the species being endemic to this area.

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Two groups of lacewings, the family Nemop­ teridae and the tribe Palparini (Myrmeleont­ idae), have undergone extensive speciation in southern Africa, whereas the related order Mega­loptera is represented by a unique relict fauna that extends along the eastern mountain ranges from the Cedarberg, Western Cape Province, to the northern Drakensberg in Limpopo Province, South Africa. The Cape Provinces and Namibia harbor 62 of the world’s known fauna of 142 species of Nemopteridae, and 47 of these are Cape endemics. If endemic species awaiting description are included, South Africa harbors more than half of the species of Nemopteridae in the world. Extensive, dedicated surveys have facilitated these assessments, which are aimed at evaluating the conservation status of southern Africa’s lacewings. These surveys have revealed the precarious existence of this unique lacewing fauna, which is severely threatened by burgeoning habitat destruction through urbanization and agriculture. The massive radiation of the Nemopteridae in southern Africa, and in the Western and Northern Cape Provinces especially, undoubtedly has been driven by parallel evolution with the vast Cape flora. All adult nemopterids are obligate pollen feeders, and evidence is increasing that many of the endemic taxa are pollinators of specific plants. The relationship between these pollinators and plants raises conservation concerns because many of the plant communities are equally threatened, highlighting the value of extensive surveys, elucidation of the biology of the species, and conservation assessments. The tribe Palparini includes the largest and most spectacular of all antlions, with wingspans up to 17 cm. All are characterized by beautifully patterned wings, the patterns having evolved as camouflage to protect these large insects from predation. Although most species are nocturnal, their wing patterns provide protection during diurnal resting among plants (Mansell and Erasmus 2002). Currently, 100 valid species of Palparini are distributed throughout the Afrotropical, Oriental, and southern Palearctic

regions, but are absent, without vestige, from the extensive Australasian region and the western hemisphere, indicating a post-Gondwana radiation. Of the 100 species, 45 occur in southern Africa, with 35 being endemic to the area. The unique vegetation and biomes of southern Africa are thought to have influenced the extensive radiation of the Palparini in the southern subcontinent. 5.5.2  Dung Beetles (Coleoptera: Scarabaeidae: Scarabaeinae)

The Afrotropical region is home to roughly half of the world’s genera and species of dung beetles, and most of the tribes are centered in, or restricted to, the region. This distribution pattern can be attributed to evolutionary history and to the suitability of two principal ecological factors that influence tribal, generic, and species distribution patterns (Davis and Scholtz 2001, Davis et al. 2002b). These factors comprise suitable climate and the number of dung types. At species and generic levels, a strong correlation exists between the richness of dung beetle taxa and the area of suitable climate. However, at the tribal level, taxon richness and taxon composition are strongly correlated with both climatic area and the number of dung types. Dung type diversity, on the other hand, varies according to the evolutionary history of mammals (Davis and Scholtz 2001, Davis et al. 2002b). The global dung beetle fauna is divided into 12 tribes (Cambefort 1991), one of which comprises three subtribes. Two tribes (Canthonini and Dichotomiini) are widespread, with principal generic richness in large southerly regions (Afrotropical, Australia + New Guinea, Madagascar, Neotropical), representing a Gondwanaland pattern. Three tribes (Eucraniini, Eurysternini, and Phanaeini) are restricted to the Americas, whereas the remaining tribes and the three subtribes of the Oniticellini are either restricted to AfricaEurasia (Gymnopleurini, Onitini, and Scarabaeini) or are centered in Africa (Coprini, Onthophagini, Sisyphini, and the three

5  Insect Biodiversity in the Afrotropical Region

s­ubtribes of the Oniticellini: Oniticellina, Drepanocerina, and Helictopleurina, the latter being endemic to Madagascar). The basal “tunneling” tribe and the basal “rolling” tribe are generically and specifically dominant in the western hemisphere, although the basal relict taxa of both are restricted to Africa (Philips et  al. 2004). Besides the three endemic American tribes, all other tribes are numerically dominant in Africa or Madagascar (Helictopleurina). The scarabaeine dung beetles, consequently, are essentially a tropical group with Gond­ wanaland ancestry. The tribes with a southern, primarily tropical, Gondwanaland position (Dichotomiini and Canthonini) occupy a basal position in a published phylogeny (Philips et al. 2004). In Africa, they are reduced to minority status, with many, although not all genera, centered in southern forests or cool southern climates. The tropics have been described as museums of diversity (Gaston and  Blackburn 1996), owing to the persistence of old  taxa. Persistence and dominance of Gondwanaland groups is greatest where present spatial factors (large areas of tropical climate) and trophic factors (low numbers of dung types) show the least differences to those in the early Cenozoic, which were warm, moist, and dominated by forest (Axelrod and Raven 1978), with low cross-­latitudinal thermal stratification (Parrish 1987). This observation is consistent with studies indicating that higher biological taxa remain constrained by adaptations to environmental conditions that occurred historically in their centers of diversification (Farrell et  al. 1992), leading to ecophysiological limitations on their  current spatial distribution patterns (Lobo 2000). Dung beetle taxa with older ancestry have been superseded largely in numerical dominance by younger tribes (Davis et  al. 2002b) where present climatic conditions and trophic factors are more dissimilar to earlier conditions. From the mid-Cenozoic, cooler, drier climate has resulted in a contraction of tropical forests in Africa (Axelrod and Raven 1978) and an increase

in savannas and grasslands. A c­oncomitant increase occurred in the number of dung types as a result of the diversification of coarse-­dungproducing mammals (Perissodactyla at 71 mya and some Artiodactyla and Proboscidea at 60 mya; Penny et al. 1999), which have achieved large body size and void large droppings. The later addition of the highly diverse ruminant Bovini in the late Miocene (10 mya), which produce a wide spectrum of large fine-fibered dung pads and small dung types such as pellets, led to increased diversification of younger dung beetle groups.

5.6 ­Conclusions The Afrotropical region is endowed with exceptional biological diversity because of its high numbers of biomes, including deserts, forests, savannas, lake systems, the eastern mountain arc, and the tremendously rich Cape region. The region is also home to Africa’s most species-rich country, South Africa, which is also the second most species-rich country in the world (Cowling and Hilton-Taylor 1994). Here, the high diversity is largely a result of the rich Cape Floristic Kingdom, the world’s richest plant diversity hotspot (Cowling and HiltonTaylor 1994), which is home to about 52% of southern Africa’s plant endemics. This value amounts to about 3.5% of the world’s flora on only about 0.2% of Earth’s surface, a ratio considerably higher than in even tropical rainforests. The Cape region is home not only to high insect species endemicity, as expected from the close association between plants and insects, but also to higher-level endemicity, including numerous endemic families, subfamilies, tribes, and genera (Scholtz and Holm 1985). The African savanna biome, which comprises about half of the continent’s surface area, carries Earth’s greatest diversity of ungulates, more than in any other biome or continent. This exceptional diversity is directly linked to the high spatial heterogeneity of African savanna ecosystems (du Toit and Cumming 1999).

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Although general studies of African savanna insects are lacking, the relative diversity and ecological importance of insect groups, such as dung beetles, probably are at least equal to those of the ungulates for some of the same reasons. Although forests occupy about 10% of tropical Africa, and comprehensive collections of insects are housed in two large Belgian museums (the Institut Royal des Sciences Naturelles and the Royal Museum for Central Africa, Tervuren) as a legacy of the colonial occupation of the Belgian Congo (now Democratic Republic of Congo), few studies seem to have considered the African tropics in the same detail as, for instance, the New World Tropics. The neglect of the African tropics probably results largely from the decayed infrastructure and civil strife in the “Congo.” Such problems have made this huge area, which encompasses most of the biome in one of Africa’s largest countries, largely inaccessible to researchers. The eastern arc mountains that form the backbone of Africa and run in a series of mountain chains from the Cape to Ethiopia have been identified as areas of high endemicity, particularly of relict groups of invertebrates. The area is thought to have served as a corridor for temperate species to spread between the Palearctic region and southern Africa during several favorable periods in the past. Intervening periods of unfavorable conditions would have restricted adaptable fauna to isolated patches of suitable habitat (Lawrence 1953, Stuckenberg 1962, Griswold 1991). Such abundance, and a host of additional impediments, creates intimidating challenges to documenters. The refrain heard about the study of insect biodiversity throughout Africa, which is where the bulk of the Old World’s biodiversity occurs, remains more or less unchanged despite the noble sentiments expressed at international biodiversity meetings held every few years. Many African countries were signatories, amid much fanfare, to the Rio Convention on biodiversity. Although some of these countries formulated “biodiversity policies” as a result of committing to do so at Rio, we are unaware of any that actu-

ally have attempted to survey their insect faunas. The official reasons given for inaction remain the same – lack of resources and a shortage of skilled and committed personnel. However, the one fact to which none will admit is the lack of political will by most governments to implement their commitments. African insect habitats are being destroyed at an unprecedented rate. Conservation generally is applied, if at all, only to tourist-attracting large mammals, and political instability or virtual collapse of road infrastructure discourages collecting from large swaths of some of the most biologically rich areas on the continent. Inane laws administered by often corrupt or incompetent bureaucrats discourage biodiversity studies by foreigners, who most often have the interest and the means to undertake the studies. The perception often held is that foreigners are intent on plundering the commercial biological potential of the fauna and flora. Collecting is therefore discouraged by an often-hostile bureaucracy that would rather learn nothing of the fauna than allow representative specimens to be collected. Even if sufficient resources and human capital were available to survey the insects, various, increasingly serious factors mitigate against gaining an idea of the historical biodiversity because of human practices. One of the most serious of these practices, which leads to total land transformation, is charcoal production, which already has led to huge tracts of land in Angola, Mozambique, and Zambia, and possibly other countries, being transformed from dense savanna woodland, one of the biome jewels of the African continent (du Toit and Cumming 1999), to open scrub and grassland. The effects on native insects are unknown but probably severe. South Africa seems to be the only African country with a serious commitment to biodiversity study and the only African country with a legal conduit for managing its biodiversity since it implemented the Biodiversity Act in 2004. The act provides for the management and conservation of the country’s biodiversity through

5  Insect Biodiversity in the Afrotropical Region

biodiversity planning and monitoring, protection of threatened ecosystems and species, control and management of alien and invasive species, regulation of bioprospecting, fair and equitable benefit sharing, and regulation of permits. The act allowed for the establishment of SANBI (South African National Biodiversity Institute), the mandate of which is to respond appropriately to biodiversity-related global policy and national priorities, make systematic contributions to the development of national biodiversity priorities, and demonstrate the value of conserving diversity and the relevance of biodiversity to the improvement of the quality of life of all South Africans. Despite the noble wording of the act, major impediments still exist for scientists who wish to study South African insect diversity. Some of these impediments are in the form of bureaucracy, complicating the process of issuing permits by the various provinces to which control of biodiversity has devolved. The inefficiency of most of the provincial permitting departments is compounded by draconian penalties for illegally collecting specimens. A recent example of this was the overnight imprisonment of a foreign researcher in the Western Cape Province for collecting a spider without the necessary permit. An admission-of-guilt plea in court and a substantial fine was the immediate outcome, but a permanent criminal record was the more serious and long-term result. The reason for the fiasco was that elephants, rhinoceroses, and invertebrates are covered by the same biodiversity laws, so collecting an insect is legally equivalent to poaching a rhino. However, as a result of concerns expressed by the biodiversity community in South Africa about the impediments to biodiversity study, a series of meetings and workshops involving representatives of SANBI, provincial permitting authorities, tertiary academic institutions, museums, and amateur insect collectors were held to address the issues. The biodiversity scientists have the interest and the will to succeed, but the question of whether the bureaucracy can be overcome remains. Only time will tell.

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Palparini (Insecta: Neuroptera: Myrmeleontidae). Acta Zoologica Academiae Scientiarum Hungaricae 48 (Supplement 2): 175–184. Miller, S. E. and L. M. Rogo. 2001. Challenges and opportunities in understanding and utilization of African insect diversity. Cimbebasia 17: 197–218. Miller, S. E., B. Gemmill, L. Rogo, M. Allen and H. R. Herren. 2000. Biodiversity of terrestrial invertebrates in tropical Africa: assessing the needs and plan of action. Pp. 204–212. In P. H. Raven and T. Williams (eds). Nature and Human Society: the Quest for a Sustainable World. Proceedings of the 1997 forum on biodiversity. National Academy Press, Washington, DC. 625 pp. Parrish, J. T. 1987. Global palaeogeography and palaeoclimate of the late Cretaceous and the early Tertiary. Pp. 51–73. In E. M. Friis, W. G. Chaloner and P. R. Crane (eds). The Origins of Angiosperms and Their Biological Consequences. Cambridge University Press, New York. Penny, D., M. Hasegawa, P. J. Waddell and M. D. Hendy. 1999. Mammalian evolution: timing and implications from using the log-determinant transform for proteins of differing amino acid composition. Systematic Biology 48: 76–93. Philips, T. K., E. Pretorius and C. H. Scholtz. 2004. A phylogenetic analysis of dung beetles (Scarabaeidae: Scarabaeinae): unrolling an evolutionary history. Invertebrate Systematics 18: 53–88 Riley, J. 2001. Indicator quality for assessment of impact of multidisciplinary systems. Agriculture, Ecosystems and Environment 87: 121–128.

Scholtz, C. H. and S. L. Chown. 1995. Insects in southern Africa: how many species are there? South African Journal of Science 91: 124–126. Scholtz, C. H. and E. Holm. 1985. Insects of Southern Africa. Butterworths, Durban. 502 pp. Schutze, M. K., N. Aketarawong, W. Amornsak, K. F. Armstrong, A. A. Augustinos, N. Barr, W. Bo, K. Bourtzis, L. M. Boykin, C. Cáceres, S. L. Cameron, T. A. Chapman, S. Chinvinijkul, A. Chomič, M. De Meyer, E. Drosopoulou, A. Englezou, S. Ekezi, A. Gariou-Papalexiou, S. M. Geib, D. Hailstones, M. Hasanuzzaman, D. Haymer, A. K. W. Hee, J. Hendrichs, A. Jessup, Q. Ji, F. M. Khamis, M. N. Krosch, L. Leblanc, K. Mahmood, A. R. Malacrida, P. Mavragani-Tshipidou, M. Mwatawala, R. Nishida, H. Ono, J. Reyes, D. Rubinoff, M. San Jose, T. E. Shelly, S. Srikachar, K. H. Tan, S. Thanaphum, I. Haq, S. Vijaysegaran, S. L. Wee, F. Yesmin, A. Zacharopoulou and A. R. Clarke. 2015. Synonymization of key pest species within the Bactrocera dorsalis species complex (Diptera: Tephritidae): taxonomic changes based on a review of 20 years of integrative morphological, molecular, cytogenetic, behavioural and chemoecological data. Systematic Entomology 40: 456–471. Stuckenburg, B. R. 1962. The distribution of the montane palaeogenic element in the South African invertebrate fauna. Annals of the Cape Provincial Museums 2: 190–205. Waterhouse, D. F. 1974. The biological control of dung. American Scientist 230: 101–108. White, I. M. and M. M. Elson-Harris. 1992. Fruit Flies of Economic Significance: Their Identification and Bionomics. CAB International, Wallingford. 600 pp.

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6 Biodiversity of Australasian Insects Peter S. Cranston Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, Australia

Much Australasian biodiversity, lacking the decimating effects of the predominantly northern‐hemisphere Pleistocene glaciations, remains intact from a much deeper geological history. To the alert and travelled northern hemisphere scientist, the biodiversity south of the equator is much more extravagant than to the north. For example, a higher taxonomic diversity of ants is recorded for a modestly revegetated hill outside the Australian National Insect Collection laboratories in Canberra than in all of the United Kingdom. Furthermore, Australasian biodiversity displays biogeographic patterns uniting the southern continents, as recognized by early explorer‐scientists such as coleopterist Wilhelm F. Erichson (1842) and polymath Joseph Hooker (1853), both of whose placements of the fauna and flora of “Van Diemen’s Land” in a global context were remark­ ably prescient. Southern hemisphere‐based entomologists such as Ian Mackerras (1925), Robin Tillyard (1926), and Launcelot Harrison (1928) recognized austral biodiversity relation­ ships prior even to knowing of Alfred Wegener’s (1915, 1924) theory of continental drift. The les­ son is that a detailed knowledge of the geology and biodiversity of the southern lands, with a comparative perspective, allowed intellectually untrammeled minds to understand the evolu­ tion of the biota, despite contrary geological orthodoxy. We might consider whether similar

constraints are hindering our deeper under­ standing of the diversification of austral insect biodiversity (McCarthy 2005).

6.1 ­Australasia – The Locale Australasia, for the purposes of this overview, comprises the series of oceanic islands, from massive to minute, in the southwestern Pacific (Fig.  6.1). It corresponds with the geological Australian section of the Indo‐Australian plate, and thus is flanked to the west by the Indian Ocean and to the south by the Antarctic/Southern Ocean. The island continent of Australia (includ­ ing Tasmania) is the largest landmass, with the globally largest “official” island of New Guinea to its north, and New Zealand to the southeast. The Australian islands of Lord Howe and Norfolk lie successively to the east, whereas New Caledonia and Vanuatu (New Hebrides) lie successively to the northeast. Further eastward of Vanuatu, Fiji lies in the Eastern Melanesian region of the Central Pacific, almost astride the boundary between the Australian and Pacific plates. Tonga lies southeast on its own microplate (terrane). The biotically defined northwestern bound­ ary to Australasia often is treated as Wallace’s Line, named for Alfred Wallace, who recognized a faunal discontinuity between the “Australasian” islands of Celebes (Sulawesi) and Lombok

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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Figure 6.1  The Australasian region.

(to the east) and Indo‐Malaysian islands includ­ ing Borneo, Java, and Bali (to the west). The Indonesian islands on the Australian side, termed Wallacea, are separated by deep water from both the Indo‐Malaysian and the Australia‐ New Guinean continental shelf. Wallace’s noted discontinuities are less evident among insects, or at least the patterns are so complex, espe­ cially concerning Sulawesi, that a simplistic interpretation is not possible (Vane‐Wright 1991, New 2002) – an issue also interpretable as “too many lines…” (Simpson 1977). This region is perhaps best understood as transitional – hav­ ing an Australian–New Guinean faunal resem­ blance that is variably attenuated with distance westward, and overlies a rich and highly endemic biota, often with continental Asian affinities that attenuate eastward. In this area, only Christmas Island (10°30’S 105°40’E), an Indian Ocean offshore Territory of Australia, will be considered in this chapter.

Although New Zealand lies close to and astride the eastern margin of the Pacific Plate, with the Alpine fault plate boundary running southwest–northeast across its South Island, here all of New Zealand and its offshore, includ­ ing subantarctic, islands are considered. The subantarctic islands represent remnant emer­ gent islands of the Campbell Plateau, lying between Antarctica and South Island New Zealand, and carry biotas exhibiting both endemic and widespread elements (Michaux and Leschen 2005).

6.2 ­Some Highlights of Australasian Insect Biodiversity Insects “down under” contain iconic exemplars. The bush fly Musca vetustissima provokes the famous Aussie “wave” and promotes the tour­ ist’s souvenir cork‐lined hat. The attentions of

6  Biodiversity of Australasian Insects

one of the most abundant and diverse ant faunas in the world authenticate the famous “Aussie barbecue.” The landscape of northern Australia is characterized by termite mounds of diverse shapes and sizes, among the most striking of which are the flattened and regularly north– south orientated structures produced by the magnetic termites (Amitermes spp.). Public attention was captured by the rediscovery and recovery of the presumed extinct Lord Howe Island stick insect (Dryococelus australis (Montrouzier)), dubbed the “land lobster” on account of its size. Selections from Australian insect biodiversity are harvested by Aboriginal Australians. The Arrente people use yarumpa (honey ants) and udnirringita (witchetty grubs), which have now entered the non‐indigenous food chain in res­ taurants catering to wealthy tourists and politi­ cal entertainment. Adult bogong moths, Agrotis infusa (Noctuidae), which gather in their mil­ lions in aestivating sites in narrow caves and crevices on mountain summits in southeastern Australia, once formed another important Aboriginal food. The nocturnal illumination of a new Parliament building in the nation’s capital acted as a giant light‐trap for migrating bogongs in such numbers that the insects entered the politicians’ consciousness and inspired the design for a Canberra‐based meeting of the Australian Entomological Society (Fig. 6.2). Australia is not unique in its ambivalent atti­ tude to insects. New Zealanders take warped pride in the voraciousness of their South Island coastal namu or sand flies (Austrosimulium spp., Simuliidae) and justifiable pride in the endemic radiations of their wetās (Anostostomatidae and Rhaphidophoridae). The wetās – outsized, flight­ less orthopterans  –  include the Little Barrier Island giant wetā (Deinacrida heteracantha) or wetāpunga (Maori for “god of ugly things”), which is one of the heaviest insects, weighing up to 70 grams (Trewick and Morgan‐Richards 2004). About one million tourists each year visit Waitomo Caves (Doorne 1999) to share an extravagant and potentially educational entomo­ logical experience  –  the bioluminescence

Figure 6.2  Logo for the Annual Australian Entomological Society meeting, incorporating bogong moths and Parliament House, Canberra.

displayed by glowworms, larvae of the dipteran Arachnocampa luminosa (Keroplatidae). For conservation of native biodiversity, Aotearoa (the Maori name for New Zealand) has one of the highest profiles of any country, following recog­ nition of the devastation caused to the unique native invertebrates and birds after the arrival of humans – both Polynesians and European colo­ nists – with their attendant rats and peridomes­ tic animals. Invertebrates feature in many species conservation plans, which depend substantially on elimination of vertebrate vermin from off­ shore islands. Central to many of the southern biogeograph­ ical studies has been the island of Nouvelle Calédonie (New Caledonia). The French have a long history of biodiversity studies in their erst­ while colony, with entomologists being promi­ nent among researchers. Early studies, notably of the flora, suggested the existence of an ancient, relictual fauna that survived from the  Cretaceous Gondwanan megacontinent. Although that thesis stimulated global scientific interest, the scenario is not quite as once believed, at least for insects. Nonetheless, this does not negate the evidently high levels of

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endemism, and multiplicity of evolutionary ori­ gins of the biota. To the north, New Guinea, the largest “offi­ cial” island on the planet, is separated from the Australian continent only by the relatively shal­ low and recent Torres Strait. This geologically (and ethnically) diverse island might have been a lesser target for pioneering exploratory ento­ mologists compared with the rainforests of Southeast Asia and the Amazon. However, early insect collectors discovered many gaudy and perhaps saleable specimens such as the largest known butterfly in the world, the Queen Alexandra’s birdwing (Ornithoptera alexan­ drae); the world’s largest moth, the Hercules moth (Coscinocera hercules); and giant stick insects (Eurycnema goliath and species of Acrophylla). Biologist‐explorers of New Guinea, including Alfred Russel Wallace (1860) and Luigi D’Albertis (1880), collected and recorded extraordinary insect diversity for a 19th‐century European audience eager for natural history tales and specimens. Papua New Guinea (PNG; eastern New Guinea) ranks twelfth globally in terms of endemism of large butterflies (Papilionidae, Pieridae, and Nymphalidae): 56 of 303 species are endemic. Economic benefits can flow from a perhaps sustainable trade in such live lepidopterans for the butterfly houses of the affluent world. More recently, the island has been the site of some laborious and intensive studies of plant‐feeding (phytophagous) insects in an attempt to establish how selective these insects are in their use of host plants such as the diverse figs (Ficus, Moraceae). In keeping with the predictions of island bio­ geographic theory, Pacific Islands, including New Zealand, have disharmonic biotas. Typically, major taxa are erratically absent, some groups show evidence of endemic radia­ tions, and levels of endemism are generally high. These islands, and especially Hawai’i, are the theaters in which the processes of species for­ mation and species extinction can be studied, for mixed in with the natives are substantial alien introductions that threaten all aspects of biodiversity retention.

6.2.1  The Lord Howe Island Stick Insect

The Lord Howe Island Group is located in the Western Pacific Ocean some 700 km northeast of Sydney, and comprises the main island of Lord Howe along with the Admiralty Islands, Mutton Bird Islands, Ball’s Pyramid, and many reefs. Geologically, the main island is the eroded remnant of a large shield volcano that erupted intermittently from the sea floor in the late Miocene (some 6.5 million to 7 million years ago). What remains are the exposed peaks of a 65 km long and 24 km wide volcanic seamount that rises from ocean depths of nearly 2 km. The seamount is near the southern end of a chain of such seamounts, most of which are submerged; the chain extends for more than 1000 km. The group was inscribed on the UNESCO World Heritage List in 1982 as an outstanding example of an oceanic island of volcanic origin, with a unique biota and important and significant nat­ ural habitats for in situ conservation of biologi­ cal diversity, including those containing species of plants and animals of outstanding universal significance from the point of view of science and conservation. Although no insects were specified in the nomination, subsequently the island has attained some fame as the site of the rediscovery of a large, flightless stick insect (Fig.  6.3). The Lord Howe Island stick insect, D. australis, was known locally as the “land lob­ ster” or “tree‐lobster” on account of its shape and size (up to 12 cm long). This phasmatid was known for its ability to run on the ground, and it was common and easily observed sheltering in banyan trees (Ficus macrophylla) on the island in the early 20th century. Its apparent demise seems to be connected with the release of black rats on the island when a supply ship ran aground in 1918, which triggered the extinc­ tions of five flightless birds. The land lobster was thought to have become extinct by the 1930s, and was entered as such in the International Union for Conservation of Nature (IUCN) Red List. Subsequent surveys failed to find any further evidence, until a rock climber on the offshore Ball’s Pyramid photographed an

6  Biodiversity of Australasian Insects

Figure 6.3  The Lord Howe Island stick insect against its home, Ball’s Pyramid.

adult female; its rare presence was confirmed in the late 1960s. Ball’s Pyramid is aptly named, being a pyramidal structure rising 500 m above sea level from a base of only 1100 m × 400 m at sea level. The idea that such a basaltic column, lacking both large woody vegetation and refu­ gial hollows, could support a population of a large phasmatids was greeted with skepticism. Numerous attempts to rediscover the species failed until in 2001 a biological survey revealed three specimens associated with the endemic shrubby paperbark (Melaleuca howeana). The following year, 24 individuals were observed associated with the same, small patch of paper­ bark, which is thought to be the only suitable habitat on the island. Retreats were clefts in the rock–root interface where seepages occurred, in contrast to the tree holes used on the main­ land prior to extinction. The rediscoverers (Pridell et  al. 2003) pointed out that the Ball’s Pyramid locality is too small to maintain a pop­ ulation against any future environmental change and made a plea for a captive‐breeding program, concurrent with elimination of rats from Lord Howe, to allow reintroduction. Action plans prepared by the New South Wales National

Parks and Wildlife Service followed the listing of the species as critically endangered (from extinct) by the Commonwealth Government. Two pairs of the insects were captured and transported to the mainland. One pair went to Melbourne Zoo, an institution with an enviable record of breeding invertebrates, and the sec­ ond was housed by one of Australia’s leading stick insect experts. Rearing has been successful using garden‐grown M. howeana as the food stock, with banyan in reserve (Zoos Victoria 2006). The necessary elimination of rats from Lord Howe Island, required for any reintroduc­ tion to succeed, remains under consideration for feasibility and cost. 6.2.2  Australasian Birdwing Conservation

The world’s largest butterfly, the Queen Alexandra’s birdwing (Ornithoptera alexan­ drae) of PNG, is a regional success story. This spectacular species, whose caterpillars feed only on Aristolochia diehlsiana vines, is limited to a small area of lowland rainforest in northern PNG. Under PNG law, this birdwing species has been protected since 1966, and international

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commercial trade was banned by endangered listing on Appendix I of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). Dead specimens in good condition command a high price, which can be more than US$2,000. In 1978, the PNG governmental Insect Farming and Trading Agency (IFTA), in Bulolo, Morobe Province, was established to control conservation and exploitation and act as a clearinghouse for trade in Queen Alexandra’s birdwings and other valu­ able butterflies. Local cultivators, numbering some 450 village farmers associated with IFTA, ranch their butterflies. Farmers plant appropri­ ate host vines, often on land already cleared for vegetable gardens at the forest edge, thereby providing food plants for a chosen local species of butterfly. Wild adult butterflies emerge from the forest to feed and lay their eggs; hatched lar­ vae feed on the vines until pupation, when they are collected and protected in hatching cages. According to species, the purpose for which they are being raised, and conservation legisla­ tion, butterflies can be exported live, as pupae, or dead as high‐quality collector specimens. IFTA, a non‐profit organization, has sold some $400,000 worth of PNG insects yearly to collec­ tors, scientists, and artists around the world, generating an income for a society that struggles for cash. Local people recognize the importance of maintaining intact forests as the source of the parental wild‐flying butterflies of their ranched stock. In this system, the Queen Alexandra’s birdwing butterfly has acted as a flagship spe­ cies for conservation in PNG, and this success story attracts external funding for surveys and reserve establishment. In addition, conserving forests in PNG for this and related birdwings undoubtedly results in the conservation of much biodiversity as an umbrella effect. The UK Darwin Initiative in 2005 funded a three‐year project “Socio‐economics of insect farming in Papua New Guinea” to assess and train ranchers and collectors in sustainable insect collecting. Early reviews suggest that burdensome licens­ ing, permits, fees, and paperwork threaten the viability of legal trade and encourage a growing

illegal trade, especially in abundant species that ought to need no CITES listing. New Guinean insect conservation efforts need a commercial incentive to provide impoverished people with some recompense for protecting nat­ ural environments. Commerce need not be the sole motivation, however: the aesthetic appeal of native birdwing butterflies flying wild in local neighborhoods, combined with local education programs in schools and communities, has saved the subtropical Australian Richmond birdwing butterfly, Troides or Ornithoptera richmondia. Larvae of Richmond birdwings eat Pararistolochia or Aristolochia vines, choosing from three native species to complete their development (Sands et  al. 1997). However, much coastal rainforest habitat supporting native vines has been lost, and the alien South American Aristolochia elegans (Dutchman’s pipe), which was introduced as an ornamental plant but then escaped from gardens, has been luring females to lay eggs on it as a pro­ spective host. This oviposition mistake is deadly because this plant is toxic to young caterpillars. The answer to this conservation problem has been an education program to encourage the removal of Dutchman’s pipe from native vegeta­ tion, from sale in nurseries, and from gardens and yards. Replacement with native Pararistolochia was encouraged after a massive effort to propa­ gate the vines. Community action throughout the native range of the Richmond birdwing seems to have reversed its decline, without any require­ ment to designate land as a reserve (Sands et al. 1997).

6.3 ­Drowning by Numbers? How Many Insect Species are in Australasia? 6.3.1 Australia

For the total Australian insect diversity, Taylor (1983) estimated about 110,000 species. Even then, this figure clearly was an underestimate. After questioning of practicing taxonomists, Monteith (1990) determined a figure of about

6  Biodiversity of Australasian Insects

20,000–40,000 beetle species, although what proportion of the total biota this constituted was unknown. Suggesting that the Australian dipteran fauna of some 10,000–12,000 species and the Australian insect fauna as a whole both comprise about 5% of their respective world totals, Colless and McAlpine (1991) extrapo­ lated to estimate global diversity in the low– mid‐range of existing estimates. Stork (1993) then suggested the existence of some 400,000 Australian insect species, of which three‐­ quarters were undescribed. In extrapolating from comparatively well‐known geographi­ cally constrained regions to generate global biodiversity estimates, Gaston and Hudson (1994) included the Australian insect biota in their analyses as “well known.” They argued that the more modest Australian species rich­ ness estimates supported their own estimated low value for total global species richness. Most recently, a combination of expert opinion and extrapolation from the rate of species dis­ covery by recent revisionary taxonomists led Yeates et al. (2003) to a figure of near 205,000 insect species for Australia. Within this esti­ mate, numbers of described and estimated species range from only 10 undescribed spe­ cies among the estimated 330 Odonata to some 60,000 undescribed Coleoptera, with only 22,000 described. The major (megadiverse) orders include estimates of 12,000 Hemiptera, 20,000 Lepidoptera, 30,000 Diptera, and 40,000 Hymenoptera; Coleoptera comprise about 40–50% of the total numbers of insects. The authors acknowledge shortcomings, including some related to revisionary taxonomists’ choices of study taxa  –  some selected their taxa on the basis of high levels of perceived novelty (upwardly biasing extrapolates), whereas others, reviewing already well‐known taxa (e.g., butterflies), contributed little in the way of species discovery (biasing downward). These figures, nonetheless, seem to reflect a reality in which Australia, with some 6% of Earth’s land area, supports about 5–6% of the global insect species diversity of some 4 mil­ lion species.

6.3.2  New Zealand (Aotearoa), Chatham Islands, and Subantarctic Islands

New Zealand, comprising two main islands with  an area much smaller than Australia (0.27 million versus 7.6 million km2), supports a commensurately lower insect biodiversity. A preliminary assessment (for Species 2000 New Zealand) provides an estimate of some 20,000 species, among them slightly more than 10,000 described species, and nearly 9000 species awaiting description. Kuschel’s (1990) claim of 40,000 species, based on extrapolation from a rather exaggerated Coleoptera diversity, seems too high, especially because Leschen et  al. (2003) assess the New Zealand Coleoptera at approximately 10,000 species. Insects on New Zealand’s offshore islands have been subject to continuing study, especially the beetles. Thus, the addition of 131 species of Coleoptera to the known fauna of Chatham Islands (ca. 40 °S) increased the total to 286 (Emberson 1998). Smaller, perhaps younger, and increasingly southerly (subantarctic) islands, emergent from the Campbell Plateau, have more modest insect biodiversity, at least as far as num­ bers alone are concerned. Of 150 insect species reported from the Antipodes Islands (ca. 49 °S) (Marris 2000), Coleoptera comprise only 25 spe­ cies in 13 families. In comparison, the Snares Islands (48 °S) have a reported 25 species in 14 families; the Bounty Islands (ca. 47 °S) have nine species in seven families; the Auckland Islands (ca. 50 °S) have 57 species in 17 families; and Campbell Island (ca. 52 °S) has 40 species in 15 families. The most austral island in the area, the Australian Macquarie Island (54.30 °S), has eight species in only two families (Williams 1982, Greenslade 1990, Young 1995, Klimaszewski and Watt 1997, Marris 2000). These data suggest that the island faunas are species poor and, under these circumstances, the use of standard multipliers from the known Coleoptera fauna to the total Insecta fauna might be misleading. This scenario is especially so on oceanic islands with unbalanced faunas and different histories and distances from

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sources. The question of endemism and biogeo­ graphic and phylogenetic relationships of the insect faunas of New Zealand will be consid­ ered below. 6.3.3  New Guinea

From ratios of the New Guinea fauna to the world fauna for well‐known groups, rates of description of new taxa, and the size of the Australian insect fauna, Miller et al. (1995) cal­ culated a possible 300,000 species of insects for New Guinea. They qualified this figure as potentially over‐ or underestimated by 100,000 species. More recently, biodiversity surveys assessing richness of phytophagous (plant‐feed­ ing) insects have delivered further insights. Insect herbivores sampled from the foliage of 15 species of figs in rainforest and coastal habitats in the Madang area, PNG, revealed 349 species of leaf‐chewing insects (13,193 individuals) and 430 species of sap‐sucking insects (44,900 indi­ viduals) (Basset and Novotny 1999). Despite a high sampling intensity, the species‐accumula­ tion curve did not reach an asymptote. Evidence from studies such as this, concerning host spec­ ificity of phytophagous insects in New Guinea, led Novotny et al. (2002) to challenge previous large multipliers based on high levels of monophagy. Based on an estimate that New Guinean Coleoptera and Lepidoptera constitute 5% of the global biodiversity of each order, a proportion derived from Sekhran and Miller (1996), new regional and global biodiversity estimates were derived from host‐specificity ratios. For butterflies, for which figures of 959 described species in New Guinea (Parsons 1999) and 15,000–20,000 species globally are likely to be accurate, Novotny et al. (2002) cal­ culated an estimated 1,179 species in New Guinea and 23,500 worldwide. 6.3.4  New Caledonia and the West Pacific

New Caledonia lies on the Tropic of Capricorn, between 19 °S and 23 °S, 1200 km due east of Capricornia, Australia, and 1500 km northwest

of New Zealand. The island is a recognized biodiversity hotspot. Some 4000 insect species had been cataloged at the time of Chazeau’s (1993) review of the terrestrial fauna of the island, but an estimate of 8000 to 20,000 insect species is realistic. Endemism is variably high – the more than 70 native species of but­ terflies and 300 species of moths exhibit ende­ mism of 38% (Chazeau 1993), whereas, according to the Department of Entomology at The Swedish Museum of Natural History (2003), all but two of 111 described species of Trichoptera are endemic. For the other land areas of the region  – Vanuatu, the Solomons, and Fiji – estimates of insect species diversity can be little more than “guestimates,” given the lack of modern surveys. Robinson (1975) calculated the total number of insect species inhabiting the Fiji group of islands as in excess of 3500. This figure is to be tested, because insect biodiversity of the Fijian islands is being inventoried in detail under the National Science Foundation‐Fiji Terrestrial Arthropod Survey (Evenhuis and Bickel 2005).

6.4 ­Australasian Insect Biodiversity – Overview and Special Elements 6.4.1 Australia

Australia, in keeping with its size as a continent occupying some 5–6% of Earth’s landmass, exhibits all major elements of insect biodiver­ sity. Among the few departures from propor­ tionality are the Isoptera (termites), with perhaps more than 10% of the global diversity; this might be so also for Phasmatodea (stick and leaf insects). The three absent ordinal level taxa, Grylloblattodea, Mantophasmatodea, and Zoraptera, are geographically restricted minor orders of low species diversity, and are not pre­ sent anywhere in Australasia. Strepsiptera and Embiidina, although represented in Australia, are absent from New Zealand. At the level of family, distinctive patterns emerge, with some

6  Biodiversity of Australasian Insects

local endemics and many more restricted to the southern hemisphere (Gondwanaland). Typical diversity patterns are shown by the aquatic orders. In Odonata, the Hemiphlebiidae, comprising a single charismatic species some­ times given the higher rank of Hemiphleboidea, is restricted to a few southern Australian pools (Trueman et  al. 1992). The family Petaluridae, represented by Jurassic fossils, has five extant Australian species, including Petalura ingentis­ sima, with a wingspan of up to 160 mm, making it the largest of living dragonflies. The small odonate families Hypolestidae, Diphlebiidae, and Cordulephyidae are endemic to Australia, whereas others are widespread, of northern ori­ gin, or patchily present in other austral conti­ nents (Gondwanaland). Early recognition of the austral relationships among the Ephemeroptera by Edmunds (1972) has been substantiated and reinforced, even as  family concepts change. The family Telo­ ganodidae (which rather unusually includes South Africa and Madagascar in its Gondwanan pattern) and many clades, including Ameletop­ sidae, Nesameletidae, Oniscigastridae, and Rallidentidae, suggest austral radiation, as do the remarkably diverse Australasian Leptophle­ biidae (Christidis 2006). Three of four Australasian families of Plecoptera (Eustheniidae, Gripopterygidae, and Austroperlidae) belong to  the monophyletic Gondwanan suborder Antarctoperlaria (McLellan 2006). In the Trichoptera, the Hydrobiosidae are predomi­ nantly austral Plectrotarsidae; Antipodoecidae are endemic to Australia; Chathamiidae, Oeconesidae, and Conoesucidae are restricted to Australia and New Zealand; Kokiriidae to South America, Australia, New Zealand, and New Caledonia; Tasimiidae to Australia and South America; and Helicophidae to New Caledonia, New Zealand, Australia, Chile, and Southwest Argentina (Wiggins 2005). Although these aquatic orders and their pre­ dominantly running‐water habitats are quite well studied, only recently has a novel aquatic diversity been uncovered – that of diving beetles (Dytiscidae) in underground aquifers beneath

arid Australia (e.g., Humphreys 2001, Cooper et al. 2002, Balke et al. 2004). This unexpectedly diverse system originated perhaps when aquatic species from temporary habitats, and from sev­ eral different lineages, evaded drought by enter­ ing calcretes (the hyporheic zone in limestone areas), essentially driven underground by his­ torical aridification of the continent in the Late Miocene/early Pliocene some 5 mya (Leys et al. 2003). Many true flies (Diptera) with immature stages associated with minor aquatic habitats such as seeps or waterfalls, including the Blephariceridae (Zwick 1977, Gibson and Courtney 2007), Chironomidae (e.g., Cranston et  al. 2002), Empididae (Sinclair 2003), and Thaumaleidae (Austin et  al. 2004), have diversified from Gondwanan ancestors. The Nannochoristidae, the only Mecoptera with an aquatic larva, likewise are present in streams of New Zealand, southeastern Australia, and Chile. The high‐ranking hemipteran suborder Coleorrhyncha comprises only the Gondwanan family Pelordiidae (mossbugs), which live among sphagnum and liverworts, especially in forests of southern beeches (Nothofagus). Patterns of familial diversity, endemism, and regional distribution, such as those shown by these aquatic insects, are mirrored within the more terrestrial orders (Cranston and Naumann 1991, Austin et al. 2004). Some strong diversifi­ cations of insects are associated with Australia’s major plant radiations: for example, the Mimo­ saceae, including Acacia; the Myrtaceae, espe­ cially Eucalyptus; and, to a lesser extent, the Casuarinaceae. Proteaceae seem, for the main part, to have avoided insect associations. Majer et  al. (1997) estimated that there could be between 15,000 and 20,000 species of phytopha­ gous insects on Eucalyptus in Australia, including members of Hemiptera (especially psylloids and coccoids), Coleoptera, Diptera, and Lepidoptera (Austin et al. 2004), but a con­ spicuous paucity of Thysanoptera (Mound 2004). The Chrysomelinae (leaf beetles) dem­ onstrate a radiation associated with eucalypts of some 750 species, but are almost completely lacking on Proteaceae (C. A. M. Reid, personal

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communication). Notable Australian plant‐ associated radiations include several independ­ ent originations of gall‐inducing Coccoidea (scale insects) (Cook and Gullan 2004, Gullan et  al. 2005); the phlaeothripid Acacia thrips (Crespi et al. 2004); the ecologically significant, lerp‐forming spondyliaspine Psylloidea (Hollis 2004, Taylor 2006); the cecidomyiid gall midges (Kolesik et  al. 2005) and near‐endemic Fergusoninidae (Taylor 2004, Scheffer et  al. 2004) (Diptera); gall‐inducing Chalcidoidea (Hymenoptera) (LaSalle 2004); and the several thousand (perhaps 5000) species of oecopho­ rine moths (Oecophoridae), the larvae of which consume mainly fallen myrtaceous leaves (Common 1994). Other disproportionately rep­ resented insect groups include the Phasmatodea, cicadas, and pselaphine Staphylinidae. Among the social insects, the short‐tongued bees (Colletinae and Halictinae) and eumenine vespid wasps are strongly represented, as are the termites, especially in arid and northern Australia. Above all, the Formicidae – the ants – rule. With about 1300 described species and subspecies (AntWiki 2015) and perhaps as many as 4000–5000 endemic species, ants dominate ecologically in all but tropical rainforest. This ant diversity and biomass, particularly in more arid Australia, is evident to any modestly obser­ vant citizen. Relictuality, which refers to the appearance of isolated high‐ranking taxa for which phyloge­ netic or fossil evidence exists of past wider dis­ tribution and diversity, is a notable feature of Australasian insects. Thus the species‐rich bulldog ants (subfamily Myrmeciinae), now restricted to Australia, indubitably include fossil taxa from Argentina and the Baltic (Ward and Brady 2003). Mastotermitidae, the once‐diverse sister group to the remaining termites, is reduced now to Mastotermes darwiniensis, a pest in northern Australia. The biting midge family Austroconopidae, which is abundant and diverse in Lebanese and other Cretaceous‐age ambers, is represented now by a single species that feeds on early morning golfers in suburban Perth, Western Australia. The cicada family

Tettigarctidae (the sister group to all other cica­ das) is known from only two extant Australian species, although several Mesozoic northern hemisphere fossil genera are described. Many other examples suggest that the southern hemi­ sphere, perhaps Australia especially, has served as a long‐term refuge from the effects of extinc­ tions in the northern hemisphere (Cranston and Gullan 2005, Grimaldi and Engel 2005). Australia’s offshore islands support some enig­ matic biodiversity, perhaps none more so than Lord Howe Island. In a report provided by the Australian Museum to New South Wales National Parks and Wildlife Service in 2003, some 1800 terrestrial and freshwater inverte­ brate species were reported for Lord Howe Island. Additional surveys have brought the Coleoptera fauna to more than 500 species, with minimally 23 species of at least 10 mm in length. Typically, for offshore islands, about half of the species are flightless, and many of these are probably extinct on the main island, whereas off­ shore islands and rocks still harbor some species. A series of observations from the first surveys in 1916 (by Arthur Lea, 2 years before rats arrived), three surveys in the 1970s, and more recent ones show that extinction for many species is proba­ ble but not definite, because species such as a large flightless scarab and blaberid cockroach have been rediscovered in sites where rats have been present for many decades (C. A. M. Reid, personal communication). The Lord Howe Island wood‐feeding cockroach (Panesthia lata) and Lord Howe Island stick insect (D. australis) are two of only 10 insect species listed as endan­ gered under the New South Wales Threatened Species Conservation Act. The more remote and far more degraded Norfolk Island only developed its fauna when regional volcanic activity ceased, probably within the past 2.3 million years (Holloway 1977). The fauna comprises endemics and a mix of derivatives with relationships to proximate areas; of the 98 species of Macrolepidoptera, 22 species and subspecies are endemic. Among the endemics, most have affinities with Australia and New Caledonia: only two have affinity with

6  Biodiversity of Australasian Insects

New Zealand (Holloway 1977). The single Norfolk Island endemic species of the otherwise New Zealand cicada genus Kikihia, K. convicta, apparently derives from a recent long‐distance dispersal from New Zealand (Arensberger et al. 2004b). Half of the 20 species of Orthoptera on Norfolk Island have associations with Australia, and the remainder are associated with New Caledonia or Southeast Asia; three native Blattodea are known, with five introduced spe­ cies, especially on the degraded Phillip Island (Rentz 1988). 6.4.2  New Zealand

One of the strongest contrasts between insect biodiversity in New Zealand and Australia is the modest diversity and ecological insignificance of New Zealand ants  –  the country has only seven genera and 11 species of native ants (Brown 1958). As on many Pacific Islands, ant numbers are increasingly being supplemented by invasive tramp ants, but this situation does not alter what is, by any definition, an impover­ ished ant fauna. New Zealand simply has an attenuated subset of Australia’s ant fauna, with no high‐level endemism. Biogeographic expla­ nations include the ecological (the generally more humid and cool climate is unfavorable) and the historic (ants failed to recolonize after major past extinction associated with submer­ sion of the islands). A second strong difference is the high rate of aptery (winglessness) among New Zealand insects, especially those living on offshore and subantarctic islands. According to Larivière and Larochelle (2004), about 25% of the New Zealand Heteroptera fauna is flightless, with rates of 65–70% in the Aradidae and Rhyparochromidae. All endemic Blattodea (cockroaches) are flight­ less, as are many Coleoptera and Orthoptera. An absence in New Zealand of the major Australian plant radiations means a lack of the associated diversifications that are seen in Australia. The four native species of Nothofagus, southern beeches, which often form natural monoculture forests, have a greater insect

diversity than might be expected (Hutcheson et  al.1999). Nothofagus hosts numerous sap‐ sucking insects, especially certain beech scales (Coccoidea), the exudates of which provide an important food resource in temperate forest ecosystems (Moller and Tilley 1989, Sessions 2001). Minor insect radiations are associ­ ated  with the podocarps, including some yponomeutid moth genera shared with Tasmania (Dugdale 1996a, McQillan 2003) and, as in Australia, many moth species develop in forest leaf litter (Dugdale 1996b). In contrast to the rather low forest insect diversity, more open habitats support endemic cicadas, orthopterans (both acridid grasshoppers and the wetās), and cockroaches. These have diversified, notably on the South Island, apparently associated with the Alpine orogeny‐induced climate changes and the development of more open upland and off­ shore habitats, including tussock grasslands and scree fields (Buckley et  al. 2001, Trewick 2001, Arensburger et  al. 2004b, Chinn and Gemmell 2004). Although New Zealand’s aquatic insects belong largely to families, and often genera, that are present in Australia or New Caledonia, Chile, and Patagonia, they display high spe­ cies  endemism (90–99% according to Collier 1993,  Harding 2003). The mayfly family Siphlaenigmatidae is endemic to New Zealand. The presence of glaciers on the South Island, presumably originating with Pliocene uplift, seems to have triggered little associated ende­ mism, excepting perhaps a monotypic endemic genus of midge, Zelandochlus, the ice worm found on and in ice caves on the Fox Glacier (Boothroyd and Cranston 1999). 6.4.3  New Caledonia, New Guinea, and Melanesia

New Caledonia is renowned for an extraordi­ nary botanical diversity, with both relicts and radiations of several plant groups, including Araucaria and Agathis and other rare and endemic gymnosperms. To test whether phy­ tophagous insect diversity might track this plant

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diversity, Holloway (1993) assessed the diver­ sity  and relationships of New Caledonian Lepidoptera, especially the Macrolepidoptera. Levels of endemism were modest, relationships tended to be directly with proximate Australian, New Guinean and, less often, New Zealand taxa, and species richness was lower than expected for the area (Holloway 1993). Although exhibiting a radiation, New Caledonia’s Rhyti­ doponera ants also seem to be derived recently from Australian relatives (Ward 1984, Lattke 2003). Entomological contributors to the treat­ ment by Najt and Grandcolas (2002), surveyed insect taxa with some diversity, but failed to find any substantial or ancient radiations, and in general Holloway’s impressions have been con­ firmed by studies of other groups. Thus, Murienne et al. (2005) found the diversification of 10 New Caledonian species of the cock­ roach genus Angustonicus (Blattidae: subfamily Tryonicinae) dated to no older than 2 million years. New Caledonia is implicated in the evolu­ tion of West Pacific cicadas in the Kikihia‐ Maoricicada‐Rhodopsalta clade distributed between New Zealand, New Caledonia, and eastern Australia. Molecular phylogenetic stud­ ies by Arensburger et al. (2004a) indicated that the group (i) originated from a New Caledonian ancestor, (ii) gave rise to one or several New Caledonian clades, or (iii) arose from an Australian ancestor that colonized both New Zealand and New Caledonia. Whichever is cor­ rect, the divergence of New Zealand genera from the Australian and New Caledonian gen­ era evidently took place in the last 11 million to 12 million years (Arensburger et  al. 2004a). Proposed adaptive radiations in New Caledonia, such as the micropterygid Lepidoptera (Gibbs 1983) that show older, vicariant relationships between the island and New Zealand, evidently need the application of molecular techniques to assess implied datings. The numbers of phytophagous insects of New Guinea show that this geologically complex island harbors a high diversity, as expected in tropical regions. Among these phytophages, the leaf‐rolling weevil family Attelabidae, notably

some species groups in the genus Euops, are associated with Nothofagus (Riedel 2001a), whereas Euops is associated with Myrtaceae in Australia (Riedel 2001b). Exceptional diversity is found in the Phasmatodea  –  New Guinea has more than 200 species of phasmids in 58 dif­ ferent genera, comprising more than 6% of the  world’s described Phasmatodea (van Her­ waarden 1998). There are also more than 400 species of Odonata in New Guinea, comprising about 10% of Odonata species worldwide (Kalkman 2006). Evolutionary biologists have uncovered a diversity of flies (Diptera) with “antlers” in New Guinea and northern Australia, among which the tephritid genus Phytalmia is  exceptionally endowed (McAlpine and Schneider 1978). The Fijian insect fauna is poorly known (Fiji Department of the Environment 1997), but in keeping with its oceanic location, it evidently has a fraction of the megadiversity of New  Guinea. Robinson (1975) surveyed the Lepidoptera and estimated there to be 600 species of Microlepidoptera and 400 of Macro­ lepidoptera. In the absence of an explicit phy­ logeny, it is unclear whether the estimation of seven endemic genera, with modest radiation (although high for a Pacific island), and several other intrinsic radiations is correct. An esti­ mated 88 ant species from Fiji (Wilson and Hunt 1967) is an underestimate; some 180 spe­ cies, including 30 exotics, are likely to be found in Fiji (E. Sarnat, personal communication). Of 33 species of Odonata recorded from Fiji, 22 (67%) were endemic (Tillyard 1924). Macro­ lepidoptera, cicadas, dolichopodid flies, and some beetle families show relationships with New Guinea, but several unexpected relation­ ships link Fiji with the New World (Evenhuis and Bickel 2005). The Fijian cicada fauna includes 14 (93%) endemic species, including one endemic genus, Fijipsalta (Duffels 1988). The cicadas, which are among the best studied of the regional insects, include the tribe Cos­ mopsaltriina (Cicadidae) found in Fiji, Vanuatu, and Tonga. This tribe forms the sister group of the Southeast Asian tribe Dundubiina and has

6  Biodiversity of Australasian Insects

no close relatives in Australia, New Caledonia, or New Zealand (de Boer and Duffles 1996, Duffels and Turner 2002). Vanuatu seems to have many single‐species representatives of genera that are otherwise widely distributed in the Asia‐Pacific region, although some modest Miocene‐dated radia­ tions in platynine Carabidae have been identi­ fied (Liebherr 2005). This finding of a platynine radiation is supported by Hamilton’s (1981) study of the endemic aphrophorine Cercopidae (Hemiptera), but no other such radiations have been documented. Although 105 of the 364 recorded Vanuatuan species of Macrolepidoptera are endemic, Robinson (1975) thought that none had its closest relatives in this Archipelago.

6.5 ­Threatening Processes to Australasian Insect Biodiversity The processes threatening insect biodiversity vary somewhat across and within Australasia, but there are several unifying causes. These are habitat loss, introduced animals (including inva­ sive ants), potential effects of climate change, and a minor possibility of overexploitation. 6.5.1  Land Clearance and Alteration

Clearance of native vegetation, including defor­ estation, remains the single most significant threat to all terrestrial biodiversity. Worldwide, only four countries exceed the ongoing rate of clearance of native vegetation in Australia (Williams et al. 2001). Rates of deforestation in New Zealand now are low, an inevitable conse­ quence given an estimated 80% loss of forest cover since human settlement. Forest loss in New Guinea, the Solomons, and Fiji continues, driven by demand from developed countries and weak central controls over logging permits and exports, and revenue collection (FAO 2000). In New Guinea, and throughout Melanesia (the Solomons, Bismarck Archipelago, and Vanuatu), Polhemus et al. (2004) have documented fresh­ water biotas threatened by alteration of aquatic

environments by logging, as well as mining and rapid human population growth. Effects of these activities on all regional freshwater insects include loss of shading by riparian vegetation, leading to elevated water temperatures, increased sedimentation and nutrient inputs, and more variable flows, including increased susceptibility to drought and flood. These mod­ ifications all lead to loss of native biodiversity, increased abundance and biomass of tolerant, sometimes alien, species, and growth of algae and often non‐native macrophytes. Replacement of native woody debris in streams with that of alien woody debris, such as from pines in Australian afforestation programs, has detri­ mental biodiversity effects, even as a riparian structure is retained (McKie and Cranston 1998). New Zealand’s deforestation seems to have caused diminished taxonomic richness, range restriction, and likely extinction of certain stream insects, as assessed at the nearly denuded, but endemism‐rich Banks Peninsula (Harding 2003). Conversion of native forests and pastures to impoverished agroecosystems dominated by alien annual grasses results in loss of native insect biodiversity. In this context, the day‐fly­ ing castniid sun‐moths (Synemon plana) have been invoked as flagship or umbrella insects (e.g., New 1997, Douglas 2004) for Australia’s ever‐diminishing native temperate grasslands, which are among its most threatened ecosys­ tems (Specht 1981). In subtropical and tropical Australian grasslands and savanna, threats to biodiversity include overgrazing by stock of native vegetation, especially in drought, and, controversially, land management by fire in sim­ ulations of putative natural fire regimes (Latz 1995, Anderson et al. 2005). 6.5.2  Introduced Animals

The sad history of the effects on native biodiver­ sity of introduced animals such as cats, goats, mongooses, rabbits, rats, and many others, especially on islands, is well known (e.g., Atkinson 1989). However, much documentation

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(and inference) relate to extinction or threats to native vertebrates, perhaps especially to ground‐ nesting birds. Only more recently has predator pressure on invertebrates (whether charismatic or not) reached the attention of conservationists and a wider public. Experimental exclosure, or removal, of vertebrate pests, shows that not only birds and lizards, but also large, flightless insects such as New Zealand’s wetās and regional stick insects, including the Lord Howe stick insect (on the vertiginous Ball’s Pyramid), can survive, even thrive, in the absence of four‐footed ver­ min. That feral animals have caused extinction is hard to verify, but can be surmised by evi­ dence such as the loss of the 15 cm wingspan Buller’s moth (Aoraia mairi), seen last by Sir Walter Buller in New Zealand’s Ruahine Range 120 years ago (while he hunted huia birds) (Meads 1990). Examination of fossil coleopteran remains provides evidence that some large spe­ cies such as the fern weevil Tymbopiptus valeas (Kuschel 1987) and a large ulodid beetle (Leschen and Rhode 2002) are now extinct and that large weevils were much more widespread in New Zealand in the past (Kuschel and Worthy 1996). Such evidence, combined with the fact that many similarly large flightless insects are now restricted largely to difficult‐to‐access, predator‐free offshore islands (Worthy 1997, Michaux and Leschen 2005) and Australia’s Lord Howe Island (Priddel et al. 2003), supports the view that vertebrate predators have been, and remain, major threats to large and edible insects. Where eradication of alien vertebrates has been successful, as on an increasing number of New Zealand’s offshore islands, the results have been spectacular, especially for native birds. A curious and unexpected effect includes the recovery of geckos, the dependence of which on scale‐insect honeydew had been masked by the presence of alien rats at this food source (Towns 2002). Although the effects of introduced vertebrates are visible and well‐documented disasters for biodiversity, a more insidious but just as serious threat comes from the ever‐expanding dis­ tribution of invasive insects. The numbers of

introduced insects can be gauged by data from New Zealand, the country with the greatest awareness and best monitoring systems for these threats. Thus, at the millennium, exotic insects included 229 beetles among nearly 1000 species sampled in and around suburban Auckland, 66 thrips in a total fauna of 119 spe­ cies, and some 100 species of aphids (Emberson 2000). Emberson (2000) argued that, by extrap­ olation, there must be more than 2500 adven­ tives, comprising about 13% of the New Zealand insect fauna. The point Emberson (2000) was making  –  that only 2.5% of these adventives were introduced for biological control purposes, with less than 1% comprising host‐specific, carefully screened insect species released and established for biological control of weeds – is important, but the numbers of exotic insects are quite staggering and are still increasing. The rain of Australian insects that descends on New Zealand after appropriate meteorological con­ ditions in the Tasman (Close et  al. 1978, Fox 1978) evidently leads to some establishment, including of phytophages on forestry plantation Eucalyptus (Withers 2001). Alien ants, none of which are native to Australasia, are among the worst of invasive animals. They create an insidious problem worldwide that threatens insect biodiversity, especially on Pacific islands where existing disturbance has predisposed habitat to inva­ sion (McGlynn 1999, LeBreton et al. 2005). On New Caledonia, the lethal effect of Wasmannia auropunctata on the native forest‐ant fauna was observed in invaded plots, where this New World invasive tramp ant represented more than 92% of all pitfall‐trapped ants (LeBreton et al. 2003). Eight months after the invasion front arrived, of the 23 prior resident native ant morphospecies (in 14 genera), only four cryptic species survived. Of particular concern in this study was that the invaded habitat was dense, pristine rainforest on ultra­ mafic soils, suspected previously of being more resistant to invasion. Such ecosystems, which support high biodiversity and narrow‐ range endemics, undoubtedly are massively

6  Biodiversity of Australasian Insects

disrupted when the native ant community is decimated  –  with ecosystem‐wide repercus­ sions likely to occur (LeBreton et  al. 2003). Such observations could be repeated through­ out the Australasian region as an invasive ant fauna, including Pheidole megacephala (the big‐headed ant), Solenopsis invicta (the red imported fire ant), Anoplolepis gracilipes (the yellow crazy ant), and Linepithema humile (the Argentine ant), threatens to spread. The economic and environmental costs associated with such invasions are well recognized, as when S.  invicta was discovered in suburban and industrial Brisbane, Australia, in 2001 (Vander­woude et  al. 2004). The species had probably been present undetected for several years already, stemming from two separate breaches of quarantine (Henshaw et al. 2005). With predictions of rapid spread across the continent (Scanlan and Vanderwoude 2006), a massive plan to eradicate the species was quickly put in place as the state (Queensland) and federal governments recognized and listed the presence of the red imported fire ant as a key threatening process to biodiversity. Through intensive baiting with methoprene and piriproxyfen, coupled with a massive pub­ lic awareness campaign, a 99% reduction had been attained by 2004. The costs for the six‐ year program were Aus$175 million, with a cost–benefit analysis showing potential costs of non‐eradication over 30 years of Aus$8.9 billion. Other introduced insects that threaten native biodiversity include honeybees (Apis melifera), the large earth bumblebee (Bombus terrestris), European wasps (Vespula spp.), and the Asian and Australian paper wasps (Polistes chinensis and Polistes humilis). Honeybees take over hol­ lows in trees for nesting and compete with native animals, including native bees, for floral resources (Goulson 2003), leading to their pres­ ence and activities being recognized as a key threatening process in New South Wales, Australia (NSW NP and WS 2011). Recognition of B. terrestris as threatening stems from its role as a pollinator of many environmental weeds

and a potential disruptor of native plant pollina­ tion, based on experiences in Tasmania and New Zealand (NSW NP and WS 2011). In New Zealand, wasps pose a major prob­ lem: P. humilis became abundant in Northland in the 1880s and remains in the north. German wasps (Vespula germanica) arrived in the 1940s and spread to the South Island 10 years later, whereas Vespula vulgaris became estab­ lished in the 1970s, and both are now wide­ spread. The most recent arrival, the Asian paper wasp (P. chinensis), was found first near Auckland in 1979, and is rapidly extending its range southward. Problems with effects of wasps on native biodiversity are particularly significant in the Nothofagus beech forests, where abundant honeydew, produced by endemic coccoids (Coelostomidiinae), pro­ vides an abundant source of carbohydrate. This resource, on which a community of hon­ eydew‐feeding native birds once thrived, has been hijacked by Vespula, particularly V. vul­ garis. Extraordinary wasp densities of 10,000 workers ha−1 and peak biomass of 3.8 kg ha−1 can develop by the late summer (Beggs 2001). Wasp demand for protein is nearly insatiable, such that for many invertebrate prey items, such as caterpillars, individual survivorship probability is near zero (Beggs and Rees 1999). Wasp densities need to be reduced by an esti­ mated 80–90% to conserve vulnerable native species, but even mass baiting with the effec­ tive fipronil and the introduction of an ichneu­ monid wasp parasitoid is unlikely to sustain such high levels of control (Beggs 2001). Asian paper wasps in warm and humid northern New Zealand can develop densities of more than 6300 wasps and 200 nests ha−1 and con­ sume 1 kg ha−1 of invertebrate biomass per season, giving rise to fears of severe effects on native ecosystems (Clapperton 1999). Control of this species is even more difficult than for Vespula because nests are difficult to find due to their location in dense bush and the infre­ quent traffic of wasp residents, and numbers of wasps are reduced only minimally by baiting and trapping (Toft and Harris 2004).

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6.5.3  Climate Change

The history of the Earth includes cyclical cli­ mate change, some of which has been induced by volcanism and solar cycles, interspersed with episodic bolide impacts. The planet is recover­ ing still from the effects of the Pleistocene gla­ ciations of much of the mid‐high latitudes of the northern hemisphere. In Australia, the Holocene period has seen reduced temperatures and increased aridity, although any linkage to northern climate variations remains unverified (Turney et  al. 2006). Nonetheless, Australian Holocene climate changes affected vegetation (with increased xeric conditions producing rainforest contraction and assisting spread of sclerophylous, Eucalyptus‐dominated vegeta­ tion). The insect biota was affected too, as dis­ tributions shifted in latitude and elevation with changing temperatures (Porch and Elias 2000 (Coleoptera), Dimitriadis and Cranston 2001 (Chironomidae)). In New Zealand the same organisms also show historical changes (Marra et  al. 2004, 2006; Woodward and Shulmeister 2007), although the causes and synchronicity might be dissimilar to those in Australia (Alloway et  al. 2007), as they relate mostly to extensive volcanism in New Zealand. In both Australia and New Zealand, El Niño–Southern Oscillation (ENSO) events have been important in the past and remain influential. Despite this background variability, the Australian govern­ ment accepted that alteration to Australia’s cli­ mate already occurs over and above natural variability (Natural Resource Management Ministerial Council 2004). Changes such as long‐term spatial and temporal variation in rainfall and temperature patterns are expected to influence Australia’s biological diversity (Natural Resource Management Ministerial Council 2004). A widely accepted scenario of 3 °C warming by 2050–2100, for example, com­ pared with a 1990 baseline (IPCC 2001, Hughes 2003), means that species with latitudinal ranges of less than about 300 km or with an elevation range less than about 300 m will dissociate totally from their present‐day temperature

envelopes (Westoby and Burgman 2006). In other words, their present‐day distributions could not be maintained. Federal acceptance of the scientific consensus concerning such expected effects on species (and ecosystems) under future climate scenarios came from a growing list of changes consistent with predic­ tions. Inevitably, perhaps because of their ecto­ thermy, some of these changes involve insects. As in the northern hemisphere, the extensive databases for butterfly locations and flight dates have provided a foundation against which changes can be assessed. Using bioclimatic modeling for 77 species of Australian butter­ flies, Beaumont and Hughes (2002) showed that, although few species had narrow climatic ranges (4,000

Nast 1972; A. F. Emeljanov, personal communication

Hemiptera– Heteroptera

8,413

Aukema and Rieger 1995, 1996, 2001, 2006; Schuh and Slater 1995

Coleoptera

100,000

Löbl and Smetana 2003–2011; I. Löbl, personal communication; A. L. Lobanov, personal communication

Neuropterida

824

V. A. Krivokhatsky, personal communication

Raphidioptera

110

V. A. Krivokhatsky, personal communication

Megaloptera

38

V. A. Krivokhatsky, personal communication

Hymenoptera “Symphyta”

1,384 (USSR)

A. L. Lobanov, personal communication

Hymenoptera Apocrita

24,310

S. A. Belokobylsky, personal communication; O. V. Kovalev, personal communication; Yu. A. Pesenko, personal communication; Davidian 2007; Fursov 2007; Grissell 1999; Jasnosh 1995; Kimsey and Bohart 1990; Kurzenko 1995; Lelej 1995a, 1995b, 2002; Nemkov et al. 1995; Pesenko 1983; Radchenko 1999; Sharkov 1995; Storozheva et al. 1995; Trjapitzin 1989; Yu and Horstmann 1997; Zerova 1995

Mecoptera

>42 (USSR)

A. L. Lobanov, personal communication (Continued)

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Table 7.2  (Continued) Order/suborder

Number of species

Source

Trichoptera

2,530

Morse 2008

Lepidoptera

25,000

Heppner 1998; S. Yu. Sinev, personal communication

Siphonaptera

900

S. G. Medvedev 1998

Diptera

40,291

Nartshuk 2003

Total

193,057

—

unique in their southern parts (Kryzhanovsky 2002), where Afrotropical, Oriental, and Neotropical elements contribute significantly to the biodiversity. A few high‐ranked groups of insects are endemic to the Holarctic: the family Grylloblattidae (western North America, Japan, Russian Far East; with one species in the Altai mountains and one in the Sayan mountains, southern Siberia); and the beetle families Amphizoidae (mountain streams of North America, and northwestern and eastern China) and Sphaeritidae (three species in the taiga of Eurasia, mountains of Sichuan, and north­ western North America). The range of the order Raphidioptera is limited almost entirely to the Holarctic. Lindroth (1957) lists land and freshwater animal species common to Europe and North America. Despite its similarity to the Nearctic, however, the Palearctic is tradi­ tionally regarded as a separate region (Sclater 1858, Darlington 1963, Emeljanov 1974, Vtorov and Drozdov 1978, Krivokhatsky and Emeljanov 2000). Insect diversity in the Palearctic is influenced by diverse climatic and other geographic condi­ tions that exhibit a well‐developed zonality. Temperature gradients are mainly responsible for the Arctic, Boreal, and Subtropical latitudi­ nal belts. The following main zones are distrib­ uted from north to south in the western part of the Palearctic: tundra, taiga, mixed and broadleaf (nemoral) forest, dry sclerophyll ­ Mediterranean‐type forest, wet subtropical for­ est, steppe, and desert. Most mountain ranges demonstrate successive series of climatic altitudinal belts similar to lowland zonality. ­ Atmospheric circulation and variations in pre­

cipitation yield the Atlantic, Continental, and Pacific longitudinal sectoral groups (Emeljanov 1974). The Atlantic sectoral group is character­ ized by two types of climate: Mediterranean, with maximum precipitation in the winter, and boreal, with maximum precipitation in the summer. The Pacific sectoral group has a mon­ soon climate with maximum precipitation dur­ ing the summer. The boundary between the Atlantic and Pacific sectoral groups is usually drawn along the Yenisei River, Tien Shan moun­ tains, and west of the Indus River in the south. The easternmost sectors of the Atlantic group and westernmost sectors of the Pacific group along this boundary, where the oceanic influ­ ence is drastically weakened, are characterized by lower precipitation and greater temperature fluctuations between summer and winter (con­ tinental and supercontinental climate); these sectors can be grouped as the Continental sec­ toral group. Continental climate is responsible for the taiga spreading southward and the steppe northward, squeezing out nemoral and subtropical zones in the Continental sectors (Emeljanov 1974). Continentality is one of the most important factors in Palearctic faunal dif­ ferentiation, splitting subtropical and nemoral zones into two isolated fragments with rather different yet, in part, closely related insect fau­ nas. In the easternmost Pacific sector, high humidity is responsible for the lack of semide­ sert and desert areas and the large southern extension of mixed coniferous and broadleaf forests that are impoverished northward, because of elimination of broadleaf elements, and that gradually change to subtropical forests southward.

7  Insect Biodiversity in the Palearctic Region

(a)

(b)

(c)

(d)

(e)

Figure 7.1  (a) Main divisions of the Palearctic Region (after Emeljanov 1974, simplified). I, Arctic (Circumpolar tundra) region; II, Taiga (Euro‐Siberian) region; III, European (nemoral) region; IV, Stenopean (nemoral) region; V, Hesperian (evergreen forest) region; Va, Macaronesian subregion; Vb, Mediterranean subregion; VI, Orthrian (evergreen forest) region; VII, Scythian (steppe) region; VIIa, West Scythian subregion; VIIb, East Scythian subregion; VIII, Sethian (desert) region; VIIIa, Saharo‐Arabian subregion; VIIIb, Irano‐Turanian subregion; VIIIc, Central Asian subregion. (b) Northern Russia, Yamal Peninsula (photo A. K. Tishechkin). (c) Northeastern Russia, Magadan Province, northern taiga (photo D. I. Berman). (d) Russia, Smolensk District, Ugra River near Skotinino Village, mixed forest (photo A. Konstantinov). (e) Russia, Caucasus (photo M. Volkovitsh).

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7.4 ­General Features of Palearctic Insect Biodiversity Roughly 200,000 species of insects are known in the Palearctic Region  –  about one‐fifth of the total number of insect species in the world (Table 7.2) (Konstantinov et  al. 2009). About half of all insects in the Palearctic are beetles. This estimate is far from final: hundreds of new species are described in the Palearctic every year. In recent years, parasitic Hymenoptera have been described most intensively, with 686 new species of Braconidae described from the Far East and neighboring areas in two volumes of the Key to Insects of the Russian Far East by S. A. Belokobylsky and V. I. Tobias (1998, 2000), which include 2593 species. In the largest family of parasitic flies, the Tachinidae, more than 680 species are included in the key to the Far Eastern fauna (Richter 2004), with 39 species and nine genera described during the preparation of the key. Most Palearctic species do not occur outside the region. In the Diptera (Fig. 7.2c), the major­ ity of species are Palearctic endemics. The per­ centage of endemic genera, and especially family‐group taxa, is much less. Only four fami­ lies of Diptera are endemic to the region (Nartshuk 1992): Eurygnathomyiidae, Phaeo­ myiidae, Risidae, and Stackelbergomyiidae. Of these, only the Phaeomyiidae or Risidae are gen­ erally accepted as distinct families; the others usually are treated as subfamilies or tribes (Sabrosky 1999, Courtney et al. this volume). One of the most obvious features of insect biodiversity in the Palearctic is its sharp increase from north to south, corresponding to the most fundamental pattern of life on Earth (Willig et al. 2003). For example, the Orthoptera (Fig. 7.2e, Fig. 7.3e), Blattodea, Dermaptera, Mantodea, and Phasmatodea are represented by 72 species in the forests, 171 species in the steppes, and 221 species in the deserts of the former USSR (Iablokov‐Khnzorian 1961). The insect fauna of the Palearctic is slightly depauperate at the order, family, and genus ­levels (compared to most other regions), but it has high species richness: that is, the number

of higher taxa with only a single species in the Palearctic is relatively low and the relative number of species per higher taxon is large. In this regard, it is similar to island faunas charac­ terized by a small number of introductions that were followed by extensive species‐level radia­ tions (Magnacca and Danforth 2006). The Palearctic and Oriental regions have about the same number of species of flea beetles (Chrysomelidae: Alticini) (about 3000, although the Oriental fauna is much less known), but differ sharply in generic diversity, with about 60 genera in the Palearctic and 220 in the Oriental fauna. Most flea‐beetle species richness in the Palearctic is concentrated in a few large, nearly cosmopolitan genera (e.g., Aphthona; Konstantinov 1998). Historically, the Palearctic fauna probably was derived from the ancient fauna of Laurasia, dra­ matically changed by the aridization of the Tertiary, but primarily by the Quaternary glaci­ ation (Lopatin 1989), which includes the largest global glaciations of the upper Pliocene and Pleistocene. Also important were fluctuations of sea level, which led not only to changes in coast lines, but also to formation of a variety of land bridges between continents and various islands, and the alpine orogenesis during which the largest mountain systems in Europe and Asia appeared (Kryzhanovsky 2002). These cli­ matic and geomorphological changes might explain the appearance of a Tibetan scarab, Aphodius holdereri Reitter, in England (Coope 1973); disjunct distributions of the helophorid beetle Helophorus lapponicus Thompson between its main range (Scandinavia to Eastern Siberia) and relict populations in mountainous areas of Spain, Transcaucasia, and Israel and Lebanon (Angus 1983); and the current restric­ tion of the water beetle Ochthebius figueroi Garrido et al., known from Pleistocene deposits in England, to a small mountain area in north­ ern Spain (Angus 1993). Insect biodiversity has a particular pattern in space and time. The distribution of specialized herbivores closely associated with specific plants and plant communities often reveals a more distinct pattern than does the distribution

7  Insect Biodiversity in the Palearctic Region

(a)

(b)

(c)

(d)

(e)

(f)

(g)

Figure 7.2  Palearctic insects in natural habitats. (a) Calosoma sycophanta (L.) (Coleoptera: Carabidae) (Turkey) (photo A. Konstantinov). (b) Nemoptera sinuata Olivier (Neuroptera: Nemopteridae) (Turkey) (photo M. Volkovitsh). (c) Eristalis tenax L. (Diptera: Syrphidae) (Turkey) (photo A. Konstantinov). (d) Cryptocephalus duplicatus Suffrian (Coleoptera: Chrysomelidae) (Turkey) (photo A. Konstantinov). (e) Poecilimon sp. (Orthoptera: Tettigoniidae) (Turkey) (photo M. Volkovitsh). (f ) Capnodis carbonaria (Klug) (Coleoptera: Buprestidae) (Turkey) (photo M. Volkovitsh). (g) Cyphosoma euphraticum (Laporte and Gory) (Coleoptera: Buprestidae) (southern Russia) (photo M. Volkovitsh). (See color plate section for the color representation of this figure.)

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(a)

(b)

(c)

(d)

(e)

(f)

Figure 7.3  Palearctic insects in natural habitats. (a) Julodis variolaris (Pallas) (Coleoptera: Buprestidae) (Kazakhstan) (photo M. Volkovitsh). (b) Julodella abeillei (Théry) (Coleoptera: Buprestidae) (Turkey) (photo M. Volkovitsh). (c) Mallosia armeniaca Pic (Coleoptera: Cerambycidae) (Turkey) (photo M. Volkovitsh). (d) Trigonoscelis schrencki Gebler (Coleoptera: Tenebrionidae) (Kazakhstan) (photo M. Volkovitsh). (e) Saga pedo Pallas (Orthoptera: Tettigoniidae) (Kazakhstan) (photo M. Volkovitsh). (f ) Piazomias sp. (Coleoptera: Curculionidae) (Kazakhstan) (photo M. Volkovitsh). (See color plate section for the color representation of this figure.)

of insects with other food specializations. Changes in the Curculionoidea (Coleoptera) fauna along a 160 km transect that crosses six types of desert plant communities in the Trans‐ Altai Gobi Desert in Mongolia illustrate this pattern (Table 7.3). Two types of plant commu­ nities exist at the extremes of the profile, a

northern steppefied desert and a southern extra‐arid desert type. The numbers of weevil species at the extremes do not differ sharply (17 in the north and 11 in the south), but only one  species, Conorhynchus pulverulentus (Zoubkoff ), occurs in all types of desert. All northern species gradually disappear s­ outhward,

7  Insect Biodiversity in the Palearctic Region

Table 7.3  Distribution of Curculionoidea across six types of desert plant communities in Trans‐Altai Gobi, Mongolia. Steppe species (+)

6†

—

*

—

*

5

4

3

2

* *

Cionus zonovi Korotyaev

+

*

*

+

*

*

*

*

Macrotarrhus kiritshenkoi Zaslavsky

+

*

Philernus gracilitarsis (Reitter)

+

*

Pseudorchestes convexus Korotyaev

+

*

*

Stephanocleonus paradoxus (Fåhraeus)

+ +

+

Desert species (*)

Pseudorchestes furcipubens (Reitter)

*

Eremochorus inflatus (Petri)

Fremuthiella vossi (Ter‐Minassian)

1

*

*

Deracanthus faldermanni Faldermann *

Deracanthus hololeucus Faldermann

*

Mongolocleonus gobianus (Voss)

*

Temnorhinus oryx (Reitter)

*

Stephanocleonus helenae (Ter‐Minassian)

*

Elasmobaris alboguttata (Brisout)

*

*

*

Perapion ?myochroum (Schilsky)

*

*

*

Perapion centrasiaticum (Bajtenov)

*

*

Anthypurinus kaszabi (Bajtenov)

Stephanocleonus potanini Faust

+

+

*

Stephanocleonus inopinatus (Ter‐Minassian)

+

+

*

Lixus incanescens Boheman

Stephanocleonus excisus Reitter

+

+

*

Sibinia sp. pr. beckeri Desbrochers

Stephanocleonus persimilis Faust Gronops semenovi Faust

+ +

*

Cosmobaris scolopacea (Germar)

+

Eremochorus mongolicus (Motschulsky)

+

+

+

Conorhynchus pulverulentus (Zoubkoff )

+

+

+

* +

+

Oxyonyx kaszabi Bajtenov

*

Platygasteronyx humeridens (Voss)

+*

Platygasteronyx macrosquamosus Korotyaev

Extrazonal community of Reaumuria soongorica (#) Corimalia reaumuriae (Zherichin)

#

Coniatus zaslavskii Korotyaev Coniatus minutus Korotyaev

#

#

#

—

#

#

—

#

#

—

† Numbers 6 to 1 indicate desert plant communities from north (6) to south (1): 6, Anabasis brevifolia steppefied desert; 5, Reaumuria soongorica + Sympegma regelii desert; 4, Haloxylon ammodendron desert; 3, Reaumuria soongorica + Nitraria sphaerocarpa desert; 2, extra‐arid Iljinia regelii desert; 1, extra‐arid Ephedra przewalskii + Haloxylon ammodendron (in dry temporary waterbeds) desert.

being substituted by southern species, in accordance with vegetation changes. The distri­ butions of (mostly predatory) carabids and ­non‐specialized phyto‐ and detritophagous ten­ ebrionid beetles mostly depend on climate, chemical and mechanical properties of the soil, and vegetation density; they follow vegetational changes less closely, but exhibit similar patterns. In some of these communities, tenebrionids are more diverse than are weevils; however, differ­ ent types of desert communities differ more sig­ nificantly in weevil species composition, and

the total weevil diversity in the Trans‐Altai Gobi exceeds that of tenebrionids. Different natural zones, particularly the Arctic, are characterized by the dominance of some higher insect taxa. The majority of the Arctic chrysomelid fauna is composed of 25 species of a single subfamily, the Chrysomelinae (with 12 species in the genus Chrysolina; Chernov et al. 1994), although a few boreal species of Cryptocephalinae and Galerucinae contribute to the hypoarctic leaf‐beetle fauna (Medvedev and Korotyaev 1980). The ­taxonomic pattern of the

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biogeographical regions has a historical ­background, but the zonal peculiarities of the faunas are largely due to specific requirements of the taxa. In the holometabolous insects, these requirements are related primarily to the envi­ ronmental conditions appropriate for larval development. An example is the chrysomelid fauna of the Trans‐Altai Gobi Desert in Mongolia. Ten species of Chrysomelidae, out of the 14 species found in the six types of desert‐ plant community (Korotyaev et al. 2005), belong to the tribes Cryptocephalini, Clytrini, and Cassidini. The case‐bearing (Cryptocephalini) and sheltered (Clytrini) larvae are better adapted to the xeric environment than are the ectophytic larvae of the Chrysomelinae and Galerucini or soil‐inhabiting larvae of the Eumolpinae and some Alticini. Another feature of insect biodiversity in the Palearctic is its organization in time. Nearly all regions of the Palearctic are subjected to strong seasonal changes in temperature and precipita­ tion. Long periods of fall and winter are charac­ terized by minimal insect activity. Some of the most‐typical winter insects are representatives of the Holarctic family Boreidae, the snow scor­ pionflies (Boreus). These small mecopterans (Fig. 7.4g) appear in the fall and winter and often hop and walk on the snow. On the Russian Plain, maximum insect biodiversity of herbi­ vores is found in late May and in June. The tax­ onomic composition of any local fauna also changes with time. A number of species are active only in early spring, particularly those in southern, more xeric regions of the Palearctic. Examples include flightless black Longitarsus (Chrysomelidae) species associated with ephemeral plants, and in their flightless fea­ tures, they are similar to alpine members of the genus (Konstantinov 2005). The maximum bio­ diversity of adult weevils in the steppe of the Northwestern Caucasus precedes the maxi­ mum local air temperature and precipitation, which might mean that the phenology of holo­ metabolous herbivores is adjusted to the maxi­ mum supply of warmth and water for the larval stage. Late maturation of hemimetabolous

insects (orthopterans, bugs, and leafhoppers) fits this speculation: the development of their larvae and nymphs proceeds in the warmest part of summer. The fauna of open landscapes in the Palearctic is highly diverse, even in groups associated predominantly with woody vegeta­ tion. In some cases, large genera of families that tend to be most species rich in woodlands are instead confined to open landscapes. The best illustration is the largest genus of the mostly xylophagous family Cerambycidae, the endemic Dorcadion: all 300‐plus species occur in meso‐ to xerophytic grasslands. No genus of dendrophilous cerambycids has comparable diversity in the Palearctic. The leaf‐mining weevil tribe Rhamphini, with more than 160 Palearctic species in 13 genera on trees and bushes, has its largest subendemic genus in the region (with one species in Namibia). This subendemic genus, Pseudorchestes, has 34 described and dozens of as‐yet‐undescribed species that develop on herbaceous plants and semishrubs of the Asteraceae. Among the predatory beetles, the lady‐beetle genus Tetrabrachys (= Lithophilus) of the endemic subfamily Lithophilinae, with 51 species (Iablokoff‐Khnzorian 1974), is the largest in the region. The vast majority of its species are confined to xeric areas of the southern Palearctic, mostly in the western half. Most species in the second largest genus in the region, Hyperaspis, with more than 30 species, also are distributed in dry, open landscapes. The great diversification of the open‐land­ scape Hyperinae and Lixinae, compared with just a few typically woodland species of these large subfamilies of the Curculionidae, is also characteristic, as is the absence of dendrophil­ ous Baridinae in the western and central Palearctic; the baridine fauna associated with herbs, however, is fairly species rich. The same tendency also is obvious in the Alticini (Chrysomelidae), Cassidinae (Chrysomelidae), and the subfamily Ceutorhynchinae, tribes Cionini and Tychiini of the Curculioninae, and Sitonini of the Entiminae (Curculionidae).

7  Insect Biodiversity in the Palearctic Region

(c)

(b) (a)

(d)

(e)

(f)

(g)

Figure 7.4  Coleoptera and Mecoptera. (a) Aphthona coerulea Goeze (Coleoptera: Chrysomelidae). (b) Clavicornaltica dali Konstantinov and Duckett (Coleoptera: Chrysomelidae). (c) Mniophila muscorum Koch (Coleoptera: Chrysomelidae). (d) Kiskeya baorucae Konstantinov and Chamorro‐Lacayo (Coleoptera: Chrysomelidae). (e) Cryptocephalus ochroloma Gebler (Coleoptera: Chrysomelidae). (f) Margarinotus (Kurilister) kurbatovi Tishechkin (Coleoptera: Histeridae). (g) Boreus hyemalis (L.) (Mecoptera: Boreidae).

The similarity between the fauna of open landscapes in the Nearctic and the faunal counterpart in the Palearctic is rather low. The  Nearctic has greater representation of the  ­ predominantly tropical weevil families Anthribidae and Dryophthoridae and the sub­ family Conoderinae of the Curculionidae, whereas the Hyperinae, Lixinae, Cyclominae, Rhythirrinini, Tychius, and many taxa of the Entiminae that dominate grassland communi­

ties in the Palearctic are absent or subordinate in the Nearctic.

7.5 ­Biodiversity of Some Insect Groups in the Palearctic Most of the large orders have wide representa­ tion in the Palearctic. More than 100,000 spe­ cies of beetles, for example, occur in the region.

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The other most species‐rich orders are Diptera, Hymenoptera, and Lepidoptera. Higher taxa with different types of food specialization gain richness in the Palearctic, including its northern parts. Parasitic wasps, for example, are repre­ sented by a greater number of species than is the entire order Coleoptera in the British Isles (LaSalle and Gauld 1991, cited by Sugonyaev and Voinovich 2006). The less‐specialized pred­ atory, mycophagous, and phytophagous fungus gnats (Mycetophilidae) and highly specialized phytophagous sawflies (Tenthredinidae) have enormous faunas, with 645 species in Karelia (Polevoi 2007) and about 800 species in Finland (A. G. Zinovjev, personal communication), respectively. Many higher taxa of noxious blood‐sucking insects, such as the orders Siphonaptera and “Phthiraptera” and the dip­ teran families Culicidae, Ceratopogonidae, Simuliidae, Tabanidae, Oestridae, and Hippoboscidae, are widely represented in the Palearctic. Of the blood‐sucking Diptera that transmit dangerous disease agents, only the Glossinidae with their infamous tsetse are absent, and the Psychodidae are restricted to the southernmost regions of the Palearctic. The Palearctic Siphonaptera fauna, with 900 species, is the largest in the world, comprising 40% of the world species and genera, although only one monotypic subfamily, with 19 species, is endemic (S.G. Medvedev 1998). Scale insects (Coccina), most conspicuous in the tropical for­ ests, are less abundant and diverse in the Palearctic but are present in all climatic zones, including the Arctic. Entomophagous wasps of the superfamily Chalcidoidea, which are associ­ ated with scale insects, have developed a special strategy of host use in the high latitudes that dif­ fers from the strategy used in the tropics (Sugonyaev and Voinovich 2006). A few orders, largely contributing to the fau­ nas of the adjacent tropical regions, and all belonging to the Orthopteroidea, are poorly represented in the Palearctic: Blattodea, Dermaptera, Mantodea, and Phasmatodea. Most higher taxa of Palearctic Orthoptera are widely distributed in the tropics, but a few sub­

families are mainly Palearctic (Deracanthinae, Glyphonotinae, Onconotinae, Pamphaginae, and Thrinchinae). Among tribes, the Chryso­ chraontini, Conophymatini, Drymadusini, Gampsocleidini, and Odonturini are endemic. Almost all the taxa in these groups have their centers of diversity and endemism in the south­ ern Palearctic (Sergeev 1993). For many large family‐group taxa, the Palearctic contains a relatively small percentage of the world fauna. For example, the beetle fam­ ily Buprestidae (Fig. 7.2f,g) comprises 2430 spe­ cies in 99 genera in the Palearctic – approximately 17% of the species and 20% of the genera in the world (Bellamy 2003, Löbl and Smetana 2006). The large group of phytophagous flea beetles (Chrysomelidae, Alticini), with about 11,000 species and 600 genera worldwide, is repre­ sented in the Palearctic by about 2400 species and 64 genera. Yet only a few genera of the Alticini are endemic to the Palearctic; most of them are distributed in the mountains of south­ ern Europe, the Caucasus, and the Mediterranean (Konstantinov and Vandenberg 1996). Many Oriental and some Afrotropical genera are represented by only a few species in the Palearctic at the eastern or southern borders of the region. The subfamily Ceutorhynchinae of the Curculionidae – similar to the Alticini in many ecological features and range of body size – had 1316 described species as of 2003, and includes Palearctic representatives of 12 of 14 tribes (Colonnelli 2004), with only two Paleotropical tribes (Lioxyonychini and Hypohypurini) absent from the region. About half of the species of this worldwide subfamily and 102 of the total 167 genera occur in the Palearctic; 79 genera and two tribes are Palearctic endemics. For many boreal and temperate groups, the Palearctic has the most species‐rich fauna. The family Cecidomyiidae (Diptera), for example, has 3057 species in the Palearctic compared with only 533 species in the Neotropics (Gagne 2007). This trend also holds for aphids, which are mostly Holarctic; their complicated life cycle is possibly an adaptation to a temperate climate.

7  Insect Biodiversity in the Palearctic Region

The Ichneumonidae (Hymenoptera) have a sim­ ilar distribution of diversity. They are richer in the northern hemisphere, particularly in the Palearctic. The tribe Exenterini, for example, is distributed almost entirely in the Holarctic, with all genera represented in the Palearctic (Kasparyan 1990). Many species have wide transpalearctic ranges that are almost entirely confined to forest regions. Most (Kasparyan 1990) are parasites of various Tenthredinidae (Hymenoptera), which are also rich in species in the Palearctic. Taeger et al. (2006) counted 1386 species of sawflies in Europe, 220 species in Norway, and eight in Novaya Zemlya. For China, the estimate is 2600 species and 350 gen­ era (Wei et al. 2006). Aquatic and amphibiotic insect groups are also rich in the Palearctic. About one‐third of the world’s blood‐sucking Simuliidae, all with aquatic larvae, are distributed in the Palearctic (Adler and Crosskey 2015). The Chironomidae, with their predominantly aquatic larvae, also are species rich in the Palearctic, dominating the Arctic aquatic complexes and including the northernmost dipterans (also southernmost in Antarctica; Nartshuk 2003). For Russia, the following species numbers are available for the largest insect orders (partly including the fauna of neighboring countries): Ephemeroptera, about 300 species (N. Ju. Kluge, personal com­ munication); Odonata, 148 species (Kharitonov 1997); Plecoptera, 225 species (Zhiltzova 2003); Megaloptera, 15 species (Vshivkova 2001); Trichoptera, 652 species (Ivanov 2007); Neuropterida, 11 species (Krivokhatsky 2001); Lepidoptera, eight species (Lvovsky 2001); Coleoptera, about 700 species (Kirejtshuk 2001); and Hymenoptera, 24 species (Kozlov 2001). Of the Plecoptera, the Euholognatha include a large number of taxa endemic to the Palearctic, such as the Scopuridae, with a sin­ gle genus of five species. The Taeniopterygidae and Capniidae contain many genera endemic to the Palearctic (six of 13 worldwide and seven of 17, respectively). Only one family, the Notonemouridae, with 69 species, is absent from the Palearctic, being distributed in the

Neotropics, Australia, and Africa south of the Sahara (Zhiltzova 2003). The ranges of many Palearctic species are relatively small, such as that of Capnia kolymensis Zhiltzova from the Kolyma River and several species of Nemoura from Iturup Island. The distributions of many species associated with cold water are restricted to mountain systems (the Alps, Carpathians, Caucasus, and Tien Shan). Their endemism at the species level reaches 60% (Zhiltzova 2003). Endemism of other aquatic insect groups, such as the Trichoptera, is esti­ mated at 36% (Zhiltzova 2003). The Palearctic is among the few places on Earth where a rare group of flies is distributed. The family Canthyloscelidae, for example, has a single genus (Hyperoscelis) with three species in the Palearctic and two other genera with four species in southern South America and four species in New Zealand (Nartshuk 1992). Among the widely distributed families of flies, several are known from the Palearctic but are absent in the Nearctic: the “acalyptrate” Camillidae, Cryptochetidae, Megamerinidae, and Xenasteiidae. Almost all are widely distrib­ uted in the Oriental or Afrotropical regions. The Nearctic has seven families of flies not known from the Palearctic. The recently estab­ lished family Xenasteiidae in the Palearctic occurs in the Mediterranean and also on the islands of the Indian and Pacific Oceans. The Apioceridae are known from all regions except the Palearctic (Nartshuk 1992). Many endemic Palearctic higher taxa have relatives in either the Nearctic or the temperate areas of the southern hemisphere. The weevil subfamily Orobitidinae, in addition to the oligo­ typic Palearctic genus Orobitis associated with Viola plants, includes the genus Parorobitis (Fig. 7.5c), with a few species (hosts unknown) in tropical South America (Korotyaev et  al. 2000), where the Violaceae are represented by more than 300 species (Smith et al. 2004). Small insect families contribute considerably to the insect biodiversity of the Palearctic Region. Scorpionflies (Mecoptera), although neither speciose nor abundant, are common in

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(a)

(c)

(b)

(d)

Figure 7.5  Coleoptera. (a) Carabus lopatini Morawitz (Coleoptera: Carabidae). (b) Cimberis attelaboides (F.) (Coleoptera: Nemonychidae). (c) Parorobitis gibbus Korotyaev, O’Brien and Konstantinov (Coleoptera: Curculionidae). (d) Theodorinus lopezcoloni Korotyaev and Alonso‐Zarazaga, 2010. (Coleoptera: Curculionidae).

mixed and nemoral European forests, and the Sialidae (Megaloptera) are a conspicuous com­ ponent of the European riparian landscape. A relatively small beetle family, the Trogossitidae, includes the worldwide synanthropic Tenebrioides mauritanicus L., which is injurious to stored products. Ostoma ferrugineum (L.) and a few species of the genera Peltis and Thymalus frequently are found under bark in all types of Palearctic forests except the northern­

most taiga. Larvae of one of the two European representatives of the beetle family Byturidae in some years destroy a considerable part of the raspberry harvest. The European Dascillus cervinus (L.) and the Caucasian Dascillus elongatus Faldermann of the small family Dascillidae are abundant under the forest canopy for short periods of their adult lives. Their Eastern Palearctic ally, Macropogon pubescens Motschulsky, is one of the few common beetles

7  Insect Biodiversity in the Palearctic Region

around bushes of Pinus pumila Regel in the hills of the middle Kolyma Basin (Northeast Asia), which has an impoverished insect fauna. Mycterus curculionides (F.) of the small family Mycteridae often dominates assemblages of medium‐sized beetles in the mid‐summer dry grasslands of the Western Palearctic. Two myco‐detritophagous families of small beetles, Cryptophagidae and Latridiidae, include several hundred brown beetles, all rather uniform in appearance. They occur almost everywhere except the northern tundra and are especially abundant in wet riparian litter. These families, as well as the predomi­ nantly mesohygrophilous and rather uniform Helodidae (= Cyphonidae), illustrate a tendency that the least conspicuous taxa often have the greatest species richness. Many staphylinid bee­ tles fit this trend, including those that live in the open (e.g., Stenus) and the cryptobionts (e.g., small Aleocharinae). The largest genus of the Alticini in the Palearctic, Longitarsus, with 221

species in the region (29 species only on Mount Hermon in Israel; Chikatunov and Pavlíček 2005), is not particularly diverse morphologi­ cally. One of the largest genera of weevils in the Palearctic, Ceutorhynchus, with about 300 spe­ cies, is also morphologically less diverse, com­ pared with the showy Oriental Mecysmoderes from the same subfamily. Of special interest are the relations between phytophagous insects using the same or similar food resource. Examples include co‐occurring weevils (Lixus and Melanobaris) whose larvae share similar locations and habits in the host (Korotyaev and Gültekin 2003). The distribu­ tion pattern of three weevil taxa (the genus Bruchela of the Anthribidae, and the subfami­ lies Ceutorhynchinae and Baridinae of Cur­ culionidae) across their hosts in northeastern Turkey (Korotyaev 2012; Table 7.4) shows no antagonism in host association at the genus and family levels in large taxa of highly specialized herbivores.

Table 7.4  Host plants of Bruchela (Coleoptera: Anthribidae: Urodontinae) in European Russia, Caucasus, and neighboring territories of northeastern Turkey, and weevils (Curculionidae) of the subfamilies Ceutorhynchinae and Baridinae associated with them (modified from Korotyaev 2012). Curculionidae Species of Bruchela

Host plant

Subfamily Baridinae

Subfamily Ceutorhynchinae

—

B. rufipes Ol.

Reseda lutea

Aulacobaris picitarsis Marsh.

B. suturalis F.

R. lutea

A. picitarsis

—

B. anatolica Pic

Sisymbrium orientale

Melanobaris atramentaria Boh.

Ceutorhynchus chalibaeus Germ.

—

Sisymbrium loeselii

Melanobaris hochhuthi Fst.

Ceutorhynchus spp.

B. orientalis Strejček S. orientale

M. atramentaria

C. chalibaeus

B. muscula K. Daniel S. orientale and J. Daniel

M. atramentaria

C. chalibaeus

B. schusteri Schils.

Erysimum canescens

M. atramentaria

—

—

Erysimum pulchellum

M. atramentaria

—

—

Erysimum sp.

Melanobaris nigritarsis Boh.

—

B. parvula Motsch.

Descurainia sophia

—

Ceutorhynchus sophiae Gyll., Ceutorhynchus spp. (Continued)

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Table 7.4  (Continued) Curculionidae Species of Bruchela

Host plant

Subfamily Baridinae

Subfamily Ceutorhynchinae

B. exigua Motsch.

Isatis ? tinctoria

M. nigritarsis, Aulacobaris coerulescens Scop.

—

B. verae Kor.

Sterigmostemum sp.

Melanobaris gloriae Kor. and Gültekin

—

B. sugonyaevi Kor.

Isatis sp.

—

Ceutorhynchus isatidis Col.

B. kasparyani Kor.

Lepidium vesicarium

—

—

B. hesperidis Khnz.

Hesperis bicuspidata

Melanobaris sp.

Ceutorhynchus inaffectatus Gyll.

B. medvedevi Kor.

Matthiola sp., Matthiola bucharica

—

—

B. concolor Fåhrs.

?Camelina sp.

—

—

B. fortirostris Kor.

?

—

—

B. albosuturata Rtt.

?Strigosella sp.

—

—

7.6 ­Biodiversity of Insect Herbivores Among the herbivores, the greatest species richness is achieved by insects with rhizopha­ gous, soil‐inhabiting larvae. These groups include the weevil subfamily Entiminae (Fig.  7.3f ) with about 14,000 known species (3500 in the Palearctic), the tribe Alticini of the Chrysomelidae with about 11,000 species worldwide (ca. 3000 species in the Palearctic), and the noctuid moths with 27,000 species (5500 in the Palearctic). Of the Entiminae, the largest genus is the Palearctic Otiorhynchus s. l., with about 1000 species; all are wingless and many have restricted ranges in the mountains of southern Europe, Anatolia, and Middle and Central Asia1. The high number of species 1  Middle Asia is a climatic region distinct from Central Asia (Jashenko and Zyuzin 2000, Korotyaev et al. 2005, Medvedev 2005). It includes the Asian republics of the former USSR and neighboring parts of Afghanistan and Iran. The region is characterized by warm winters and maximum rainfall in spring and autumn. Central Asia is a climatic region that includes Mongolia and a large area of north-central and northwestern China. It is characterized

­ robably relates little to trophic specializations p because many species are apparently polypha­ gous, which is probably true for the entire sub­ family Entiminae. Winglessness likely facilitates geographic iso­ lation. Otiorhynchus includes a great number of parthenogenetic forms that are genetically iso­ lated, with their own ranges and ecological associations. Many other, mostly wingless, gen­ era of the Entiminae include parthenogenetic forms. The vast territory of the Russian Plain with its short post‐glaciation history has faunas of the genera Otiorhynchus (18 species) and Trachyphloeus (nine species) that consist exclu­ sively of parthenogenetic forms whose known bisexual ancestors, when present, have narrow ranges in the neighboring or rather distant mountain systems. Most of the parthenogenetic forms occur in the temperate and boreal forests and the steppes, whereas no endemic partheno­ genetic forms are known from the tundra, and only a few live in the desert zone (Korotyaev by an extreme continental climate with harsh winters and maximum rainfall in late summer. The term Middle Asia is used in the Russian literature, but in the English-language literature Middle Asia is incorporated into Central Asia.

7  Insect Biodiversity in the Palearctic Region

1992a). The relict bisexual forms often are local­ ized in the mountains, whereas their partheno­ genetic derivatives are in the plains. The wingless species of Otiorhynchus contra­ dict speculation that a limited number of spe­ cies can be produced within a single genus, presuming that only a certain number of combi­ nations of morphological characters co‐occur to give rise to viable forms, whereas many other combinations, being maladaptive, are selected against. This idea might apply to planktonic forms (Zarenkov 1976) but not to terrestrial beetles. Otiorhynchus in the broad sense has a great number of species that differ only in the proportions of their antennal funicle, sexually dimorphic characters, vestiture, and coloration. Considering that every new taxon potentially could produce a further set of descendants with innumerable combinations of old and new char­ acters, one can hardly imagine reasonable limits for the diversity of species that could evolve in Otiorhynchus and other apterous beetles. Parthenogenesis increases this diversity, but here a limitation does exist: parthenogenetic forms of weevils do not have more than six hap­ loid chromosome sets, and hexaploids are the terminal products of parthenogenesis. The diversity of a taxon of specialized herbi­ vores is often proportional to the number of species in the host‐plant taxon (although this statement is more hypothetical than verified). Even so, many species of the higher host taxon have no insect community of their own, and a single or a few host species can harbor many herbivores. This situation applies to Ephedra in Mongolia; 10 species of the weevil tribe Oxyonychini (Fig. 7.5d) (Korotyaev 1982; B.A.K., unpublished data) live on Ephedra sinica Stapf and Ephedra przewalskii Stapf, whereas no species of Oxyonychini are associated with six (Grubov 1982) other Mongolian species of Ephedra. Similarly, 14 species of Oxyonychini are associated with Ephedra major Host (= E. procera Fisch. and Mey.) in the Western Palearctic (Colonnelli 2004), which is probably the host plant with one of the greatest numbers of weevils specialized on a single species in the

Palearctic Region. Often, only a few, or no, her­ bivores can be found in areas with a wide variety of potential hosts, whereas relatively depauper­ ate habitats or countries can harbor greater insect biodiversity. For example, in Ul’yanovsk Province in the middle Volga area of Russia, nine species of the weevil genus Tychius are found on nine species of Astragalus (Fabaceae) (Isaev 2001), whereas in Mongolia, which has 68 species of Astragalus (Sanchir 1982), only four or five species of Tychius are associated with this host genus. Some plant families with subordinate p ­ ositions in the flora and vegetation in the southern Palearctic harbor specific and occasionally spe­ cies‐rich communities of weevils and leaf bee­ tles. This is particularly true for small herbaceous lianas of the families Cucurbitaceae, Cuscutaceae, and especially Convolvulaceae. For example, the phytophagous community of field bindweed (Convolvulus arvensis L.) includes the Turanian weevil Alcidodes karelinii (Boheman) of the large Paleotropical genus of Curculionidae, Necatapion bruleriei (Desbrochers) of the monotypical Eastern Mediterranean genus of Apionidae (Friedman and Freidberg 2007), Galeruca rufa Germar of the specialized south­ ern Palearctic subgenus Emarhopa, at least four of the five species of the Western Palearctic genus Hypocassida with Afrotropical affinities (Borowiec 2000), and several species of the flea‐ beetle genus Longitarsus and seed beetles (Bruchinae) from the Palearctic and Paleotropical genus Spermophagus, which has 90 species (Borowiec 1991). These species‐rich communi­ ties are the northern outposts of the Paleotropical biota in the Palearctic fauna. The number of specialized and occasional arthropods on a particular plant species can be quite high. For example, 175 species are reported on Lepidium draba L. (Brassicaceae), with the majority being insects (Cripps et al. 2006). For the entire superfamily Curculionoidea, excluding scolytines, the plant species to beetle species ratio is 6 : 1 in the Caucasus and Mongolia. In the northern taiga and tundra zones of Magadan Province and Chukchi

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Autonomous District, this ratio is about 12 : 1 (13  :  1 in the impoverished biota of the Kamchatka Peninsula and the Koryak Plateau north of it), and about 30 : 1 on far‐northern Wrangel Island (B.A.K., unpublished data). In local steppe areas, the ratio is about 2.5 : 1 (Korotyaev 2000; B.A.K., unpublished data). The diversity of beetle herbivores is unevenly distributed among higher plant taxa. Grasses and sedges that dominate the vegetation over vast territories in the Palearctic usually possess depauperate insect communities, consisting mostly of planthoppers (Auchenorrhyncha), although the genus Carex has the greatest num­ ber of insect herbivores among herbaceous plants (75; Emeljanov 1967). Most Palearctic insects with chewing mouthparts, such as wee­ vils and leaf beetles, avoid monocots. Among the Palearctic Chrysomelidae, a few genera of flea beetles (e.g., Chaetocnema and Psylliodes) include a relatively large number of species that feed on monocots. Most other chrysomelids associated with monocots in the Palearctic belong to a few primitive subfamilies, such as the predominantly temperate, aquatic Donaciinae with 62 species in the former USSR (Lopatin et al. 2004). A few Palearctic species of the large, mostly tropical tribe Hispini are asso­ ciated with grasses. In Belarus, 64 of 351 spe­ cies of leaf beetles feed on Poaceae and Cyperaceae (Lopatin and Nesterova 2005). Two small genera of stem‐mining cerambycids (Theophilea and Calamobius) and the two larg­ est Palearctic genera with rhizophagous larvae (Dorcadion and Eodorcadion) are associated with Poaceae (Plavilshchikov 1958, Miroshnikov 1980, Cherepanov 1996). Among weevils, most of the monocot feeders belong to family‐ and genus‐group taxa with predominantly extra­ tropical distributions (family Erirhinidae; sub­ family Bagoinae, tribe Mononychini, and genera Prisistus and Oprohinus of the Ceutorhynchinae; and genus Limnobaris of the Baridinae, Curculionidae) and tropical distri­ butions (families Brachyceridae and Dryophthoridae; Apsis albolineatus (F.) of the Curculionidae: Myorhinini). Buprestids of the

small but m ­ orphologically specialized genera Cylindromorphus and Paracylindromorphus are associated with grasses, sedges, and reeds (Phragmites australis (Cav.) Trin. ex Steudel). Several species of Aphanisticus develop on Juncus (Juncaceae), and larvae of the special­ ized buprestid genus Cyphosoma (Fig. 7.2g) develop in tubers of Bolboschoenus (Ascherson) Palla (Cyperaceae). Orthopterans  –  “hexapod horses”  –  are the only insects with chewing mouthparts that are abundant on grasses, although not all of them feed on monocots. Most Palearctic phytophagous insects are associated with seed plants (Spermatopsida). Conifers (Pinophyta) host less diverse insect com­ munities than do angiosperms (­Mag­noliophyta). For example, of 351 species of leaf  beetles (Chrysomelidae) in Belarus, only four  feed on conifers: the monophagous Cryptocephalus pini L. (Cryptocephalinae), oligophagous Calomicrus pinicola Duftschmidt, and polyphagous Cryptocephalus quadripustulatus Gyllenhal and Luperus longicornis F.  (Lopatin and Nesterova 2005). Even at the border of northern taiga in Northeast Asia, only eight of 130 species of Curculionoidea (excluding Scolytinae) are asso­ ciated with conifers. Yet, a vast number of wood borers are associated with conifers, primarily beetles of the Anobiidae (including Ptininae), Bostrichidae, Buprestidae, Cerambycidae, and the subfamily Scolytinae of the Curculionidae, all of which, even in northern taiga, regularly cause damage to forests and plantations. Lepidoptera developing on foliage also include serious forest pests, and a few sawflies (Hymenoptera) attack both strobiles and wood. In total, 202 species of strictly oligophagous insects are associated with five genera of coni­ fers in the former USSR (Emeljanov 1967): Pinus (82 species), Picea (50), Larix (25), Juniperus (23), and Abies (22). Ephedra (Ephedraceae) is unique in having an entire fauna of the endemic weevil tribe Oxyonychini, with 20 genera and about 60 species (Colonnelli 2004). Most xylo­ phagous buprestids and longhorn beetles that develop on Ephedra also are specific to this genus. Some planthoppers and apparently less

7  Insect Biodiversity in the Palearctic Region

mobile Sternorrhyncha also are specialized on this plant, as indicated by the occurrence of small predatory coccinellids of the genus Pharoscymnus in southern Mongolia only on Ephedra (Konstantinov et  al. 2009); Pharoscymnus auricomus Savoiskaya is associ­ ated mainly with these plants in sand deserts of Middle Asia (Savoiskaya 1984), and an unidenti­ fied Pharoscymnus sp. was found on Ephedra in the Judea Desert in Israel (B.A.K., unpublished data). Leaf beetles and weevils do not com­ monly feed on both conifers and angiosperms, but some large and widely distributed weevil genera (e.g., Anthonomus, Hylobius, and Cossonus) include species that develop on either conifers or angiosperms. Ferns and mosses have relatively small numbers of phytophagous insects in the Palearctic. Among leaf beetles, fern feeding is known only in the Himalayas, where many species of the genus Manobia (Alticini) use various ferns. Among the Buprestidae, larvae of the mainly Oriental genus Endelus (Agrilinae) feed on ferns. Some European Otiorhynchus weevils also feed on ferns. Mosses are less populated by flea beetles in the northern Palearctic than in the south. The only known moss‐living flea beetle genus in the temperate Palearctic is the oligotypic Mniophila muscorum Koch (Fig. 7.4c). In the Himalayas, the mountains of Yunnan, and farther south in Asia, most of the moss‐living flea beetles belong to the same genera as the leaf‐litter flea  beetles (e.g., Benedictus, Clavicornaltica (Fig.  7.4b), Paraminota, and Paraminotella) (Konstantinov and Duckett 2005), except for Ivalia and Phaelota, which live in mosses in southern India, but are not found in leaf litter or mosses in the Palearctic (Duckett et  al. 2006, Konstantinov and Chamorro‐Lacayo 2006). In the New World, the only moss‐living flea bee­ tles belong to the genus Kiskeya (Fig. 7.4d) (Konstantinov and Chamorro‐Lacayo 2006). All moss‐feeding flea beetles share a similar habitus. They are among the smallest flea beetles and have round bodies, relatively robust appendages, and somewhat clavate antennae. The Holarctic flea‐beetle genus Hippuriphila is unique in its host choice: all four species feed

on Equisetum (Equisetopsida) (Konstantinov and Vandenberg 1996). No other leaf beetle in the Palearctic feeds on plants of this taxon, but a few species of Bagous (Curculionidae) and all  four species of the Holarctic genus Grypus  (Erirhinidae) also are associated with Equisetum. It is unknown why some plant groups have diverse phytophagous assemblages whereas oth­ ers do not. The Palearctic weevil fauna, for instance, has a small number of species that develop on grasses (Poaceae) and sedges (Cyperaceae) in the steppe and desert landscapes, where many plants of these families are domi­ nant. Some plant taxa that are diverse have a low diversity of insect consumers. Two plant genera (Allium and Artemisia) have similar representa­ tion in the Mongolian vegetation but differ sharply in the diversity of their weevil communi­ ties. Thirty species of Allium are found in Mongolia. Many of them dominate plant com­ munities and are major sources of food for graz­ ing animals, but only a single weevil of the specialized ceutorhynchine genus Oprohinus is associated with them. The wormwood genus Artemisia has 65 species in Mongolia (Leonova 1982) and dominates many types of plant com­ munities. These plants have diverse phytopha­ gous assemblages of more than 100 species of Auchenorrhyncha and Coleoptera (Buprestidae, Chrysomelidae, and Curculionidae). Some plants have species‐rich phytophagous communities, such as oaks (Quercus) among trees, Artemisia among herbs and semishrubs, and sedges (Carex) among herbs (Emeljanov 1967). Many highly specialized herbivores are associated with plants that have a high level of chemical and mechanical defenses, such as Aphthona (Chrysomelidae) (Fig. 7.4a), Perotis cuprata (Klug) (Buprestidae), and Oberea erythrocephala (Schrank) (Cerambycidae) on Euphorbia; Aphthona nonstriata Goeze and Mononychus punctumalbum (Herbst) (Curculionidae) on Iris pseudacorus L.; Nastus and Lixus spp. (Curculionidae) on Heracleum; and a few Buprestidae, Lema decempunctata (Gebler), several Alticini in the genera Psylliodes and Epitrix, two species in two genera

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of Cassidini (Chrysomelidae), Neoplatygaster venustus (Faust), and Augustinus koreanus Korotyaev and Hong (Curculionidae) on various Solanaceae. Some chrysomelids and weevils spe­ cialize almost exclusively on plants that contain toxic secondary compounds, combining unre­ lated taxa in their host ranges. For example, Psylliodes species feed on Brassicaceae, Cannabaceae, Cardueae of the Asteraceae, Poaceae, and Solanaceae. Of the four Far Eastern Russian Lema species (Chrysomelidae), two develop on monocots, one on Solanaceae, and one on Cardueae (Medvedev 1992). An analysis of host specialization of 321 species of flea bee­ tles (Chrysomelidae) in the European part of the former USSR and the Caucasus shows that plant families most frequently used as hosts for flea beetles are among the most speciose in the flora. The most species‐rich families of plants on the Russian Plain are the Asteraceae, Poaceae, Rosaceae, Fabaceae, Cyperaceae, Lamiaceae, Scrophulariaceae, and Brassicaceae (Alexeev and Gubanov 1980). The plant families most often used by flea beetles are the Brassicaceae, Lamiaceae, Asteraceae, Boraginaceae, Scrophu­ lariaceae, Euphorbiaceae, and Poaceae; for the buprestid tribe Acmaeoderini, they are the Fabaceae, Fagaceae, Anacardiaceae, Apiaceae, Rosaceae, Asteraceae, and Moraceae (Volkovitsh and Lobanov 1997); and for the weevil subfamily Ceutorhynchinae (in the entire Palearctic), most hosts are in the Brassicaceae, Ephedraceae, Lamiaceae, Boraginaceae, Asteraceae, Fagaceae, and Liliaceae. Among plant families, the Brassicaceae are common and numerous in the Palearctic and Nearctic, but their weevil communities in the two regions are quite different. Nearly half of the Palearctic fauna of the weevil subfamily Baridinae  –  about 60 species in six endemic genera  –  is associated with crucifers, whereas crucifer‐eating Baridinae are not known in the Nearctic. Another weevil subfamily, the Ceutorhynchinae, is much less species rich in the Nearctic than in the Palearctic, with about 80 species of a single genus Ceutorhynchus, as opposed to more than 300 species of

Ceutorhynchus and six species of three other small genera in the Palearctic. This subfamily includes members of at least 11 Holarctic spe­ cies groups. The Brassicaceae are unique in hav­ ing at least 450 species of specialized beetles in the Palearctic (Cerambycidae, Chrysomelidae, Urodontidae, and Curculionidae with its sub­ families Baridinae, Ceutorhynchinae, and Lixinae) that feed on its many species. About 60 species of flea beetles feed on the Brassicaceae in France (Doguet 1994). The plant family Asteraceae has a diverse community of phytophagous beetles. About 65 species of flea beetles, for example, feed on vari­ ous asteraceans in France (Doguet 1994), and 67 species of leaf beetles feed on the Asteraceae in Belarus (Lopatin and Nesterova 2005). Asteraceae‐feeding Baridinae are present in both the Palearctic and Nearctic, but they belong to different genera or even tribes, as do the Baridinae living on hygrophilous monocots. Insect communities on oaks probably are richest in the Palearctic (Emeljanov 1967). Some weevil genera (e.g., Curculio) on oaks are equally represented in the Nearctic, but some, such as several genera of the tribe Rhamphini (Curculioninae) and genus Coeliodes (Ceutorhynchinae), are lacking in the Nearctic. Some insects demonstrate major differences in their host choice in the Palearctic and other biogeographical regions. Flea beetles in the Palearctic, for example, feed mostly on herbs and grasses, with just a few species on woody plants. Flea beetles in the Oriental Region feed mostly on bushes and trees. Thus, in the Palearctic, they occur mostly in open spaces such as meadows and swamps, whereas in the Oriental Region, they are species rich in forest communities.

7.7 ­Boundaries and Insect Biodiversity The boundaries between faunal complexes of any rank (e.g., biogeographical realms or assem­ blages of insects in two adjacent localities) and

7  Insect Biodiversity in the Palearctic Region

the distributional limits for particular species typically cross physical gradients. Although the literature on this matter is voluminous (Darlington 1963), we add several new Palearctic examples. The boundary between the western and east­ ern parts of the Palearctic for most groups of plants and animals is situated between the Altai Mountains and Lake Baikal; for some taxa, it coincides approximately with the Yenisei River. Two typical Arctic Chrysolina species (Chrysomelidae), Chrysolina cavigera Sahlberg and Chrysolina subsulcata Mannerheim, have not been found west of the Yenisei River (Chernov et  al. 1994). At the source of the Yenisei, at Kyzyl City in Tuva, where the width of the river barely exceeds 100 m, the fauna dif­ fers considerably between the left (western) bank and the right (eastern; in Tuva, northern) bank. Chrysolina jakovlevi Weise occurs mostly north of Tuva in southern Krasnoyarsk Territory and Khakasia. In Tuva, it inhabits only stony slopes in a narrow strip of desert steppe on the right bank of the Yenisei (Medvedev and Korotyaev 1976). Chrysolina tuvensis Medvedev is known only from the desert steppe on the right bank near Kyzyl, and Chrysolina sajanica Jacobson occurs in the dry steppe on the southernmost West Sayans pied­ mont. The wingless Chrysolina urjanchaica Jacobson, an endemic of the right‐bank steppe and the interfluvial area of the Ka‐Khem and Bii‐Khem rivers (Korotyaev 2001b), is substi­ tuted on the left bank by a similar and closely related species, Chrysolina convexicollis Jacobson, distributed throughout the rest of Tuva and in adjacent northwestern Mongolia. A wingless weevil, Eremochorus zaslavskii Korotyaev, endemic to the right bank, substi­ tutes there for the widely distributed Eremochorus sinuatocollis (Faust). These exam­ ples demonstrate the isolating role that a rela­ tively narrow river can have. Rivers and their valleys also have a role as distribution path­ ways. Land insects tend to penetrate farther north or south along valleys of major rivers in the Palearctic.

Another boundary exists along the Ural Mountains and lower course of the Volga River. Isaev (1994) found several species of beetles with eastern distributions reaching the right bank of the Volga in Ul’yanovsk Province, including a steppe weevil, Ceutorhynchus potanini Korotyaev, that is distributed in Siberia from the West Sayan Mountains to central Yakutia, as well as in Mongolia. Ceutorhynchus tesquorum Korotyaev, which is distributed across Tuva and eastern Mongolia and co‐ occurs with C. potanini in Tuva on Alyssum obovatum C. A. Mey. (Turcz.) (B.A.K., unpublished data), also was found on this plant in the south­ ern Urals (Orenburg Province), where it is sym­ patric with C. potanini (Dedyukhin 2014). Mountain systems represent obvious borders between faunas. The Carpathians limit distribu­ tion to the east for a number of beetle species, including carabids (Carabus auronitens F. and Carabus variolosus F.) and a chafer (Hoplia praticola Duftschmidt). A number of southeastern European species do not reach farther west than the Carpathians (Arnoldi 1958). Climate might explain why some distribu­ tional limits do not coincide with obvious physi­ cal boundaries. The southern boundaries of the ranges of several Euro‐Siberian weevils, such as Phyllobius thalassinus Gyllenhal, Ceutorhynchus pervicax Weise, Ceutorhynchus cochleariae Gyllenhal, and Trichosirocalus barnevillei (Grenier), run along the southern slope of the West Sayan Range, but these species are not found in the northern foothills of this range. The distribution of these species to the south is apparently not limited by the high mountain ranges, but rather by the aridity. T. barnevillei is present in the Yenisei flood land below and south of the forest margin, which is a typical dis­ tribution for woodland species outside forest massifs. Two common Euro‐Siberian weevils have the southern margins of their ranges on northern slopes of different mountain chains in Tuva. Hemitrichapion reflexum (Gyllenhal) is found only on the southernmost ridge of the West Sayan, the Uyukskii Range, whereas Brachysomus

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echinatus (Bonsdorff ) is found only on the northern slope of the Eastern Tannu‐Ola Range. One is a steppe species, and the other is a forest species. Their distributions in Tuva fit the rule formulated by the well‐known plant geographer O. E. Agakhaniantz (1987): migrants occupy slopes facing the direction of the country from which they came. Yet, the preceding examples of species with the southern boundaries of their ranges running along the southern slope of West Sayan do not follow this rule.

7.8 ­Local Biodiversity High local insect biodiversity is illustrated by five closely related endemic species of the wee­ vil genus Ptochus in a small area of Daghestan (Ismailova 2006). Three species are located along the river, about 30 km apart, their ranges separated by Andiiskoe Koisu River tributaries, and two are on opposite sides of the mountains facing the river. All species are flightless, similar externally, and feed on the same species of Artemisia. In addition to these five, an endemic, Ptochus daghestanicus Formánek, is distributed along the western Caspian Sea coast, and the Ponto‐Caspian Ptochus porcellus Boheman is widespread in the plains and mountainous parts of the republic. A similar pattern of local biodi­ versity is known for some Middle Asian Prosodes (Tenebrionidae). The high level of biodiversity often is maintained by reproductive isolation associated with complicated structure of the genitalia (Medvedev 1990). Local biodiversity of some insect groups is increased by separation of periods of insect activity, either daily or seasonally. A well‐known example is the scarabaeid genus Chioneosoma in southern Kazakhstan. Six sympatric species, in addition to having different habitat associations, have sequential flight periods, with most adults flying in different plant layers. Of the two species that co‐occur in the Muyunkum Sands and exhibit no clear differences in flight habits, one flies before sunset and the other half an hour after the flight of the first species ceases

(Nikolajev 1988). These differences enhance reproductive isolation of species with similar larval habits. Seasonal differentiation of phy­ tophagous insect assemblages follows changes in vegetational aspects: ephemeral plants possess specific insect communities often formed by particular insect taxa, occasionally using a spe­ cific habit such as gall inducement (Kaplin 1981). Non‐specialized feeders also can exhibit high species biodiversity, such as predatory carabids, coprophagous scarabs, and detritophagous ten­ ebrionids, of which many include genera with more than 500 species (e.g., Carabus, Fig. 7.5a). Local biodiversity of parasitoids can be higher than that of herbivores. For example, about 80 species of ichneumonids were collected on one daily excursion in the Kamchatka Peninsula (D.  R. Kasparyan, personal communication), whereas the entire weevil fauna of the peninsula comprises about 50 species (Korotyaev 1976). Yet, in more southern regions, phytophagous insects are locally rich. On the plains of the Northwestern Caucasus, for example, one excur­ sion on 19 May 1979 yielded 39 species of the weevil subfamily Ceutorhynchinae. The super­ family Curculionoidea is represented by 551 species in Berlin (Winkelmann 1991). Wanat (1999) reported 480 species of Curculionoidea (excluding Platypodidae and Scolytinae) in the Białowieża Primeval Forest of eastern Poland, probably the largest broadleaf forest in Europe. The advantage of a specialized phytophagous habit over a detritophagous one is seen by com­ paring the faunas of Tenebrionidae and Curculionidae in the Taman’ Peninsula in Krasnodar Territory. The former family is repre­ sented on the small peninsula by 36 species (Abdurakhmanov and Nabozhenko 2011) and the latter by 321 species (B.A.K., unpublished data). The Tenebrionidae show a wide variety of adaptive zones that are exploited by suprage­ neric taxa (tribes and subtribes), although none is occupied by more than three species (e.g., by the genera Pedinus and Nalassus, which are  characteristic of the Western Scythian steppes) (Fig. 7.6). In the Curculionidae, even the least‐­specialized broadnosed weevils with

7  Insect Biodiversity in the Palearctic Region

(b)

(a)

(d) (e) (i)

(c) (k)

(f) (j)

(g)

(h)

(n)

(m) (p) (l)

(s)

(q)

(o)

(t) (r)

(u)

(v)

(w)

(x)

(y)

(z)

Figure 7.6  Examples of Tenebrionidae from the Taman’ Peninsula (photos K. V. Makarov). (a) Tentyria nomas (Pallas). (b) Stenosis punctiventris (Eschscholtz). (c) Asida lutosa Solier. (d) Pimelia subglobosa subglobosa (Pallas). (e) Blaps halophila Fischer von Waldheim. (f ) Oodescelis polita (Sturm). (g) Dendarus punctatus (Audinet‐Serville). (h) Pedinus femoralis femoralis (L.). (i) Leichenum pictum (Fabricius). (j) Melanimon tibialis tibialis (Fabricius). (k) Ammobius rufus (Lucas). (l) Gonocephalum granulatum pusillum (Fabricius). (m) Opatrum sabulosum sabulosum (L.). (n) Crypticus quisquilius quisquilius (L.). (o) Alphitophagus bifasciatus (Say). (p) Diaclina testudinea (Piller and Mitterpacher). (q) Phaleria pontica Semenov. (r) Phtora reitteri (Seidlitz). (s) Scaphidema metallicum (Fabricius). (t) Trachyscelis aphodioides Latreille. (u) Alphitobius diaperinus (Panzer). (v) Tenebrio obscurus Fabricius. (w) Centorus tibialis Zoufal. (x) Cossyphus tauricus Steven. (y) Laena starcki Reitter. (z) Nalassus faldermanni (Faldermann).

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root‐­feeding larvae are represented by much greater numbers of species (Otiorhynchus by 16), whereas oligo‐ and monophagous crucifer feeders of the subfamilies Lixinae, Baridinae, and Ceutorhynchinae comprise three, seven, and 36 species, respectively.

7.9 ­Insect Biodiversity and Habitats Plant communities in the Palearctic are classi­ fied as zonal, azonal, or extrazonal (Chernov 1975, Walter and Breckle 1985). Zonal commu­ nities are situated on “the flat elevated areas with deep soil which are neither too porous to water, like sand, nor retain too much water, like clay … There must be no influence from ground water” (Walter and Breckle 1985). The particu­ lar regional climate has its full effect on such areas, called euclimatopes or plakor in Russian. Azonal vegetation appears when the groundwa­ ter table is so high that the whole area is covered with bogs or when vegetation is on sand or allu­ vial soil. Extrazonal vegetation is zonal vegeta­ tion outside its climatic area: for example, steppe meadows in forest zones. The distribution of insects among these types of communities has some regularity. Zonal insect faunas are not particularly rich in the northern Palearctic, but increase in richness southward (Chernov 1966). They usually are formed of species whose ranges are associated with a particular zone. Ranges tend to be rela­ tively large in northern zonal communities and small in southern communities. Most southern zones (e.g., steppe) have some endemics (e.g., the chrysomelid Aphthona sarmatica Ogloblin), whereas azonal and intrazonal plant communi­ ties in the north have a larger number of species with wider ranges. Insects with larger ranges tend to occur in non‐specific habitats, either intra‐ or extra­ zonal. In Mongolia, for example, leaf beetles with transpalearctic ranges commonly occur in ruderal and agricultural habitats, whereas spe­ cies with smaller, Central Asian ranges occur in deserts or saline habitats specific to Mongolia

(Medvedev 1982), where many widespread spe­ cies also occur in high populations (Korotyaev et  al. 1983). Ranges of many taiga insects also can be large, covering the entire taiga zone. The azonal riparian landscape has a high pro­ portion of insect biodiversity in most of the natural zones, including the tundra (Chernov 1966), taiga (Ivliev et al. 1968), northern part of the Stenopean forests (Egorov et  al. 1996), steppes (Medvedev and Korotyaev 1976), and deserts (Korotyaev et al. 1983), with the propor­ tion of the riparian species in the total fauna increasing northward in the taiga zone. Azonal, mainly riparian, communities also include species that are endemic to certain zones. The weevil genus Dorytomus, for exam­ ple, is one of the largest genera of riparian beetle complexes, with 63 species in the Palearctic. Most of its members occur in floodland habi­ tats. In the oceanic sectors, they are distributed across several zones, so that in the Russian Far East, the fauna of the taiga is largely the same as that in the nemoral Stenopean forests. Yet, in the desert and lower mountains of Middle Asia, most Dorytomus species are endemic: for exam­ ple, all four species in southern Tajikistan are endemic to Middle Asia (Nasreddinov 1975). The entire riparian landscape in the desert zone, with its specific type of forests called “tugai,” has characteristic insect complexes that include water beetles and bugs, amphibionts, xylobi­ onts, and herbivorous insects. Leaf‐beetle com­ munities of tugai are highly specific (Lopatin 1977). Most genera endemic to Middle Asia and southern Kazakhstan occur there (e.g., Atomyria, Jaxartiolus, and Parnops). Lopatin (1977) suggested that the tugai leaf‐beetle fauna is closely related to the Mediterranean fauna, differing from it in having a number of northern elements (e.g., Donacia, Gastrophysa, and Phaedon), which dispersed into Middle Asia around the Pleistocene. Many insect communities are hidden in the substrate and are less conspicuous than the large and beautiful butterflies, dragonflies, acridids, and bees, or the irritating horse flies and mosquitoes. They, nonetheless, have diverse

7  Insect Biodiversity in the Palearctic Region

roles, such as preying on injurious and benefi­ cial animals and decomposing dead organisms. Beetles, with their hard bodies, dominate most types of these hidden assemblages except those where rapid larval development in semi‐liquid substrates (e.g., dung and carrion) gives an advantage to flies, although there, too, many beetles hunt fly larvae. Dozens of insect species constitute different kinds of coprobiont, necro­ biont, and dendrobiont (mostly under‐bark) communities. Several large beetle families are specialized for these sorts of habitats. Most Silphidae (carrion beetles) consume large and medium‐sized carrion; Catopinae (Leiodidae) feed on small carcasses; and Trogidae, Necrobia (Cleridae), and Dermestes (Dermestidae) feed on dry vertebrate skin. Succession of the spe­ cies‐rich necrobiont beetle communities is con­ spicuous when several dead bodies of similar size and of a single species are inspected; three species of Dermestes were found on a single hedgehog corpse in Stavropol Territory in April 2013 (B.A.K., unpublished data). Necrobiont communities depend on climate. They are depauperate in the tundra, although the carcasses of many species of birds and mam­ mals provide food. The permafrost makes the environment suitable only for a few small car­ rion beetles (Catopinae) and Thanatophilus. In the Gobi Desert, dry, hot air impedes develop­ ment of fly larvae; the necrobiont communities are dominated by a relatively small number of beetle species. Several beetle families are specialized fungi­ vores, including most of the Ciidae, Erotylidae, Endomychidae, many Tenebrionidae (e.g., Bolitophagus reticulatus L.), the subfamily Dorcatominae of the Ptinidae, and some Nitidulidae (e.g., Cyllodes ater (Herbst) and Pocadius species). Beetle communities of a par­ ticular tree fungus in the southern taiga of the Urals and Western Siberia are composed of doz­ ens of species. For example, 54 species in 16 families occur on Daedaleopsis confragosa (Bolton: Fr.) Schrot (Krasutskii 2007). In the nemoral zone, especially in the Far East, fungal beetle communities are more diverse and

include representatives of exotic Oriental gen­ era. On Kunashir Island, large erotylids of sev­ eral species are visible for 20 m in thin forest, where they sit on the stroma of large tree fungi. Leiodidae are more speciose and abundant in mild, humid oceanic climate, especially in fall; Agathidium laevigatum Erichson is present even on Bering Island (Lafer 1989). Diverse insect communities exist under bark and in forest leaf litter. These communitites are dominated by beetles, but several families of flies also contribute to the overall diversity, as do many parasitic Hymenoptera and several families of bugs, the strongly flattened Aradidae being the most characteristic. Much of these communities consist of scolytines, their preda­ tors and parasites, and consumers of the fungi and debris in their tunnels. One of the largest genera of beetles in these complexes is Epuraea (Nitidulidae), with more than 100 species in the former USSR (Kirejtshuk 1992). Coprophagous assemblages are particularly diverse, depending on season, landscape, and type and age of the excrement. These assem­ blages include many well‐known scarabs, such as Copris, Scarabaeus, and Sisyphus, as well as countless species of the largest beetle genera Aphodius and Onthophagus. Up to 13 species of Aphodius, as well as two species of Onthophagus, can be found in just a few neighboring deposits of dung in Leningrad Province, Russia (the late O. N. Kabakov, personal communication). Some Hydrophilidae also are common in dung. Numerous coprophagous insects are hunted by fly larvae and predatory beetles of the families Histeridae (Fig. 7.4f ) and Staphylinidae. Animal nests also have variably specific insect communities in which many flies, beetles, bugs, fleas, and lice predominate. Zhantiev (1976) provides data on the occurrence of dermestids in insect and mammal nests. Nests and colonies of social insects host species‐rich communities; 200 species of beetles, for example, occur in bumblebee nests. Myrmecophilous insects include many species with characteristic struc­ tural adaptations to life in ant nests, including bare, glabrous, uniformly brown bodies with

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tufts of setae for tactile or chemical communi­ cation with the hosts. The largest genus is prob­ ably Thorictus (Dermestidae), which, because of its aberrant appearance, was long held in a sepa­ rate family. The termitophilous Eremoxenus chan Semenov‐Tian‐Shansky in Middle Asia and the myrmecophilous Amorphocephala coronata Germar of the Mediterranean region are the few Western Palearctic members of a group of commensal Brentidae. Even in urban environments, insects form species‐rich communities. Occasionally, some predatory and saprophagous species irritate humans. In the Academy Archive in St Petersburg is a case from the mid‐1990s that increased activity of larval dermestids (Attagenus smirnovi Zhantiev) caused anxiety among the staff. Inspection of the volumes of the Academy Sessions protocols with M. V. Lomonosov’s signature revealed an invasion by Lasioderma (Ptinidae), the remains of which were then eaten by larvae of the harmless Attagenus smirnovi. During the reconstruction of the Stroganov Palace at Nevski Prospect in St Petersburg in the late 1980s, a dozen beetle spe­ cies were found in the 40 cm thick larch beams in the attic, including dermestids and wood‐ borers. Forty‐two species of dermestids were listed by Zhantiev (1976) as harmful to stored products in the former USSR. Although some introduced species can be harmful, the majority of the most destructive species of dermestids in every natural zone belong to the local fauna (Zhantiev 1976). The urban fauna of phytophagous insects is also rich and increasing; 799 species of insects, for example, are known from the city of Moscow (Russia). This fauna is dominated by exposed and partly hidden phyllophagous forms (328 species), followed by exposed and partly hidden Auchenorrhyncha, Sternorrhyncha, and Heteroptera (143 species), leaf miners (124), gall inducers (122), and wood borers (110, mainly scolytines) (Belov 2007). A specialized insect assemblage, including beetles and flies of three families, occurs along the seashore. The most widely distributed ­beetle

group in this assemblage is the tenebrionid tribe Phaleriini, which lives on sandy beaches. A characteristic feature of these fast, small‐ to medium‐sized beetles is their sand‐colored integument, with dorsomedial infuscation. Small hydrophilids of the genus Cercyon and various Staphylinidae and Histeridae occur under decaying algae. On the Pacific shore, sev­ eral similar species of the endemic genus Lyrosoma (Silphidae) are abundant at the shore­ line, especially on the Kurile and Komandorski islands. A member of the weevil subfamily Molytinae, Sthereus ptinoides (Germar), with a boreal amphipacific distribution, lives on drift­ wood. In southern Japan, the peculiar weevil genus Otibazo is confined to seashores. The plant genus Cakile (Brassicaceae), which occu­ pies the outermost sandy strip of beach where the salt spray reaches, has a complex of two weevil species in the northern Atlantic basin: Ceutorhynchus cakilis Hansen in Europe and Ceutorhynchus hamiltoni Dietz in North America. These two weevils belong to different species groups, illustrating a tendency of the Ceutorhynchinae to exploit marginal habitats with pioneer‐plant communities. In Europe, several non‐specialized crucifer feeders of the Curculionidae occur on Cakile maritima Scopoli and Cakile euxina Pobed. A tribe of supralittoral weevils, the Aphelini, is distributed along the Pacific Coast from northern California to the temperate Far East, as well as in Australia. In Japan and the southernmost portion of the Russian Far East, Isonycholips gotoi Chûjo and Voss (Aphelini) lives among grasses on dry coastal sand dunes. An additional coastal insect assemblage exists here, including large weevils of the tribe Tanymecini and Craspedonotus tibialis Schaum of the fossorial ground‐beetle tribe Broscini. In the Atlantic sector, the genus Onycholips (two species in northwestern Africa), the fossorial broad‐nosed weevil Philopedon plagiatus (Schaller), and several species of the tribe Brachyderini live on sand dunes along the Baltic coast. P. plagiatus is par­ thenogenetic and was apparently introduced to inland seashores. Carabids of the genera Broscus

7  Insect Biodiversity in the Palearctic Region

and Scarites and tiger beetles (Cicindela) are common on sandy beaches. Coastal rocks in the northern Pacific have a highly specific beetle, Aegialites stejnegeri Linell, of the monotypic subfamily Aegialitinae (Salpingidae), which lives in cracks and seabird nests (Nikitsky 1992).

7.10 ­Insect Biodiversity and the Mountains The Palearctic has a number of mountain sys­ tems, including the Alps, Carpathians, Caucasus, Pamirs, Tien Shan, Urals (dividing the continents of Europe and Asia), Altai, Sayan, Tibet, and northern Himalaya. The majority of Palearctic mountains belonging to the Alp– Himalayan belt are relatively young, except the Urals. The mountain systems are situated in dif­ ferent parts of the Palearctic, with different cli­ matic and other geographic conditions. Their patterns of insect biodiversity, however, share a number of features. Insect biodiversity in the Palearctic moun­ tains changes with climate along altitudinal gra­ dients (Walter and Breckle 1985). Generally, from the piedmont to the mountain tops, the following altitudinal belts are recognized: col­ line‐montane (lower and upper), alpine (lower and upper), and nival (Walter and Breckle 1985). Although these altitudinal belts do not corre­ spond precisely to the zones from south to north, insect biodiversity usually decreases from the bottom to the top of the mountains, as it does from south to north in the Palearctic. The level of endemism, however, increases from bottom to top. An important reason for high biodiversity of mountain‐insect faunas is that many groups in the plains find refugia in corre­ sponding mountain belts when climatic condi­ tions change and zones fluctuate. For example, many species widely distributed in the Arctic and Boreal regions occur in the upper mountain belts in southern Europe; this kind of distribu­ tion is called “arcto‐alpine” or “boreo‐montane,” depending on the specific features of the range. During the glacial age, these insects moved

southward with the glaciers, and found refugia in the high mountains when the climate became warmer and the ice shield retreated. Many mes­ ophilous groups find appropriate environments in mountains during aridization in adjacent plains, accounting for the considerable number of so‐called paleoendemics usually represented by one or a few species in remote mountain sys­ tems. Examples include carabid beetles of the genus Broscosoma scattered along the entire Alp–Himalayan mountain belt (Kryzhanovsky 2002), and the monotypical cerambycid genus Morimonella recently described from the Caucasus. The capacity of the mountain systems to accumulate great numbers of endemic species is facilitated by the broad diversity of habitats as well as the distributional barriers. Wingless spe­ cies are among the most speciose mountain taxa; they are usually classified as neoendemics. For example, the Caucasian fauna of the largest weevil genus, Otiorhynchus s. l., is provisionally estimated at 250 species (Savitskii and Davidian 2007); 50 small, blind, wingless, forest‐litter and, partly, endogean species of the carabid tribe Trechini are recorded from the Caucasus, mostly from its western part (Belousov 1998). Conversely, southerly oriented mountain chains allow the possibility of deep penetration of some typically Palearctic insect groups into the Oriental Region, and vice versa. Alpine insect communities of Middle Asia are relatively poor, but highly endemic. For example, of approximately 800 leaf beetles in Middle Asia, 175 occur in the alpine belt, of which 150 are endemics (Lopatin 1996). Among them are Oreomela, with more than 80 species in the alpine regions of the Tien Shan, Himalayas, Altai, and southwestern ridges of China between 2400 and 4300 m, and Xenomela, all 11 species of which are known from the Tien Shan between 1300 and 3000 m (Lopatin and Nesterova 2004). This unusually high level of endemism might be explained by the specific alpine environment and high degree of isolation. Alpine biodiver­ sity further increases because many species

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with larger ranges are represented by special­ ized morphs in the mountains that might not have species status, but differ genetically. However, insect groups that are most abun­ dant and species rich elsewhere are not always species rich in the alpine belt. For example, the most speciose leaf‐beetle groups in the Palearctic are the Galerucinae sensu lato, ­followed by the Chrysomelinae and Crypto­ cephalinae (Fig. 7.4e). In the alpine belt of Middle Asia and northwestern China, the most speciose are the Chrysomelinae fol­ lowed by the Galerucinae, Eumolpinae, and Cryptocephalinae (Lopatin 1996). In Yakutia, thousands of male hover flies (Syrphidae) sometimes swarm on mountain tops, while females feed on flowers at the bot­ toms and on the slopes of the mountains. In the late afternoon, with the flow of warm air, females fly to the mountain tops, where copulation occurs. A similar kind of behavior (hilltopping) is known for butterflies and for flies in the fami­ lies Sarcophagidae, Tabanidae, and Tachinidae (Barkalov and Nielsen 2007). The mountain forest belt usually has higher species biodiversity than does the alpine belt. Mid‐altitude forests in the Caucasus and Transcaucasia include a number of endemics, many of which are flightless. Examples include the chrysomelids Psylliodes valida Weise and Aphthona testaceicornis Weise in the forests of the Northwestern Caucasus and Altica breviuscula Weise in the narrow strip of mountain ­forest in Talysh (Azerbaijan). Specialized herbi­ vores (e.g., weevils) are most species rich in the piedmont forest belt in Abkhazia (Caucasus) (Zarkua 1977). The high‐altitude fauna of the Palearctic is also unique, compared with that of the neigh­ boring Oriental Region. Palearctic montane flea‐ beetle communities (in the Caucasus, Crimea, and Middle and Central Asia) consist of species in rich, cosmopolitan genera such as Longitarsus and Psylliodes. In the Oriental Region (Southern Himalayas, Western Ghats), however, species occurring at high altitudes belong to genera with limited ranges, and many are confined to the

Himalayas or do not occur outside the Oriental Region. A characteristic feature of the Palearctic highland fauna is the weevil subfamily ­ Ceutorhynchinae at the upper margin of insect distribution. Several species of Ceutorhynchus, Neophytobius, Scleropterus, and others reach the highest altitudes in the upper mountain zone in the Altai, Sayan, Tien Shan, Sredinnyi Kamchatka Range, Tibet, and Himalayas. Another characteristic feature of the Palearctic alpine fauna of weevils is the concentration of bisexual forms of species that reproduce parthe­ nogenetically at lower elevations (Korotyaev 1992a). The alpine belt in the largest part of the conti­ nental sector lacks the multicolored, tallgrass meadows typical of the European mountains or, if they are present, they are poorly developed. Typical of the Sayan Mountains and the ranges to the south and southwest are mountain tun­ dra, shortgrass subalpine meadows with large orange‐yellow flowers of Trollius asiaticus L. (Ranunculaceae), alpine steppe, and an endemic alpine type of vegetation – dense, mesophilous, meadow‐like grasslands dominated by Cobresia spp. (Cyperaceae), from which no specific wee­ vils or leaf beetles are known. Edelweisses (Leontopodium, Asteraceae) are common in the West Sayan and other mountains of Tuva, descending in places to the mid‐forest belt and occurring in pastures. Intense collecting in Tuva on edelweisses by B.A.K. in 1969–72 revealed no herbivores, although Bajtenov (1977) described the weevil Pseudostyphlus leontopodi Bajtenov from Altai. The alpine weevil fauna of this mountain country is poor but characteris­ tic, formed largely of representatives of several genera of Apionidae, Notaris and Tournotaris of the Erirhinidae, Lepyrus, several genera of Hyperinae, Dactylotus globosus (Gebler), a few Sitona species, and the Ceutorhynchinae (Curculionidae). Endemic to this area are many wingless Carabidae, including Carabus, Nebria, and Trechus in the highlands; the montane sub­ genus Aeneobyrrhus of Byrrhus, with five spe­ cies, and one of the three species of the Holarctic

7  Insect Biodiversity in the Palearctic Region

genus Byrrhobolus (Byrrhidae); and several oli­ gotypic genera and considerable numbers of species of Chrysomelidae. The predominantly montane butterfly genus Parnassius (Papilionidae) is represented by several species. The multizonal Aporia crataegi L. (Pieridae) often occurs in great numbers. In the tangle of mountain ridges of West Altai, at the boundary of Kazakhstan and Russia, a heterogeneous but­ terfly fauna with 176 species exists, including several pairs of closely related Eastern and Western Palearctic species, as well as represent­ atives of the Middle Asian fauna (Lukhtanov et al. 2007). Wide variation in altitudinal extension is characteristic of the steppes of Mongolia, adja­ cent Tuva, and the Russian Altai. Steppes occupy plains and the bottoms of variably sized depres­ sions, but also south‐facing mountain slopes in the forest zone and the highest mountain reaches, usually with southern exposure, adja­ cent to and alternating with other subalpine and alpine habitats, such as isolated Larix stands, subalpine meadows, and mountain tundra. Mountain‐tundra steppe, with its characteristic flora, is referred to by botanists as “alpine steppe.” Insects of alpine steppe include a few characteristic species, along with several com­ mon mountain‐steppe insects. Among beetles, this kind of distribution is found in Stephanocleonus (Curculionidae), Crosita, and Chrysolina (Chrysomelidae). Mountain steppe consists of several altitudi­ nal types that are less clearly separated than is the alpine steppe from the rest of the steppes. In the most elevated southwestern part of Tuva, adjacent to the Altai, a few subendemic species of weevils and chrysomelids, mostly of the same genera that constitute the bulk of the alpine steppe fauna, occur only in the highest areas, usually on stony slopes, but not in the alpine steppe. A diverse and characteristic fauna is associ­ ated with mountain areas that have climates intermediate between that of steppe and desert, and vegetation with shrubs (mostly Caragana and Atraphaxis) and perennial wormwoods

(Medvedev 1990). One of the largest weevil gen­ era subendemic to Central Asia, Alatavia with 13 species, is distributed there, with only three species in central and eastern Mongolia occur­ ring in the plains, which in this area are about 1000 m or more above sea level. Many insects in the mountains have com­ mon features that are viewed as adaptations to high‐altitude life. A high percentage of alpine insects are flightless (e.g., more than 80% of chrysomelid beetles in the genus Oreomela). Mountain beetles, such as Psylliodes valida Weise (Chrysomelidae) and Geotrupes inermis Ménétriés (Geotrupidae), have a more swollen prothorax than do their lowland relatives. Many alpine beetles have a high level of mel­ anization of the integument, similar to that in Arctic insects. Their elytra, often covered with ridges, are convex, forming a subelytral cavity that functions as a temperature and humidity buffer for the poorly sclerotized abdominal tergites. Most alpine insects live close to the ground or under rocks and plants, even if their closest relatives occupy other habitats (Lopatin 1971). Numerous alpine leaf beetles are vivipa­ rous or oviviviparous (Oreomela spp.; Lopatin 1996), as are some Arctic leaf beetles. Because of the short warm season, the life cycle of some insects exceeds two years, and overwintering can occur at various life stages (Lopatin 1996).

7.11 ­Temporal Changes in Insect Biodiversity The most obvious recent changes in Palearctic insect diversity may be roughly classified as fol­ lows: (i) reduced diversity in areas densely pop­ ulated by humans, (ii) increased extinction and vulnerability of species, (iii) distributional shifts of species, and (iv) increased numbers of inva­ sive species. Reduction of insect diversity and extinction of species are well‐known phenomena in intensely exploited areas, which have attracted increasing social concern. For example, protec­ tive measures have been proposed by the Red

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Data books not only for densely populated areas such as Krasnodar Territory (Zamotajlov 2007), but also for the least‐populated areas such as the  Chukchi Autonomous District (Chereshnev 2008). Distributional shifts of many insect species in recent decades, often associated with global climate change, have been observed in differ­ ent parts of the Palearctic, from western European countries, where distribution maps have been produced for vast numbers of spe­ cies, especially of butterflies, to the south of the Russian Far East, where a sphinx moth, Acosmeryx naga Moore, with predominantly southern‐temperate to tropical Oriental distri­ bution, has become common (Beljaev 2003). In the Northwestern Caucasus, an area with the highest insect diversity in Russia, and where faunistic surveys have been carried out regu­ larly for nearly 40 years, distributional shifts of several weevil species have been recorded in the past decade (Korotyaev 2013a). The west­ ern Mediterranean weevil Otiorhynchus aurifer Boh., first recorded in Ukraine in 1974, probably crossed the Kerch Straight with transport and was found on 7 June 2009 on Taman’ Peninsula, damaging Fraxinus pennsylvanica Marsh. It might not have become estab­ lished on the peninsula, however, as no beetles were found there in 2012 (B.A.K., unpublished data). The eastern Mediterranean weevil Otiorhynchus ovalipennis Boh., previously known in Krasnodar Territory only from the Black Sea coast, was found more than 100 km inland, damaging Juglans regia L. (walnut) near Krasnodar. Alcidodes karelinii (Boh.), which is common on field bindweed (Convolvulus arvensis L.) in Kazakhstan, Transcaucasia, and Middle Asia, had been recorded in the North Caucasus only in Daghestan until 2003, when it was collected at the eastern boundary of Krasnodar Territory; it is now found regularly in the plains of the Northwestern Caucasus up to its western border at the Sea of Azov. Orchestes mutabilis Boh., which is commonest in the steppe regions of Eastern Siberia and

northeastern Mongolia, was known from a few specimens from the Lower Volga and southern Urals, but has now reached the western limits of Stavropol Territory in the North Caucasus, where it seems to have replaced its European relative, Orchestes alni (L.), on Ulmus pumila L. Last, but not least, the number of overseas invaders in the Palearctic is rapidly increasing (Izhevskii 2008). A phenomenon of particular interest is the establishment of phytophagous insects on alien hosts, often from a different continent. One example is the replacement of an Australian cerambycid, Phoracantha semipunctata (Fabricius), on Eucalyptus spp. in Israel by its Australian congener Phoracantha recurva (Newman) (Friedman et  al. 2008), which required about 70 years. A week before this chapter was written, an East Asian seed beetle, Megabruchidius dorsalis (Fåhrs.), was found in Krasnodar in the pods of Gleditsia triacanthos L. (honey locust), from which previ­ ously only Megabruchidius tonkineus (Pic) had been reared (Korotyaev, 2011b, 2013b, 2015). The host plant is of North American origin, and both seed eaters are of East Asian origin.

7.12 ­Insect Diversity in Major Biogeographical Divisions of the Palearctic Various ideas exist on the subdivisions of the Palearctic, beginning with that of Wallace (1876) (Semenov‐Tian‐Shansky 1936, Lopatin 1989). We follow the subdivisions proposed by Emeljanov (1974), which are based on climatic and other physical conditions most closely reflected by vegetational cover and which largely follow subdivisions proposed by botanists (Lavrenko 1950). Emeljanov (1974) recognized the following regions: Circumpolar, Euro‐ Siberian taiga (boreal), European and Stenopean nemoral, Hesperian (Mediterranean and Macaronesian) and Orthrian evergreen forest (subtropical), Scythian steppe, and Sethian (Saharo‐Gobian) desert.

7  Insect Biodiversity in the Palearctic Region

7.12.1  Arctic (Circumpolar Tundra) Region

The northernmost part of the Palearctic Region is the Arctic (Fig. 7.1aI,b). It includes the coldest areas of the Palearctic, and its southern border corresponds approximately with the 12 °C iso­ therm of the warmest month (July) (Chernov 2002). In European Russia, the southern border runs along the southern border of the tundra and forest‐tundra (Lopatin 1989). Here, we con­ sider the Arctic in the broad sense, including the Hypoarctic (= Subarctic) as its southern subzone. Altogether, about 3300 species of insects live in the Arctic (including the American Arctic), representing 0.6% of total insect diversity. Relative species richness of insects in the Arctic is about 15%, compared with 50% for the world (Chernov 2002). Sixteen insect orders occur in the Arctic. Beetles constitute 13% of the Arctic insect fauna, and flies 60% (about 90% in more northern regions) (Chernov 1995). The most common beetles in the Arctic are the Carabidae, Staphylinidae, and Chrysomelidae. Of the 1800 genera of car­ abid beetles, 22 occur in the Arctic (Chernov et  al. 2000, 2001). The Curculionidae are less common but are represented by a relatively large number of species. Of the remaining large families of Coleoptera, in addition to the entirely aquatic Dytiscidae, the Coccinellidae and Elateridae are most conspicuous in the southern part of the tundra, but they are repre­ sented by only a few species. The biodiversity of phytophagous insects decreases more strongly than that of predatory insects from south to north. For example, even an outdated list of the Carabidae of Magadan Province and Chukchi Autonomous District (Budarin 1985) includes 161 species, whereas an updated list of Apionidae, Curculionidae, and Erirhinidae of the same area has slightly more than 100 names (B.A.K., unpublished data). In the Republic of Adygea in the Northwestern Caucasus, 354 species of Carabidae (Zamotajlov and Makaov 2011) and 434 spe­ cies of Curculionidae (Korotyaev and Arzanov

2011) have been recorded. Predatory beetles constitute about 70% of the total beetle fauna in the Arctic, whereas they make up about 25% in temperate areas (Chernov et al. 1994). A characteristic feature of the Asian Arctic is the wide distribution of the steppe plant com­ munities of several types, including the cold (= cryophytic) steppe and the tundra‐steppe, which are especially developed in Northeast Asia. Many insects occur in these Arctic steppes. Some are endemic and many are dis­ tributed outside the tundra zone in the south­ ern Siberian and Mongolian steppes and in the mountains of eastern Middle Asia (Berman et al. 2002). Insect communities of Wrangel Island, north of the Chukchi Peninsula, described in detail by Khruleva (1987), are dominated by Diptera (76 species), Coleoptera (67), Lepidoptera (54), and Hymenoptera (at least 46). Aquatic insects are well represented by the Ephemeroptera, Plecoptera, and Trichoptera, and the aquatic Diptera are dominated by the Chironomidae (46 species; Makarchenko and Makarchenko 2014) and Tipulidae. Among other groups, relatively large forms with well‐developed flight predomi­ nate. The Lepidoptera include two species of Pieridae (Colias), two of Lycaenidae (two gen­ era), seven of Nymphalidae (all Boloria), five of Satyridae (three Erebia and two Oeneis), two of Geometridae, two of Lymantriidae, 10 of Noctuidae (six genera), seven of Arctiidae (six genera), and one of Pterophoridae. Of the Hymenoptera, the entire superfamily Apoidea is represented by only three species of Bombus (Khruleva 1987; O. A. Khruleva, personal communication). The absence in the Arctic of a few taxa that are abundant and diverse from the southern boundary of the Palearctic to the taiga zone is noteworthy. These taxa include the Orthoptera, beetles of the family Tenebrionidae, ants (represented by a single species in the riparian shrub tundra; Chernov 1966), and predatory Hymenoptera (e.g., Sphecoidea and Vespoidea).

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7.12.2  Forest Regions

Forests occupy most of the Palearctic. They are classified into five regions: the taiga, stretching across Eurasia in the boreal climatic zone; the nemoral European and Stenopean regions in the temperate zone; and the subtropical Hesperian and Orthrian regions. The contiguous regions of the different climatic zones are more similar to each other, in many respects, than to their zonal counterparts. Along the same lines, the affinities of the insect faunas of the Hesperian and Orthrian regions are overshadowed by the similarities they have with their respective neighboring regions. As a result, biogeographic attribution of some large areas often becomes problematic. Anatolia, for example, is classified by Emeljanov (1974) as the zone intermediate between the Mediterranean subregion of the Hesperian region and the Saharo‐Gobian Desert region, but it is considered by Kryzhanovsky (2002) as an area with predomi­ nantly steppe‐type vegetation that is attributed to the boreal biota. The Anatolian insect fauna includes some taxa typical of each of the three regions but lacks others no less characteristic of them. It also has many endemic species and genera. Anatolia apparently has accumulated natural complexes typical of several climatic zones in a much narrower range of altitudes when compared with the Himalayas, where all vegetational types from tropical forests to boreal deserts and nival communities exist. Insect biodiversity in the forests of the Palearctic is great, compared with that of the Arctic, due mostly to a relatively warm, humid climate that allows a variety of plant communi­ ties to thrive. Numerous plant species provide environments for many phytophagous insects, even those not directly associated with woody plants. The number of species of flea beetles, for example, increases from a few in the Arctic to 83 in the taiga, 131 in mixed forests, and 163 in broadleaf forests of the Russian Plain (Konstantinov 1991). Iablokov‐Khnzorian (1961) gives a figure of 580 species of beetles in 35 families feeding on various Pinaceae in the

Palearctic. Most species belong to the Scolytinae (Curculionidae) (177), Cerambycidae (108; Fig. 7.3c), other Curculionidae (76), Buprestidae (59), and Anobiinae (37) of the Ptinidae. A good portion of the species (121) is known from Europe and the Mediterranean (84). Palearctic weevils in the genus Magdalis, with 57 species associated exclusively with woody plants (Barrios 1986), are distributed across all forest zones. Only three (the largest) of the 10 Palearctic subgenera of Magdalis are repre­ sented in the taiga, and none of them is endemic to it, whereas seven subgenera occur only in the temperate and subtropical zones. The northern boundary of the range of Magdalis consists of species of the nominotypical subgenus, which develop on Pinus silvestris L. in Europe and on P. pumila Regel in Northeast Asia, where this characteristic shrub forms the northern forest margin. The southern boundary also includes species of Magdalis s. str., most of which are associated with Pinus species (13 of 16 species with known hosts), whereas one species is asso­ ciated with Abies, Cedrus, and Picea, and two non‐specific feeders develop on Larix. No spe­ cialized Magdalis (or scolytines; M. Yu. Mandelshtam, personal communication) are known from Pinus sibirica Du Tour (Barrios 1986), the most economically valuable Siberian conifer. In the taiga, only Betula, Prunus, and Sorbus are used by Magdalis, whereas Populus, Quercus, Ulmus, and several Rosaceae are hosts of all southern species except those of the nomi­ notypical subgenus. Of the deciduous trees, the Salicaceae have the most diverse beetle fauna in the northern forests (Ivliev et  al. 1968, Korotyaev 1976, Medvedev and Korotyaev 1980), and Quercus has the greatest number of specialized phy­ tophagous insects in the entire Palearctic (Emeljanov 1967). Dorytomus is the most spe­ cies‐rich genus of weevils in the southern Russian Far East (the northernmost part of the Stenopean region). Most weevils, including phyllo‐ and carpophagous and wood‐boring species, differentiate Salix from Populus, and many distinguish Populus tremula L. from other

7  Insect Biodiversity in the Palearctic Region

Populus species, but some polyphagous beetles, such as Saperda populnea (L.), Lamia textor (F.) (Cerambycidae), and Cryptorhynchus lapathi (L.) (Curculionidae), feed on Salix and Populus. Among the willows, narrow‐leaved riparian species (Salix viminalis L., Salix alba L. and similar species in Europe, and Salix udensis Trautv. and C. A. Mey. and Salix schwerinii E. Wolf in the Far East) have the largest communi­ ties of weevils and chrysomelids. The broad‐ leaved Salix caprea L. in Europe has numerous specialized feeders. The family Salicaceae includes a Far‐Eastern monotypical genus (Chosenia), in addition to Populus and Salix. Little is known of the phytophagous community of this tall tree in the south of its range in Japan, Korea, northeastern China, and the Russian Far East. In northeastern Russia (Magadan Province and Kamchatka Territory), two species of Dorytomus (probably developing in catkins) and the leaf‐miner Rhamphus choseniae Korotyaev (all Curculionidae) are monophagous on Chosenia arbutifolia (Pall.) A. Skvorts. All three are distributed southward at least to Primorskii Territory in Russia. No specialized chrysome­ lids or cerambycids are known on Chosenia, although several species from poplars and wil­ lows are recorded as occasional feeders. Another highly diverse phytophagous order, the Lepidoptera, also feeds on the Salicaceae over other trees and shrubs in urban landscapes at the southern border of the taiga in St Petersburg (Lvovsky 1994) (Table 7.5). Temperate and subtropical forest faunas of many insect groups are more diverse in the Far East than in the Western Palearctic, which is separated from the woodland Afrotropical biota by the wide desert zone. Coleoptera are repre­ sented in the Stenopean region by many fami­ lies unknown from the European region, such as the Cupedidae of the Archostemata; the aquatic Aspidytidae recently described (Ribera et  al. 2002) from South Africa and found in China (Shaanxi: Aspidytes wrasei Balke, Ribera and Beutel); and the Helotidae, Inopeplidae, Ischaliidae, Monommidae, Othniidae, Pilipalpidae, Synteliidae, Trictenotomidae, and

Table 7.5  Trees, bushes, and semishrubs most preferred as host plants by Lepidoptera in St Petersburg, Russia (modified from Lvovsky 1994).

Host plant

Number of associated Lepidoptera

Salix

58

Betula

54

Populus tremula L.

48

Populus

37

Alnus

29

Quercus robur L.

22

Vaccinium myrtillus L., Vaccinium uliginosum L.

19

Padus avium Mill.

17

Malus domestica Borkh.

14

Sorbus aucuparia L.

14

Tilia

11

Calluna vulgaris

10

Acer

9

Ulmus

9

Rubus idaeus L.

8

Pinus sylvestris L.

8

Crataegus

7

Lonicera

6

Corylus avellana L.

6

Ribes

6

Rosa

5

Cerasus vulgaris Mill.

5

Frangula alnus Mill.

5

Fraxinus

5

Larix

4

Syringa

3

Cotoneaster

3

Picea

3

Viburnum

1

Euonymus

1

Symphoricarpus

1

Aesculus hippocastanum L.

1

Caragana

1

Sambucus

1

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Zopheridae of the Polyphaga (Lehr 1992). Many subfamilies and tribes of the largest phytopha­ gous families can be added to this list, such as the Megalopodinae and Chlamysini of the Chrysomelidae, and more than 20 tribes of the Curculionoidea. Many large weevil taxa with predominantly tropical (Oriental or Paleotropical) distribu­ tions gradually decrease in representation in the eastern forest faunas through the subtropical Orthrian and temperate nemoral Stenopean regions, and some do not reach the taiga. This trend is demonstrated at the family level by the Anthribidae, Brentidae, and Dryophthoridae and by the Paleotropical tribe Mecysolobini of the Curculionidae, with more than 150 species, including seven in Japan (Morimoto 1962), four in Korea (all shared with Japan and Russia), and two in the south of the Russian Far East. At the generic level, the northern impoverishment of the fauna is exemplified by the second‐largest genus, Mecysmoderes, of the weevil subfamily Ceutorhynchinae, with more than 100 species in East and Southeast Asia, more than 10 in Japan, two in South Korea, and one in the Sakhalin and Kunashir islands. On the contrary, large boreal and temperate genera decrease in species southward and reach tropical countries, if at all, as single representa­ tives in the northernmost mountain systems; examples include Carabus and Chrysolina in Vietnam. The Holarctic weevil genus Dorytomus includes 19 species in boreal Northeast Asia, 28 species in the southern (Stenopean) part of the Russian Far East, 10 species in Japan, and seven in Korea, mostly in the central and south‐­central Stenopean part of the peninsula (Hong et al. 2001). 7.12.3 Taiga

The taiga (Fig. 7.1aII, c) is the largest ecozone in the world, stretching from the Atlantic to the Pacific Ocean. Together with its Nearctic coun­ terpart, it occupies 13% of Earth’s landmass (Schultz 1995). Despite its large size, it is rela­ tively uniform floristically. Sochava (1953)

r­ecognized three main types of taiga in the former USSR: dark coniferous forests domi­ ­ nated by spruces (Picea spp.) and firs (Abies spp.); pine forests with P. silvestris; and larch forests with any of three species of Larix. One of the characteristic features of the taiga is the small number of lianas. Clematis (Ranunculaceae) is the only common represent­ ative; an oligotypic, specialized genus of flea beetles (Argopus) feeds on it. Many insects in the taiga are associated with the most common conifers and occur in abun­ dance, sometimes becoming serious pests. Among the lepidopteran pests are Lymantria monacha (L.) (Lymantriidae), Dendrolimus pini L. (Lasiocampidae), and Dioryctria abietella Denis and Schiffermüller (Pyralidae). Common pests also include scolytine beetles (e.g., Ips, Pityogenes, and Polygraphus). The Scolytinae have a fairly large number of species in the taiga, mostly associated with conifers. In northern Europe, both Picea abies (L.) Karsten and Pinus silvestris have multispecies assemblages of sco­ lytines (up to 15 species on a single tree; M. Yu. Mandelshtam, personal communication), and in Siberia and the Far East, Larix species are heavily attacked, although by few species. Birches, constituting a considerable part of the northern forests, harbor a few species, and alder still fewer. Xylophagous Cerambycidae are not species rich in the taiga but include several spe­ cies that damage conifers and regularly exhibit outbreaks. Coleoptera constitute a considerable part of the taiga insect fauna, and are dominated by the Carabidae, Curculionidae, and Staphylinidae. Ermakov (2003) listed 592 beetle species in 64 families collected in the northern Urals in 1998–2001, from the plains to the highest point at 1492 m. Many taiga insects have enormous ranges stretching across the Palearctic and have a ten­ dency to become invasive if introduced to the Nearctic. For example, the core of the buprestid fauna of the Euro‐Siberian taiga is formed mainly of transpalearctic species, such as Dicerca furcata (Thunberg), Buprestis rustica

7  Insect Biodiversity in the Palearctic Region

(L.), and Anthaxia quadripunctata (L.). Two of the most common buprestids are associated with the coniferous genus Larix: Buprestis strigosa Gebler and Phaenops guttulata (Gebler). Some high‐level forest taxa constituting a considerable part of the nemoral and subtropi­ cal faunas are absent from the taiga, including singing cicadas (Cicadidae), crickets (Grylloidea), and glow worms and fireflies (Lampyridae). Among the weevils, no Brentidae or Platypodidae are present in the taiga. Among the Chrysomeloidea, the Chlamysini, Lampro­ sominae, and Megalopodinae are absent. 7.12.4  Nemoral European and Stenopean Forests

These forests (Fig. 7.1aIII, aIV, d, e; Fig. 7.7c) account for 10% of Earth’s landmass (Schultz 1995). The Palearctic nemoral zone, with origi­ nal vegetation dominated by coniferous‐broad­ leaf (or mixed) and broadleaf forests, consists of two isolated parts, the European and Stenopean regions (Emeljanov 1974). The fragmentation of the nemoral zone followed an increase of continentality that probably occurred in the Pliocene (Sinitsyn 1965), when the northern tundra and taiga zones expanded southward and the steppe and desert zones drifted north­ ward. The occurrence of numerous closely related vicariant species of buprestids, car­ abids, cerambycids, histerids, and other insects in both the European and Stenopean regions supports this hypothesis (Volkovitsh and Alexeev 1988, Kryzhanovsky 2002). For exam­ ple, a number of pairs of closely related vicari­ ant species of Buprestidae are in the European and Stenopean nemoral regions, including Lamprodila rutilans (F.) and Lamp­rodila amurensis (Obenberger), Eurythyrea aurata (Pallas) and Eurythyrea eoa Semenov, and Chrysobothris affinis (F.) and Chrysobothris pulchripes Fairmaire. In European forests, the most species‐rich weevil taxa are associated with the woodland landscape  –  herbage under the canopy

and  especially in the openings, forest litter, and decaying plant matter – rather than with the trees themselves. Representative genera include Acalles and its allies, Dichotrachelus, Otiorhynchus, Plinthus, and several smaller genera of Plinthini; none of them is repre­ sented in the Stenopean region. On the con­ trary, major taxa of the Curculionidae with larval development in the leaves, fruits, or wood of woody plants have poorer representa­ tion in European forests than in Stenopean forests. Examples include the leaf‐mining tribe Rhamphini (seven genera with 51 species in Japan, Morimoto 1984; five genera with 27 species in Europe, Lohse 1983), and the genus Curculio in the broad sense, with 13 species in the south of the Russian Far East and 50 in Japan (Egorov et  al. 1996), and 11 in Central Europe. Of the main forest‐inhabiting higher weevil taxa, only the tribes Anthonomini, Magdalini, and Pissodini are almost equally represented in the European and Stenopean regions. The Eastern and Western Palearctic members of the largest weevil subfamily, Entiminae, with soil‐inhabiting larvae, are represented almost exclusively by endemic genera (and subgenera in a few trans‐ or amphipalearctic genera), except for a small number of widely distributed species. Many other insects associated with trees also are more species rich in the Stenopean region than in the European region. For example, the nitidulid genera Epuraea, which occurs mostly under bark, and Meligethes, which is associ­ ated exclusively with herbaceous woodland plants, are represented in the fauna of the southern Russian Far East by 47 and 20 spe­ cies, respectively, out of approximately 100 in the former USSR (Kirejtshuk 1992). Among ancient faunal elements worthy of mention as endemic to the Stenopean region is the beetle Sikhotealinia zhiltzovae Lafer, origi­ nally (Lafer 1996) placed in the separate mono­ typic family Sikhotealiniidae, but later (Kirejtshuk 2000) transferred to the Mesozoic family Jurodidae (suborder Archostemata), which was thought to be extinct. Other

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(a)

(b)

(c)

(d)

(e)

(f)

Figure 7.7  (a) Russia, Astrakhan Province, near Lake Baskunchak, steppe (photo M. Volkovitsh). (b) Armenia, Vedi desert (photo A. Konstantinov). (c) Russia, Sakhalin Island, mixed forest (photo A. Konstantinov). (d) Italy, Sicily, mountain forest with Fagus (photo M. Volkovitsh). (e) Nepal, Lantang District, mountain forest (3200 m) (photo A. Konstantinov). (f ) Bhutan, Shemgang District (2900 m) (photo A. Konstantinov).

­examples  include Declinia relicta, a species of the  recently described coleopteran family Decliniidae (Nikitsky et  al. 1993); a relict ­longhorn beetle, Callipogon (Eoxenus) relictus

Semenov, with Neotropical affinities; the aquatic beetle Aspidytes wrasei; and representatives of the coleopteran family Synteliidae known only in this part of the Palearctic.

7  Insect Biodiversity in the Palearctic Region

7.12.5  Hesperian and Orthrian Evergreen Forests

These forests (Fig. 7.1aV, aVI; Fig. 7.7d–f ) origi­ nated from a single region of sclerophyllous vegetation that existed at the edge of Arcto‐ Tertiary and Tropical‐Tertiary forests until the end of the Neogene along the Tethys Ocean (Axelrod 1975a). Aridization changed the domi­ nant plant communities from evergreen lauro­ phyllous forests to sclerophyllous forests and chaparral‐macchia. Insect relicts of the lauro­ phyllous forests currently occur in some semi‐ arid areas of the Palearctic, such as the Canary Islands, Himalayas, and southern China. As a result of Pleistocene glaciation, boreal elements are also present in the Hesperian and Orthrian evergreen forests, mostly at high elevations in various mountain systems. The Macaronesian subregion of the Hesperian region includes the islands of Madeira, the Canaries, Azores, and Cape Verde, with typical oceanic climates. The insular insect fauna is less rich than is the continental fauna. It has many endemics and includes Mediterranean and Afrotropical elements. For example, the fauna of the Canary Islands, the largest of the region, contains 230 species of ground beetles, of which 140 are endemics; of 83 genera, 14 are endemic and two are shared with Madeira. The buprestid fauna of the Canaries includes 20 species in nine genera, of which 12 species are endemics. The buprestid fauna of the Canaries is less diverse, compared with the 189 species and 29 genera in Spain and 224 species and 31 genera in Morocco. The Mediterranean insect fauna is species rich and highly endemic. Oosterbroek (1994) suggested that the Mediterranean region in a broad sense (including Anatolia, Armenia, and Hyrcania), together with the Far East, is the most species‐rich area in the Palearctic. The insect fauna of the Mediterranean proper con­ stitutes about 75% of the Western Palearctic fauna (Balletto and Casale 1991). For example, the flea beetle genus Longitarsus, with about 500 species in the world and 221 in the Palearctic, has 158 in the Mediterranean (in the

narrow sense), of which about 10% are e­ ndemics. Of 461 species of Neuropterida in the Mediterranean (in the broad sense), 230 are endemics; of 677 species of butterflies (Lepidoptera), 416 are endemics; and of 498 species of Tipulidae (Diptera), 361 are endemics (Oosterbroek 1994). The most species‐rich areas of the Mediterranean are the Balkans and Asia Minor (Oosterbroek 1994). Widespread temperate European and Palearctic species con­ tribute significantly to the overall biodiversity of the region. The Mediterranean biota, however, has been impoverished by human influences over a long period of time (Mooney 1988). The Orthrian region includes the Himalayas (lower and middle altitudinal belts of the south­ ern slope of the Central and Eastern Himalayas up to 2000–3000 m, belonging to the Oriental Region or to territories transitional between the Palearctic and Oriental Regions; Emeljanov 1974) and parts of China, Japan, and southern­ most Korea. Because Pleistocene glaciation did not cover the eastern part of its territory, the region contains many floristic and faunistic rel­ icts (Axelrod 1975b). The insect fauna of the Orthrian region is rich and has many Oriental elements. For example, the leaf‐beetle fauna of the small Himalayan country of Nepal has 797 species, which is nearly half the number of spe­ cies in the entire fauna of the former USSR (Medvedev and Sprecher‐Uebersax 1999) and more than twice that in Mongolia (Medvedev 1982). The most primitive dragonfly family, Epiophlebiidae, occurs in the Orthrian region (Himalayas and Japan) (Kryzhanovsky 2002). Faunal connections between the Mediterra­ nean subregion of the Hesperian region and the Orthrian region are of interest. Species of a few buprestid genera are split almost evenly between these zoogeographical entities: Polyctesis has two species in the Mediterranean subregion and two in the  Orthrian region, Ptosima has one species in the Mediterranean subregion and two in the Orthrian region. Eastern Mediterranean and Irano‐Turanian faunal elements are com­ mon in the West Orthrian subregion, but disap­ pear in the eastern portion of the region.

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Species of the predominantly Western Palearctic and Afrotropical buprestid genera Julodis (Fig. 7.3a) and Julodella (Fig. 7.3b) occur in the West Orthrian subregion. The West Orthrian subre­ gion is also the western limit for Oriental genera such as Microacmaeodera, and the northern limit of distribution for the Paleotropical genera Sternocera and Coroebina. From west to east in the Orthrian region, the influence of the Oriental fauna increases significantly. In Yunnan, for example, about half of the bupres­ tid  fauna is Oriental. An influence of the Holarctic  and Stenopean groups increases in the East  Orthrian subregion, as illustrated by  a  few  buprestid genera and subgenera: Nipponobuprestis (six species in Southern China and Japan) and Sapaia (Yunnan and North Vietnam) (Volkovitsh and Alexeev 1988, Kuban’ et al. 2006). 7.12.6  Steppe (Scythian) Region

The steppe (Fig. 7.1aVII; Fig. 7.7a) stretches from the Hungarian lowland to eastern Siberia, Mongolia, and northern China, with the south­ ern border along the Black Sea, Crimean and Caucasian mountains, and the deserts of Kazakhstan and Middle Asia. The steppe is characterized by the following climatic condi­ tions: well developed to extreme continentality (Mongolian steppes differ by more than 100 °C between the winter minimum and summer maximum), limited and uneven precipitation, and strong winds. Genuine steppe landscape nearly lacks forests, with only some gallery for­ ests situated along the rivers, small isolated for­ ests in depressions (ovragi, balki), and mountain forest belts. The steppe landscape (the steppe proper, prairies, and pampas), occupying only 8% of the planet’s land surface, provides 80% of the world’s cereals and meat and other cattle products (Mordkovich et al. 1997); 66% of the steppes are located in Eurasia. Due to fertile soils and favorable climate, the steppes have been severely transformed by agriculture. Some steppe ­remnants occur in southern Ukraine and the

south of European Russia, but in the northern Caucasus, steppe communities are almost entirety gone, except for some fragments on slopes unsuitable for agriculture (Korotyaev 2000). The same is true for the nearly com­ pletely cultivated northern Kazakhstan steppes (“Tselina” = virgin soil). Large steppe areas still exist in Tuva and Mongolia. The steppe is usually subdivided into the West Scythian and East Scythian subregions (Emeljanov 1974), with the boundary in the area between the Altai Mountains and Yenisei River; subregions are further divided into provinces and subprovinces. The boundary between the Western and Eastern Palearctic steppe faunas is quite sharp. In the close territories of southeast­ ern West Siberia and Tuva, the weevil faunas are nearly equal, consisting of 320 species (Krivets 1999) and 311 species, respectively (B.A.K., unpublished data), including one and at least 35 species, respectively, of Stephanocleonus. Strong, frequent winds might be largely responsible for flightless forms in the steppes. Flightlessness is particularly common for ground‐dwelling beetles. Among them, the spe­ cies‐rich cerambycid genus Dorcadion is char­ acteristic of the central and western parts of the Scythian region, whereas its close relative Eodorcadion populates the eastern part. Species of Dorcadion are active in the spring, and those of Eodorcadion in the middle of the summer, according to the maximum precipitation in the respective regions. Many steppe carabids are also flightless, including the most conspicuous, viz., Callisthenes and some Calosoma (Fig. 7.2a). Flightless insects are common in dry variants of the steppes with sparse vegetation: for example, in Tuva and Mongolia, where the predominance of medium‐sized and large wingless orthopter­ ans and beetles is impressive. Some large weevil genera with almost exclusively fully winged spe­ cies are represented in the Palearctic steppes by wingless species. Examples include two wing­ less species out of more than 50 Pseudorchestes in the Palearctic  –  Pseudorchestes tschernovi Korotyaev and Pseudorchestes convexus Korotyaev, which are minute leaf‐miners on

7  Insect Biodiversity in the Palearctic Region

semidesert and desert wormwoods (Artemisia pauciflora Web. ex Stechm. etc.) in Kazakhstan and Mongolia (Korotyaev 2011a)  –  and the entire subgenus Anthonomidius of the world­ wide Anthonomus, with four species on Potentilla. A characteristic feature of steppe vegetation is the prevalence of the underground biomass rel­ ative to the above‐ground biomass, leading Paczoski (1917) to call the steppe “the forest upside down.” The proportion of weevils with soil‐inhabiting larvae in the Ciscaucasian steppe (20%), nonetheless, is less than that in the six types of the Trans‐Altai Gobi desert communi­ ties (40–57%) and at the southern boundary of the adjacent mountain steppes (54%), and equals that in the desert solonchaks and oases (Korotyaev 2000). A variety of beetles, from predators to phy­ tophages, are rich in the steppes. S. I. Medvedev (1950) gave an excellent review of the steppe fauna, which is especially detailed for the western steppes. He reported 5300 species of beetles in the steppes from Moldova to Transbaikalia; how­ ever, only half of them occur in the true steppe landscape. Weevils (Curculionidae s.l., except Scolytinae) are the most species‐rich group of beetles in the steppes of the former USSR (763 species), followed by ground beetles (Carabidae, 752 species), rove beetles (Staphylinidae, 657), leaf beetles (Chrysomelidae, 500), and scarabs (Scarabaeoidea, 288) (Medvedev 1950, cited by Iablokov‐Khnzorian 1961). Many groups of saprophagous beetles are well represented in the steppes. The largest beetle genera, Aphodius and Onthophagus, dominate the dung‐beetle assemblages throughout the steppe zone. Some species of Aphodius are asso­ ciated with burrows of steppe rodents, the sus­ liks (ground squirrels) and marmots. Regional faunas of Aphodius include as many as 150 spe­ cies in Kazakhstan and Middle Asia (Nikolajev 1988) and about 50 mostly steppe species in Mongolia (Puntsagdulam 1994). The Mongolian steppe fauna of coprophagous scarabaeids is more diverse (59, 32, and 35 species in the forest steppe, genuine steppe, and desert steppe,

respectively) than is the desert fauna (seven spe­ cies) (Puntsagdulam 1994). The most conspicuous detritophagous group of beetles in the steppes is the family Tenebrionidae, of which the most common is Opatrum sabulosum (L.). A few species of the genus Pedinus also are typical of the East European steppes (P. femoralis (L.) being the most common and widely distributed), but missing from the steppes of Kazakhstan, Mongolia, and Siberia, the fauna of which is dominated by the genera Anatolica, Penthicus, Melanesthes, Scythis, and Blaps with 42, 25, 13, 12, and 10 species, respectively, in Mongolia and Tuva (Medvedev 1990). These genera, except Blaps, are poorly represented in the European steppes, where no genus of Tenebrionidae has gained a particular diversity. For example, on the Taman’ Peninsula, which is predominantly steppe landscape, 21 of the 26 genera of tenebrionid beetles are represented by only one species (B.A.K., unpublished data). Among pollinators, several medium‐sized, hairy, and brightly colored scarabaeoid beetles of the family Glaphyridae, with thin, short elytra (Amphicoma and Glaphyrus)  –  apparently mimicking bumblebees  –  are specific to the western steppes but lacking in the Siberian and Mongolian steppes. Two related families, the Malachiidae and Dasytidae, are common on flowers throughout the steppe zone. Alleculids are conspicuous only in the western steppes. Steppe herbivores are numerous and often zone specific. The Lepidoptera and Coleoptera are apparently most species rich in the steppes. In the Karadagh Nature Reserve in the Crimean steppe, 1516 species of Lepidoptera have been found (Budashkin 1991); 796 species  are recorded from the largely dry‐woodland Abrau Peninsula in the Black Sea, and 300 s­ pecies from the almost forestless Taman’ Peninsula (Shchurov 2004). In the steppes  of  the  Northwestern Caucasus near Novoaleksandrovsk, 169 species of weevils dominate the herbivorous insect assemblage,  with the second largest group, the Chrysomelidae, barely reaching half the weevil total, and other beetle families (Buprestidae and

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Cerambycidae) being represented by at most six or seven species. The Auchenorrhyncha (plan­ thoppers and leafhoppers) and Orthoptera have no more than 20 and six species, respectively, in that area (Korotyaev 2000, 2001a; B.A.K., unpub­ lished data). Most steppe‐specific buprestids are represent­ atives of Sphenoptera (subgenera Chilostetha and Sphenoptera s. str.), which are mainly root borers; Agrilus (subgenus Xeragrilus), which are associ­ ated mainly with Artemisia; and endemic Palearctic Cylindromorphus, which feed on Cyperaceae and Poaceae. Leaf‐mining species of the genus Trachys are common on Lamiaceae plants in the western steppes, and those of Habroloma are associated mainly with Erodium (Geraniaceae). The tribe Dorcadionini, with soil‐inhabiting larvae, is the most characteristic group of cer­ ambycid beetles in the steppes. The three cer­ ambycid genera with the greatest numbers of species in the Caucasus  –  Dorcadion (43), Phytoecia (40), and Agapanthia (16)  –  com­ prise more than a quarter of the entire fauna (343 species) of this extensively wooded mountain system. They are associated with herbaceous vegetation, and most  –  31 of 43 species of Dorcadion in the Caucasus (Danilevskii and Miroshnikov 1985)  –  live in the steppes. Leaf beetles have a number of groups specific to the steppes. No fewer than 50 species of sev­ eral subgenera of Chrysolina occur in the steppes, and some large subgenera (e.g., Pezocrozita) are subendemic. All species of Chrysolina are associ­ ated with herbs and semishrubs (mostly Artemisia species), and are especially diverse in the steppes of southern Siberia and Mongolia. Many Chrysolina of the central Palearctic steppes are wingless. Chrysolina and two tribes of actively flying leaf beetles, the Clytrini and Cryptocephalini (Fig. 7.2d), with no flightless species in the Palearctic, dominate the steppe chrysomelid assemblages. In the Cryptocephalini, Cryptocephalus is the most species‐rich genus of leaf beetles in the steppes and includes many common species on Artemisia, Atraphaxis, and

Caragana, the most characteristic steppe semi­ shrubs and shrubs. The steppe flea‐beetle (Alticini) fauna is the most species rich among the flatland flea‐bee­ tle faunas of the European part of the former USSR, with 198 species (Konstantinov 1991). This fauna also has the lowest percentage of species with transpalearctic ranges (16.2%) (Konstantinov 1991). In the Bruchinae, the monotypic tribe Kytorhinini includes 12 species of the single genus Kytorhinus, associated mostly with Caragana (Fabaceae) and distributed from Austria and southeastern European Russia to Nepal and the Far East (Anton 2010, Legalov 2011; Kytorhinus kergoati Delobel and Legalov is erroneously referred to as “rushanensis” in the latter publication), with one circumboreal spe­ cies, Kytorhinus pectinicornis Melichar (Legalov 2011). The single member of the monotypic subgenus Kytorhinoides, Kytorhinus thermopsis Motschulsky, is associated with the steppe herb Thermopsis lanceolata, which is subendemic to the steppe zone. The genera Bruchidius, Bruchus, and Spermophagus are represented in the steppes by a few species, including some endemics. A Nearctic species, Acanthoscelides pallidipennis (Motschulsky), has been intro­ duced together with its American host, a ripar­ ian bush, Amorpha fruticosa L. (Fabaceae), and is now the second most common bruchid (after Spermophagus sericeus Geoffroy) in the North Caucasian steppes, having reached China in the east. Two other alien species, the East Asian Megabruchidius tonkineus and M. dorsalis, have become established in the Northwestern Caucasus in recent decades and infest seeds of the honey locust tree, G. triacanthos, in the windbreaks (Korotyaev 2015). The largest phytophagous group, the Curculionoidea, is species rich in the steppes. Of the 11 families in the steppes, only the Apionidae and Curculionidae are represented by more than 10 species, but most of the families, except the Nanophyidae and Dryophthoridae, include at least one endemic or subendemic steppe spe­ cies. The Nemonychidae (Fig. 7.5b) and

7  Insect Biodiversity in the Palearctic Region

Brachyceridae occur only in the southeastern European steppes. The Anthribidae and Rhynchitidae are represented by one endemic species each in the Continental Sector on Caragana (Fabaceae) and Spiraea (Rosaceae), respectively. The Urodontidae include 10 spe­ cies of the Palearctic genus Bruchela in the steppes, of which Bruchela orientalis (Strejček) is trans‐zonal, Bruchela exigua Motschulsky is endemic to extreme southeastern Europe, and Bruchela kaszabi (Strejček) is endemic to south­ ern Mongolia; all are associated with xerophilic Brassicaceae. The Erirhinidae include the trans‐ zonal riparian endemic Lepidonotaris petax (Sahlberg) and East Scythian Notaris dauricus Faust. The Attelabidae are represented in east­ ern Mongolia and Transbaikalia by a few Stenopean species, mostly on Ulmus pumila L. The Apionidae are common throughout the entire steppe zone from its southernmost parts to the cold steppes and tundra steppe of the Siberian Arctic zone. They comprise 11% of the entire Curculionoidea fauna (410 species) of the steppe on Taman Peninsula (Korotyaev 2004; B.A.K., unpublished data), and 12% of the 169 species of the steppe of Stavropol Territory in the Northwestern Caucasus (Korotyaev 2000, 2001b; B.A.K., unpublished data). In Siberia and Mongolia, with their impoverished steppe flora and extreme continental climate, the Apionidae constitute a smaller part of the steppe‐weevil fauna (about 3% in the steppe zone of Tuva, with somewhat more than 220 species). The Curculionidae are the most species‐rich family in the entire steppe zone, although only a few estimates are available. Of the two investigated steppe areas in the plains of the Northwestern Caucasus, one is the Taman Peninsula (Korotyaev 2004). The other steppe area is a fragment of about 2 hectares isolated from the closest native vegeta­ tion by fields and orchards (Korotyaev 2000). Both lists of the Curculionoidea are dominated by the Ceutorhynchinae, Entiminae, and Curculioninae, followed by the Apionidae. Aside from the steppes of China, where no specific studies have been con­ ducted, the rest of the Eurasian steppe‐weevil fauna is characterized by dominance of four

s­ubfamilies, the Ceutorhynchinae, Entiminae, Curculioninae, and Lixinae. The first three are richest in Europe and Anatolia, whereas the Lixinae overwhelmingly dominate in Mongolia and adjacent parts of Eastern Siberia. The xylophagous Curculionoidea are poorly represented in the steppes. Scolytines are repre­ sented mostly by thamnobionts and dendrobi­ onts that develop on steppe bushes such as Prunus spinosa L. No specialized scolytid spe­ cies is known on Caragana, a genus characteris­ tic of the Central Asian steppes, and only one polyphagous species has been recorded from this steppe bush in Mongolia (Yanovsky and Tegshzhargal 1984). One scolytid genus, Thamnurgus, is herbivorous. One of its species, Thamnurgus russicus Alexeev, is endemic to the meadow‐steppe subzone of European Russia, developing on Delphinium cuneatum Stev. (Ranunculaceae) (Alexeev 1957), and another species, Thamnurgus caucasicus Reitter, is com­ mon on Carduus (Asteraceae) in the North Caucasian steppes. Only a few scolytid species are found in the steppe on the Taman’ Peninsula. In addition to Th. caucasicus, a single species of Scolytus has been found on cut branches of fruit trees in a village, one species attacks introduced conifers, and one lives on introduced Fraxinus pennsylvanica. No herbivorous cossonine is known in the steppe, but a few xylophagous spe­ cies attack trees in riparian stands and groves of U. pumila in the southeastern Mongolian steppe. The only xylophagous family‐group taxon of the Curculiondae represented in the steppe zone is the Mesoptiliinae, which includes four species in Mongolia and Transbaicalia on Amygdalus, Grossularia, and U. pumila (Barrios 1984); most of them also occur in the neighbor­ ing zones. 7.12.7  Desert (Sethian) Region

Palearctic deserts form a great belt stretching from northern Africa to northwestern China and western India (Fig. 7.1aVIII; Fig. 7.7b). Depending on the climatic conditions, soil com­ position, and vegetation, three large subregions

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usually are distinguished in Palearctic deserts: Saharo‐Arabian, Irano‐Turanian, and Central Asian (Lavrenko 1950, Emeljanov 1974, Kryzhanovsky 2002). Geographic position and climate partly determine the similarities and distinctions among the insect faunas of all sub­ regions. The Saharo‐Arabian subregion includes a great number of taxa of Afrotropical origin. The Irano‐Turanian subregion shares many taxa with the Mediterranean subregion, par­ ticularly with the East Mediterranean Province of the Hesperian region, whereas its North Turanian Province has many features of the Central Asian subregion. The flatland desert insect fauna is xerophilic and relatively poor, other than some desert‐spe­ cific groups. Of approximately 800 species of leaf beetles in Central and Middle Asia, 233 are found in deserts (Lopatin 1999). The Cryptocephalinae are the most numerous, fol­ lowed by the Alticini and Eumolpinae. Some insect groups are poorly represented or absent in flatland deserts, such as grasshop­ pers (Orthoptera: Ensifera), earwigs (Dermaptera), aphids (Aphidina), some brown lacewings (Hemerobiidae), ground beetles (Carabidae, excluding specialized groups), Megaloptera, Raphidioptera, and Mecoptera. Other insect groups are abundant in the deserts, such as some groups of Blattodea, Mantodea, Orthoptera (particularly some groups of locusts: Catantopinae, Oedipodinae, and Pamphaginae), Hemiptera (particularly Psyllina, Auchenorrhyncha, and Heteroptera), and Neuropterida (Ascalaphidae, Mantispidae, Myrmeleontidae, and Nemopteridae; Fig. 7.2b). The desert fauna has a large percentage of endemic taxa (Kryzhanovsky 1965). In the Orthoptera, the family Acrididae contains a number of endemic tribes (Dericorythini, Diexini, Egnatiini, Iranellini, and Uvaroviini), mostly in the subfamily Catantopinae, which is common in both the Sahara and Gobi subre­ gions (Sergeev 1993). Endemics constitute almost 70% of the leaf beetles (Lopatin 1999). Insect biodiversity sharply increases in the mountains, with altitude belts inhabited by

mesophilous groups, particularly in the Irano‐ Turanian subregion (Kryzhanovsky 2002). The borders between steppes and deserts in the Palearctic generally are not sharp and usu­ ally are represented by an intermediate subzone of semideserts now typically attributed to the steppe zone as the desert steppe. Faunal changes along climatic and vegetational gradients are illustrated with examples of three family‐group taxa of the Coleoptera in the Trans‐Altai Gobi. Gradual changes were studied in species assem­ blages of the superfamily Curculionoidea (Table 7.3), Chrysomelidae (except Bruchinae) and Tenebrionidae (Table 7.6) across six types of zonal plant communities, from steppefied deserts (sites 6 and 5) in the north of the 160 km long soil and vegetation profile to extra‐arid deserts with only one (site 2) or two species of plants (site 1) (Fig. 7.3d). The general pattern is a subsequent substitution of species with the greatest portions of their ranges in the moun­ tain steppe or desert steppe north of site 6 by species distributed in true deserts. The Tenebrionidae differ from the herbivo­ rous taxa in the broader overlap of the steppe and desert complexes along the profile, such that the number of tenebrionid species is greater than the number of weevils at most sites, although the total number of weevils in the pro­ file is 1.3 times that of tenebrionids. Also distin­ guishing the Tenebrionidae from the herbivorous beetles is their much larger portion of zonal desert species in the total Trans‐Altai Gobi fauna (Table 7.6): 59% for the tenebrionids, com­ pared with 37% for the Curculionoidea and 31% for the Chrysomelidae (excluding Bruchinae). A drop in biodiversity occurs at site 6 close to the Dzhinst Mountains, with developed steppe com­ munities, relative to the more distant site 5. The greatest diversity is found at the sandy Haloxylon desert (site 4). Two special faunistic surveys of Coleoptera have been conducted in different parts of the Palearctic deserts. The first was by a French scientific mission (Peyerimhoff 1931) along an 800 km route in the Central Sahara, including the Hoggar Plateau, in February–May 1928,

7  Insect Biodiversity in the Palearctic Region

Table 7.6  Distribution of Tenebrionidae across six types of desert plant community in Trans‐Altai Gobi, Mongolia. Steppe species (+)

6† 5

4

3

1

Desert species (*)

—

*

Dilamus mongolicus Kaszab

—

*

Penthicus lenczyi Kaszab

— Blaps miliaria Fischer de Waldheim

2

* +

Psammoestes dilatatus Reitter

*

Melanesthes heydeni Cziki

+

+

Platyope mongolica Faldermann

+

+

*

Blaps kiritshenkoi Semenov and Bogačev * *

Melanesthes czikii Kaszab *

Monatrum prescotti Faldermann

+

+

+* *

*

Blaps femoralis medusula Kaszab

+

+

+* *

*

*

Sternoplax mongolica Reitter

*

Anatolica polita borealis Kaszab

Anatolica mucronata Reitter

Catomus mongolicus Kaszab

+

+

+* *

*

*

Blaps kashgarensis gobiensis Frivaldski

Anatolica cechiniae Bogdanov‐Kat’kov

+

+

+* *

*

*

Trigonoscelis sublaevigata granicollis Kaszab

Anatolica sternalis gobiensis Kaszab

+

+

+* *

*

*

Cyphosthete mongolica Kaszab

+* +* *

*

*

Anatolica amoenula Reitter

Eumilada punctifera amaroides Reichardt + Epitrichia intermedia Kaszab

+* +

Microdera kraatzi Reitter

+* +* +* +* + +* Cyphogenia intermedia A. Bogačev

—

*

*

+* * *

*

Anemia dentipes Ballion *

Pterocoma reitteri Frivaldszky

† Numbers 6 to 1 indicate desert plant communities from north (6) to south (1): 6, Anabasis brevifolia steppefied desert; 5, Reaumuria soongorica + Sympegma regelii desert; 4, Haloxylon ammodendron desert; 3, Reaumuria soongorica + Nitraria sphaerocarpa desert; 2, extra‐arid Iljinia regelii desert; 1, extra‐arid Ephedra przewalskii + Haloxylon ammodendron (in dry temporary waterbeds) desert.

and the second was a part of the investigation on insects in the main plant communities of the Trans‐Altai Gobi in July–early October 1981 and in the summer of 1982 by the Joint Soviet–Mongolian Biological Expedition (Korotyaev et  al. 1983). Although the periods and organization of the collecting differed sig­ nificantly, the results are similar (Table 7.7). Differences in the family sets from the two sur­ veys are of two kinds. The absence of several aquatic families in the Trans‐Altai Gobi is due to the small number and small size of natural water bodies, whereas a rather large river and several freshwater streams were investigated in the Sahara. The other important difference is the presence of the two predominantly tropical families in the Sahara, the Bostrichidae and Brentidae, which can be explained by the ­location of the area at the southern border of

the Palearctic. The presence of several families (e.g., Alleculidae, Cantharidae, Leiodidae, Nitidulidae, Oedemeridae, and Pselaphidae) with one or two species in only one of the two faunas is probably accidental, resulting mainly from the difference in collecting periods. Several features are common to the Gobian and Saharan beetle faunas and characteristic of the desert Palearctic fauna in general. These are the leading positions of the Curculionidae and Tenebrionidae and the relatively wide represen­ tation of other large families such as the Buprestidae, Carabidae, Chrysomelidae, Scarabaeidae, and Staphylinidae, but not the Cerambycidae. Also noteworthy is the absence of the Silphidae from the desert faunas, in sharp contrast to the Mongolian steppes, where the large black beetle Necrophorus argutor Jakovlev is common around dense colonies of pikas and

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Table 7.7  Number of species of Coleoptera in the Trans‐Altai Gobi and Central Sahara. Family

Trans-Altai Gobi

Central Sahara

Carabidae

43

36

Haliplidae

—

1

Dytiscidae

4

19

Gyrinidae

—

2

Georyssidae

—

1

Hydrophilidae (including Helophoridae)

5

13 (including Helophoridae and Hydraenidae)

Hydraenidae

3

?

Histeridae

15

11

Leiodidae

1

—

Staphylinidae

30

43

Pselaphidae

—

2

Scarabaeidae sensu lato

15 (Aphodius, 6; Onthophagus, 1)

30

Dryopidae

—

4

Heteroceridae

—

2

Buprestidae

16 (Anthaxia, 1; Acmaeoderella, 1; Sphenoptera, 7; Agrilus, 3; Paracylindromorphus, 1)

20 (Anthaxia, 4; Acmaeodera, 4; Sphenoptera, 2; Agrilus, 1; Cylindromorphus, 1)

Elateridae

9 (Aeoloides, 1; Aeloderma, 1; Zorochrus, 1; Agriotes, 1; Cardiophorus, 2)

8 (Drasterius, 2; Zorochrus, 1; Agriotes, 1; Cardiophorus, 1)

Cantharidae

1

—

Dermestidae

12 (Dermestes, 4; Attagenus, 6 or 7; Anthrenus, 2)

11 (Dermestes, 1; Attagenus, 5; Anthrenus, 1)

Bostrichidae

—

8

Anobiidae

2 (Xyletinus)

1 (Theca)

Stylopidae

1

—

Cleridae

3 (Emmepus arundinis Motsch., Necrobia rufipes DeG., Opetiopalpus sabulosus Motsch.)

4 (Emmepus sp., Necrobia rufipes)

Dasytidae

—

5

Melyridae

3

5

Nitidulidae

—

1

Cybocephalidae

2

3

Phalacridae

4

2

Cucujidae

2

2

Silvanidae

1 (Airaphilus sp.)

1 (Airaphilus sp.)

Helodidae

—

1

7  Insect Biodiversity in the Palearctic Region

Table 7.7  (Continued) Family

Trans-Altai Gobi

Central Sahara

Cryptophagidae

3 (Cryptophagus, 2)

1 (Cryptophagus)

Coccinellidae

27 (Hyperaspis, 1; Coccinella, 5; Scymnus s. l., 6; Pharoscymnus, 2)

11 (Hyperaspis, 1; Coccinella, 1; Scymnus s. l., 4; Pharoscymnus, 2)

Mordellidae

4 (Mordellistena, 3; Pentaria, 1)

3 (Mordellistena, 1; Pentaria, 2)

Rhipiphoridae

1 (Macrosiagon medvedevi Iablokov‐Khnzorian)

1 (Macrosiagon)

Oedemeridae

1 (Homomorpha cruciata Sem.)

—

Anthicidae

15 (Steropes latifrons Sumakov; Notoxus, 2; Anthicus s. l., 11; Formicomus sp., 1)

19 (Notoxus, 2; Anthicus s. l., 14)

Meloidae

3

23

Alleculidae

—

1

Tenebrionidae

42

70

Scraptiidae

1 (Scraptia sp.)

1 (Scraptia straminea Peyer.)

Cerambycidae

4 (Chlorophorus ubsanurensis Tsherep., Ch. obliteratus Ganglb., Asias mongolicus Ganglb., Eodorcadion kozlovi Suv.)

6

Chrysomelidae

51 (including Bruchinae (6): Rhaebus, 1; Spermophagus, 2; Bruchidius, 3)

23 (including Bruchinae (2): Caryoborus, 1; Bruchidius, 1)

Anthribidae (Urodontinae)

1 (Bruchela)

5

Brentidae

—

1

Apionidae

15

13

Curculionidae

73

39

susliks. The Scolytinae also are absent, although a desert species, Thamnurgus pegani Eggers, is found on Peganum harmala L. (Peganaceae) in Turkmenistan. Relatives of this beetle are known from Euphorbiaceae in tropical Africa and the Mediterranean (Mandelshtam et al. 2011). To survive in extreme desert conditions, insects have developed a number of specialized behavioral, ecological, morphological, and physiological adaptations. Sand‐desert forms have arisen in several beetle families (e.g., Dermestidae; Zhantiev 1976). The set of hyper­ throphied characters can mask the affinities to such an extent that a desert dermestid, Thylodrias contractus Motschulsky, has been described repeatedly in several families (R. D. Zhantiev, personal communication). Adaptive rearrangements of various body structures are

manifested by desert Braconidae (Hymenoptera). In addition to depigmentation of the integu­ ment and enlargement of the eyes, in connec­ tion with nocturnal activity, the braconid wasps exhibit a smoothening of the body sculpture for reflection of light and heat, shortening of the wings with basal shifting of the cells associated with strong winds in open landscapes, and elon­ gation of the labiomaxillary complex for feeding on flowers of desert plants (Tobias 1968).

­Acknowledgments Dedication: We dedicate our chapter to the memory of an outstanding entomologist, Gleb Sergevich Medvedev, who was a mentor and a friend for most of our lives, and from whom we

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learned very much and could have learned much more. The work presented in this chapter would not have been possible without help and advice from our friends and colleagues – experts on various insect groups – especially those at the Zoological Institute in St Petersburg (Russia), including L. N. Anisyutkin (Blattodea, Dermaptera), S. A. Belokobylsky (Hymenoptera: Braconidae), A. F. Emeljanov (Auchenorrhyncha, zoogeography), N. V. Golub (Psocoptera, Zoraptera), A. V. Gorokhov (Orthoptera), D. R. Kasparyan (Hymenoptera: Ichneumonidae), the late I. M. Kerzhner (Heteroptera), O. V. Kovalev (Hymenoptera: Cynipoidea), V. A. Krivokhatsky (Neuropteroidea), V. G. Kuznetsova (Psocoptera, Zoraptera), A. L. Lobanov (Coleoptera, data­ bases), A. L. Lvovsky (Lepidoptera), M. Yu. Mandelshtam (Scolytinae), A. Yu. Matov (Lepidoptera, Noctuidae), the late G. S. Medvedev (Coleoptera: Tenebrionidae), E. P. Nartshuk (Diptera), the late Yu. A. Pesenko (Hymenoptera: Apoidea), S. Yu. Sinev (Lepidoptera), and A. V. Stekolshchikov (Sternorrhyncha: Aphidina), and from many other institutions, M. L. Chamorro‐Lacayo (Trichoptera, Department of Entomology, University of Minnesota, MN, USA), the late O. N. Kabakov (St Petersburg, Russia), N. Ju. Kluge (Ephemeroptera, Department of Entomology, St Petersburg University, Russia), A. S. Lelej (Hymenoptera: Mutillidae, Institute of Biology and Soil Science, Far Eastern Branch, Russian Scademy of Sciences, Vladivostok, Russia), S. W. Lingafelter, M. Pogue, F. C. Thompson, and N. E. Woodley (Systematic Entomology Laboratory, USDA, Washington DC, USA), K. V. Makarov (Moscow State Teacher‐training University, Moscow, Russia), W. Steiner (Department of  Entomology, Smithsonian Institution, Washington DC, USA), I. Löbl (Geneva, Switzerland), the late I. K. Lopatin (Department of Zoology, Byelorussian State University, Minsk, Belarus), R. D. Zhantiev (Department of Entomology, Moscow State University, Moscow, Russia), and A. G. Zinovjev (Hymenoptera: Tenthredinidae, Boston, MA, USA).

We thank V. I. Dorofeyev (Komarov Botanical Institute, Russian Academy of Sciences, St Petersburg) for identification of some plants referred to in the text; D. I. Berman and Yu. M. Marusik (Institute of Biological Problems of the North, Far Eastern Branch, Russian Academy of Sciences, Magadan), O. A. Khruleva (Institute of the Ecology and Evolution, Russian Academy of Sciences, Moscow), and S. A. Kuzmina (Paleontological Institute, Russian Academy of Sciences, Moscow) for useful advice and the many‐year supply of interesting material col­ lected in their studies in the north; D. I. Berman for excellent photographs of northern land­ scapes; O. Merkl (Hungarian Natural History Museum, Budapest) for help at the Budapest Museum and consultations and excursions with B.A.K. to several unique landscapes in Hungary; A. L. L. Friedman (Department of Zoology, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel) for loan of material of Israeli Coleoptera, consultation on the Israeli fauna, providing useful literature, and organizing a col­ lecting trip in Israel for B.A.K.; L. Gültekin (Atatürk University, Erzurum, Turkey) for organizing collecting trips to Turkey and the fruitful long‐term collaboration; N. A. Florenskaya (St Petersburg, Russia) for the habi­ tus illustration of Theodorinus lopezcoloni; H. Bradford for the habitus illustration of Cimberis attelaboides and E. Roberts (Systematic Entomology Laboratory, USDA, Washington DC, USA) for the habitus illustration of Clavicornaltica dali; and K. V. Makarov (Moscow State Teacher‐Training University) for the design and production of Fig. 7.6, with his excellent photographs of Tenebrionidae from the Taman’ Peninsula. The work was performed with the use of the collection of the Zoological Institute, Russian Academy of Sciences, St Petersburg. We greatly appreciate the advice and construc­ tive suggestions of our friends and colleagues who read this manuscript at various stages of completion: V. Grebennikov (Entomology, Canadian Food Inspection Agency, Ottawa), V. Gusarov (Department of Zoology, Natural

7  Insect Biodiversity in the Palearctic Region

History Museum, University of Oslo, Oslo, Norway), S. W. Lingafelter, R. Ochoa, A. Norrbom (Systematic Entomology Laboratory, Washington DC, USA), and A. K. Tishechkin (Department of Entomology, Louisiana State University, Baton Rouge, Louisiana, USA). We are particularly thankful to P. H. Adler and R. Foottit for editing this manuscript and their numerous and valuable suggestions. The studies of M.G.V. and B.A.K. were per­ formed in the framework of the State Research Project nos. AAAA-A17-117030310210-3 and -117030310205-9 and supported by the Russian Foundation for Basic Research (grant  nos. 13‐04‐01002 A, 13‐04‐10002 K and 16-04-00412A).

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Schuh, R. T. and J. A. Slater. 1995. True Bugs of the World (Hemiptera: Heteroptera): Classification and Natural History. Cornell University Press, Ithaca, New York. 336 pp. Schultz, J. 1995. The Ecozones of the World: The Ecological Divisions of the Geosphere. Springer‐ Verlag, Berlin. 449 pp. Sclater, P. L. 1858. On the geographical distribution of the class Aves. Journal of the Linnean Society of London, Zoology 2: 130–145. Sergeev, M. G. 1993. The general distribution of Orthoptera in the main zoogeographical regions of North and Central Asia. Acta Zoologica Cracoviensia 36: 53–76. Sharkov, A. V. 1995. Family Eupelmidae – Eupelmid wasps. Pp. 170–177. In P. A. Lehr (ed). Key to Insects of the Russian Far East. Volume 4. Neuropteroidea, Scorpionflies, Hymenopterans. Part 2. Nauka, St Petersburg. [In Russian]. Shchurov, V. I. 2004. The butterfly and moth fauna (Insects, Lepidoptera) of the Taman’ Peninsula. Pp. 53–68. In Yu. V. Lokhman (ed). Ekologicheskiye Problemy Tamanskogo Poluostrova. Kubanskii Gosudarstvennyi Universitet, Krasnodar. [In Russian]. Semenov‐Tian‐Shansky, A. 1936. Limits and Zoogeographic Divisions of the Palearctic Region for Land Animals Based on the Distribution of Coleopterous Insects. Academy of Sciences Publishing House, Moscow– Leningrad. 16 pp. [In Russian]. Sinitsyn, V. M. 1965. Ancient Climates of Eurasia. Part 1. Paleocene and Neocene. Leningrad. 167 pp. [In Russian]. Smith, N., S. A. Mori, A. Henderson, D. Wm. Stevenson and S. V. Heald. 2004. Flowering Plants of the Neotropics. Princeton University Press, Princeton, New Jersey. 594 pp. Sochava, V. B. 1953. Vegetation of the forest zone. Pp. 7–61. In E. N. Pavlovsky (ed). Animal World of the USSR. Volume 4. Izdatel’stvo Akademii Nauk SSSR; Moscow, Leningrad. [In Russian]. Steinmann, H. 1997. World Catalogue of Odonata. Volume 1. Zygoptera. The Animal Kingdom. A Compilation and Characterization

of the Recent Animal Groups. 110. Walter de Gruyter, Berlin, Germany. 500 pp. Storozheva, N. A., V. V. Kostjukov and Z. A. Efremova. 1995. Family Eulophidae – Eulophid wasps. Pp. 291–505. In P. A. Lehr (ed). Key to Insects of the Russian Far East. Volume 4. Neuropteroidea, Scorpionflies, Hymenopterans. Part 2. Nauka, St Petersburg. [In Russian]. Sugonyaev, E. S. and N. D. Voinovich. 2006. Adaptations of Chalcidoid Wasps (Hymenoptera, Chalcidoidea) for Parasitization Soft Scales (Hemiptera, Sternorrhyncha, Coccidae) under Different Latitude Conditions. KMK Scientific Press Ltd., Moscow. 263 pp. [In Russian]. Taeger, A., S. M. Blank and A. D. Liston. 2006. European sawflies (Hymenoptera: Symphyta) – a species checklist for the countries. Pp. 399–504. In S. M. Blank, S. Schmidt and A. Taeger (eds). Recent Sawfly Research: Synthesis and Prospects. Goecke and Evers, Keltern. Takhtajan, A. L. 1978. Floristic Regions of the World. Nauka, Leningrad. 246 pp. [In Russian]. Tobias, V. I. 1968. System, Phylogeny, and Evolution of the Family Braconidae (Hymenoptera). Abstract of the DSc Dissertation. Leningrad. 28 pp. [In Russian]. Trjapitzin, V. A. 1989. Parasitic Hymenoptera of the Fam. Encyrtidae of the Palearctic. Nauka, Leningrad. 487 pp. [In Russian]. Ukrainsky, A. S. 2013. The harlequin lady beetle, Harmonia axyridis Pall. (Coleoptera, Coccinellidae) in the North Caucasus. Euroasian Entomological Journal 12: 35–38. [In Russian]. Volkovitsh, M. G. 2007. Emerald Ash Borer, Agrilus planipennis – a new dangerous ash pest in European Russia. http://www.zin.ru/ Animalia/Coleoptera/rus/eab_2007.htm [Accessed 22 May 2013]. Volkovitsh, M. G. and A. V. Alexeev. 1988. Comparative characteristics of the fauna of buprestids (Coleoptera, Buprestidae) of Northern Eurasia. Pp. 42–58. In V. V. Zlobin (ed). Svyazi Entomofaun Severnoi Evropy i

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Sibiri. Zoologicheskii institut Akademii nauk SSSR, Leningrad. [In Russian]. Volkovitsh, M. G. and A. L. Lobanov. 1997. Data bank of host associations of the buprestid tribe Acmaeoderini (Coleoptera, Buprestidae) of the Palearctic. Pp. 166–187. In S. D. Stepan’yants, A. L. Lobanov and M. B. Dianov (eds). Bazy Dannykh i Komp´Yuternaya Grafika v Zoologicheskikh Issledovaniyakh. Trudy Zoologicheskogo instituta Rossiiskoi akademii nauk, Volume 269. St Petersburg. [In Russian and English]. Vshivkova, T. S. 2001. Megaloptera. Pp. 373–380. In S. Ya. Tsalolikhin (ed). Key to Freshwater Invertebrates of Russia and Adjacent Lands. Volume 5. Nauka, St Petersburg. [In Russian]. Vtorov, P. P. and N. N. Drozdov. 1978. Biogeography. Prosveshcheniye, Moscow. 271 pp. [In Russian]. Wallace, A. R. 1876. The Geographical Distribution of Animals (2 volumes). Macmillan, London. 607 pp. Walter, H. and S.‐W. Breckle. 1985. Ecological Systems of the Geobiosphere. Volume 1. Ecological Principles in Global Perspective. Springer‐Verlag, Berlin. 242 pp. Wanat, M. 1999. Ryjkowce (Coleoptera: Curculionoidea bez Scolytidae i Platypodidae) Puszczy Bialowieskiej – charakteristika fauny. Parki Narodowe i Rezerwaty Przyrody 18 (3): 25–47. Wei, M., H. Nie and A. Taeger. 2006. Sawflies (Hymenoptera: Symphyta) of China – checklist and review of research. Pp. 503–574. In S. M. Blank, S. Schmidt and A. Taeger (eds). Recent Sawfly Research: Synthesis and Prospects. Goecke and Evers, Keltern. Willig, M. R., D. M. Kaufman and R. D. Stevens. 2003. Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annual Review of Ecology, Evolution and Systematics 34: 273–309. Winkelmann, H. 1991. Liste der Rüsselkäfer (Col.: Curculionidae) von Berlin mit Angaben zur Gefährdungssituation (“Rote Liste”). In A. Auhagen, R. Platen and H. Sukopp (eds). Rote Listen der gefährdeten Pflanzen und Tiere in

Berlin. Schwerpunkt Berlin (West). Landschaftsentwicklung und Umweltforschung, Sonderheft 6: 319–357. Wood, S. L. and D. E. Bright, Jr. 1992. A catalog of Scolytidae and Platypodidae (Coleoptera), Part 2: Taxonomic index. Great Basin Naturalist Memoirs 13: 1–833. Woodley, N. E. 2001. A world catalog of the Stratiomyidae (Insecta: Diptera). Myia 11 (8): 1–475. Yanovsky, V. M. and D. Tegshzhargal. 1984. Bark‐beetles (Coleoptera, Scolytidae) of the Mongolian People’s Republic. Nasekomye Mongolii 9: 404–417. [In Russian]. Yu, D. S. and K. Horstmann. 1997. A catalogue of world Ichneumonidae. Part 1: Subfamilies Acaenitinae to Ophioninae. Memoirs of the American Entomological Institute 58: 1–763. Zamotajlov A. S. (scientific editor). 2007. Red Data Book of Krasnodar (Animals). 2nd edition. Centre of the Development of the Krasnodar Territory, Krasnodar. 480 pp. Zamotajlov, A. S. and A. K. Makaov. 2011. Family Carabidae – Ground Beetles. Pp. 19–58. In A. S. Zamotajlov and N. B. Nikitsky (eds). Coleopterous Insects (Insecta, Coleoptera) of the Republic of Adygea (Annotated Catalogue of Species) (Fauna conspecta of Adygheya. No 1). Maikop, Adygheiskii Gosudarstvennyi Universitet.. [In Russian]. Zamotajlov, A. S., V. N. Orlov, M. V. Nabozhenko, N. V. Okhrimenko, E. A. Khachikov, M. I. Shapovalov and I. V. Shokhin. 2010. Analysis of the pathways of formation of the entomofaunistic complexes in the Northwest Caucasus based on the material of coleopterous insects (Coleoptera). Entomologicheskoe Obozrenie 89: 178–218. [In Russian; English translation: Entomological Review 2010, 90: 331–371]. Zarenkov, N. A. 1976. Lectures on the Theory of the Systematics. Izdatel’stvo Moskovskogo Universiteta, Moscow. 140 pp. [In Russian]. Zarkua, Z. D. 1977. Weevils (Coleoptera: Attelabidae and Curculionidae) of Abkhazia. Abstract of the PhD Dissertation. Baku. 26 pp. [In Russian].

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Zerova, M. D. 1995. Parasitic Hymenoptera – Eurytominae and Eudecatominae of the Palearctic. Navukova Dumka, Kiev. 456 pp. [In Russian]. Zhantiev, R. D. 1976. Dermestids of the USSR Fauna. Izdatel’stvo Moskovskogo Universiteta, Moscow. 181 pp. [In Russian].

Zhiltzova, L. A. 2003. Insecta Plecoptera. Volume 1, Issue 1. Plecoptera, Group Euholognatha. Fauna of Russia and Neighboring Countries. New series N 145. Nauka, St Petersburg, Russia. 537 pp. [In Russian].

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8 Biodiversity of Aquatic Insects John C. Morse Department of Plant and Environmental Sciences, Clemson University, Clemson, South Carolina, USA

Water is critical for life on Earth. Living organ­ isms are composed mostly of water and require water for most of their metabolic functions. Terrestrial species have structures and methods for acquiring water periodically, or they live in habitats that are adequately moist to meet their needs. Many organisms, however, live fully sub­ merged in aqueous habitats, so that water for them is unlimited, as long as the water does not evaporate or disappear for other reasons. Three‐quarters of Earth’s surface is covered with oceans that are rarely or only marginally inhabited by insects. Several reasons have been proposed to explain why insects are so uncom­ mon in oceans, such as low calcium concentra­ tion in seawater, competitive exclusion by Crustacea, or a need to evolve highly sophisti­ cated osmoregulatory and respiration mecha­ nisms simultaneously (Cheng 1976). Apart from oceans, water occurring on and under the sur­ face of the ground is habitat for a highly diverse insect fauna. Unlike ocean water, this water occurring above the level of the oceans is fresh, with typically lower concentrations of salts and other solutes. Below the surface of the ground, water flows slowly in interstitial spaces of sedi­ ments and is especially abundant below the water table, often in aquifers, sometimes dis­ solving rocks, such as limestone, and creating subterranean cracks and caverns. Above the surface of the ground, habitable water occurs in

a variety of lotic (flowing water) habitats includ­ ing seeps, springs, creeks, and rivers, and many kinds of lentic (standing water) habitats such as pools, ponds, lakes, and the many relatively small quantities of water in puddles, aerial epi­ phytes, and artificial containers (e.g., footprints, birdbaths, exposed cisterns, open metal cans, and old tires). Water is of particular concern not only because of its critical importance for life, includ­ ing human life, but also because it is the most obvious habitat into which the effects of terres­ trial activities are concentrated. Precipitation carries to streams and groundwater most of the effects of activities occurring on otherwise “dry land,” including deposition of sewage, fertilizers, carcasses, and other nutrients; release of toxic manufactured products and byproducts; mobi­ lization of sediments that result from exposure of soil to precipitation and runoff; and removal of trees and other riparian vegetation. Because most aquatic insects remain below the surface of the water, they are rarely seen, so the high diversity of insects that inhabit fresh­ water ecosystems for at least part of their lives is poorly known by most people. Most of these insect species, especially in tropical parts of the world, are still unknown even to scientists. Along with other small invertebrates, aquatic insects are an indispensable part of the food web and of nutrient cycling in freshwater e­ cosystems

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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(or “spiraling” in streams, e.g., Newbold et  al. 1982, 1983; Figure. 8.1), and are an essential component of the diets of fish, amphibians, and many birds and mammals. For this reason, insect imitations are attractive to fly‐fishing enthusi­ asts (e.g., McCafferty 1981). Because of the spe­ cies‐specific variation in tolerances that insects have for a wide range of environmental circum­ stances, insects also are used widely as indica­ tors of the level of pollution in the waters that we drink and use for recreation and many practical purposes (Barbour et al. 1999). Eggs, larvae, and pupae of some species of wasps (Hymenoptera) and moths (Lepidoptera), and especially of beetles Coleoptera) and flies (Diptera), occur in freshwater ecosystems, and adults of some of the beetles also live there. Because these groups are discussed in more detail in other chapters, their aquatic species will be mentioned only briefly here. Some groups of insects have only a few species that live in the water or that live closely associated with water, such as grasshoppers (Orthoptera), earwigs (Dermaptera), lice (Phthiraptera), and scorpion­ flies (Mecoptera). Because they contribute little to the themes of this chapter, they will be men­ tioned only briefly. The focus of this chapter, therefore, will be the mayflies (Ephemeroptera), dragonflies and damselflies (Odonata), s­ toneflies

(Plecoptera), bugs (Hemiptera‐Heteroptera), hellgrammites (Megaloptera), spongillaflies (Neuroptera‐Sisyridae, Nevrorthidae), and cad­ disflies (Trichoptera).

8.1 ­Overview of  Taxa 8.1.1  Mayflies (Ephemeroptera)

Mayflies occur globally in a wide variety of lotic and lentic habitats. The life cycle of a mayfly includes egg, larva, subimago (winged imma­ ture form), and imago (male or female adult) stages. Eggs and larvae typically occur in natural lotic and lentic habitats; subimagoes and ima­ goes are aerial and terrestrial, usually flying or resting in vegetation near the habitat of the eggs and larvae. One life cycle usually is completed per year, but some species have more than one generation each year or require two years. Up to 9000 eggs (Fremling 1960) can be laid by a single female on the water surface by touching it or resting on it, below the water surface (a few Baetis species), or from the air above the water (a few species). Eggs usually require a few weeks to develop, but can enter diapause for 3–11 months. Larvae usually eat bits of organic mat­ ter collected or scraped from the substrate or

Figure 8.1  The nutrient spiraling concept provides an understanding of the way that organic nutrients cascade through coarse particulate organic matter (CPOM), dissolved organic matter (DOM), and fine particulate organic matter (FPOM) by the action of physical, chemical, and biological agents as these nutrients pass downstream (Newbold et al. 1982, 1983).

8  Biodiversity of Aquatic Insects

filtered from suspension in the water; a few rare species are predators (Waltz and Burian 2008). A larva undergoes 9–45 molts before swimming to the water surface and emerging as a subimago (Unzicker and Carlson 1982). Usually the sub­ imago flies into the nearby vegetation, where it molts to an imago in a few hours. Adults mate usually while flying, typically after a female flies through a male swarm over or near the water. They live for a few minutes to a few days and do not feed. 8.1.2  Dragonflies and Damselflies (Odonata)

Dragonflies and damselflies are widely distrib­ uted and abundant in almost all permanent fresh and brackish water. They are particularly abundant in warmer waters such as those in lowlands of tropical and subtropical regions. A  few species are semiaquatic in bog moss, damp leaves, and seepages, and a few tropical species inhabit water in bromeliads or tree holes. The Odonata have egg, larval, and adult stages, with eggs and larvae usually submerged in lentic or lotic habitats and aerial adults flying or resting near the water. Eggs can be endo­ phytic, laid in living or dead plant tissue above or below the water through the use of an ovi­ positor, or they can be exophytic, laid in sand or silt in shallow areas of a stream or released above the water surface (Tennessen 2008). They hatch in 5–30 days (Huggins and Brigham 1982), sometimes with a winter diapause (Tennessen 2008). The predatory larvae pass through 10–15 instars and complete a life cycle in a few weeks to as long as five years, depend­ ing on the species and the availability of inverte­ brate prey (Tennessen 2008). Larvae of different species capture prey either by stalking them on the stems of aquatic plants or on the sediment surface, or by hiding in fine sediments and ambushing them. After a larva crawls out of the water onto some stable terrestrial substrate, often at night, adult emergence takes about half an hour. The adult remains close to the water (e.g., Cordulegastridae) or flies away from water for one or more weeks, later returning to its

species‐specific habitat to feed, mate, and lay eggs (e.g., Aeshnidae). Adults are predatory, feeding on other flying insects captured in flight. Males often guard territory into which females are permitted or attracted. Mating typi­ cally occurs in tandem, with a male using the end of its abdomen to grasp the female behind the head while she receives the sperm from spe­ cial copulatory organs on the male’s second or third abdominal sternum, the male having transferred the spermatophore there earlier from the end of its abdomen. A significant mon­ ograph on odonate biology was provided by Corbet (1999). 8.1.3  Stoneflies (Plecoptera)

Stoneflies are distributed globally, mostly in cold mountain streams, but with about one‐ third of all species occurring in the tropics (Zwick 2003). These insects have egg, larval, and adult life‐history stages, with aquatic eggs and larvae and terrestrial adults. Eggs are laid above water or on the water surface. They sink to the bottom and attach to the substrate by a sticky gelatinous covering or by chorionic anchoring devices. The eggs hatch usually in 3–4 weeks, but can undergo diapause for 3–6 months in intermittent habitats, especially in the families Leuctridae, Nemouridae, Perlidae, and Perlodidae. Larvae are generally univoltine, with one generation each year, but they are sometimes semivoltine, with one generation every two or three years. Growth rates can vary in different taxa, especially in those that undergo egg or larval diapause in response to various environmental conditions (Stewart and Stark 2002). The number of larval instars is variable in many stonefly species, ranging from 10 to more than 22 instars (Sephton and Hynes 1982, Butler 1984). Larvae sprawl on the substrate or cling to rocks, feeding mostly as shredders of dead veg­ etation or predators of small arthropods (Stewart and Stark 2008). The emergence of adult stoneflies is similar to that of adult Odonata – larvae crawl out of the water, usually at night, then attach to a rock or log, and exit the

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last larval exuviae in about 5–10 minutes (Stewart and Stark 2002). Adults live 1–4 weeks, and some species feed on epiphytic algae or young leaves or buds (Stewart and Stark 2008). Communication for mating is often facilitated by tapping (“drumming”) on substrates with the  end of the abdomen, the vibrations being detected in the potential mate’s subgenual organs (Stewart and Maketon 1991). Mating is accomplished while standing and facing the same direction, with the male positioned on top of the female (Stewart and Stark 2008). 8.1.4  Cockroaches (Blattodea)

Most cockroaches are terrestrial, but a few tropical species live in epiphytic bromeliads, and others readily enter streams where they swim or climb among submerged vegetation and other substrates. Little is known about the biology of these aquatic cockroaches, but a few species are known to eat living or decomposing plant tissue. 8.1.5  Grasshoppers and Crickets (Orthoptera)

This familiar group of insects is mostly terres­ trial, feeding usually on living plant tissue. A few species feed on plants beside or emerging from streams and ponds (Bland 2008). One species that feeds on water hyacinth is being bred for possible release as a means to control this weed in the wild (Franceschini et al. 2005, Lhano et al. 2005, Adis et al. 2007). 8.1.6  Earwigs (Dermaptera)

One species of this order, Anisolabis maritima (Bonelli), is a predator of small animals beneath litter and driftwood on marine beaches (Langston 1974, Langston and Powell 1975). 8.1.7  Lice (Phthiraptera)

A few species of lice are ectoparasites of birds and mammals that live in freshwater and marine habi­ tats. Some species of Menoponidae, for example, feed on bits of feathers, skin, and blood of geese and ducks (Price 1987), and Echinophthiriidae

suck the blood of otters, sea lions, seals, and wal­ ruses (Kim 1987). 8.1.8  Bugs (Hemiptera)

Most of the cicadas, hoppers, scale insects and their relatives (suborders Sternorrhyncha and Auchenorrhyncha) in this order live on plants that have little or no association with surface water. However, several families of bugs in the suborder Heteroptera are intimately associated with freshwater habitats. Hemiptera probably evolved an aquatic lifestyle at least five times (Carver et al. 1991): 1)  a few species of auchenorrhynchous leaf­ hoppers (Cicadelloidea) feed on the emer­ gent portions of freshwater vascular plants; 2)  among the Hemiptera‐Heteroptera, the Dipsocoroidea are shore‐dwelling burrowers under stones; 3)  the Gerromorpha (or “Amphibicorisae” or “Amphibicorizae”) are all water‐surface dwell­ ing bugs; 4)  the Leptopodomorpha are shore‐dwelling climbers and burrowers; 5)  the Nepomorpha (or “Hydrocorisae” or “Hydrocorizae”) mostly swim beneath the water surface. Most of the species diversity for aquatic bugs is in the Gerromorpha and the Nepomorpha. A variable number of eggs is usually laid beneath or at the surface of the water in plants or in sand, fastened to the substrate at one end with a sticky substance or a slender stalk; females of species of the giant water bug genera Abedus and Belostoma (Belostomatidae) lay eggs on the backs of males, where they are aerated and protected from pre­ dation (Yonke 1991). Larvae resemble adults in general body form, although they lack wings and reproductive structures, and live usually in the same aquatic habitats. Most larvae grow through five instars, usually with one generation each year, although some are multivoltine (Sanderson 1982). Surface‐dwelling and semi‐aquatic fami­ lies are usually most common in late summer, whereas Nepomorpha families are most ­frequent

8  Biodiversity of Aquatic Insects

in late fall. Respiration for Nepomorpha usually is by means of a transported air bubble that is replenished from time to time; a few species of Naucoridae and Aphelocheiridae respire with a plastron (permanent air film); all others are air breathers, including Nepidae and some Belosto­ matidae that access the air with respiratory siphons or straps (Sanderson 1982, Polhemus 2008). Most Heteroptera reduce predation with noxious excretions from abdominal (larvae) or thoracic (adults) scent glands, or use these sub­ stances to groom themselves, reducing microbial growth on their bodies (Kovac and Maschwitz 1989). All Hemiptera larvae and adults have sucking mouthparts; these are organized into a three‐ or four‐segmented beak for most Het­ eroptera (Corixidae are an exception) and are used primarily to feed on fluids of plants or ani­ mals. The forewings of adult Heteroptera are leathery basally and membranous apically, but many species are apterous as adults, and many other species have both macropterous and brachypterous forms. The habitats of the aquatic Heteroptera are highly variable among the fami­ lies and genera, but most often they involve emergent vegetation in shallow water. Other hab­ itats include the shores of surface freshwaters (many taxa), marine intertidal zones (some Saldidae), the surface of the open sea (genus Halobates in Gerridae), ocean beaches, estuaries, brackish and alkaline lentic habitats, high moun­ tain lakes, hot springs, roadside ditches, tempo­ rary pools, bogs, swamps, and running water of all types (Polhemus 2008). 8.1.9  Wasps (Hymenoptera)

Several families of wasps have representatives that are internal parasitoids of the eggs or larvae of other aquatic insects, with at least 10 such fam­ ilies in North America (Bennett et  al. 2008). Agriotypidae are external parasitoids of the pupae of Trichoptera (Elliott 1982). Spider wasps of the genus Anoplius (Pompilidae) capture and para­ lyze submerged spiders of the genus Dolomedes, carrying them one at a time to a nest in the bank, and laying an egg externally so that the resulting

wasp larva can feed on the spider (Evans and Yoshimoto 1962). 8.1.10  Hellgrammites and Alderflies (Megaloptera)

The larvae of Megaloptera are aquatic, whereas the eggs, pupae, and adults are terrestrial. Several hundreds of the tiny cylindrical eggs are laid in rows or layers in rounded or quadrangu­ lar masses on substrates above the water (Flint et al. 2008). Hatchlings drop to and through the water surface and swim to appropriate habitat (Brigham 1982a). Larvae live usually in rivers, permanent and temporary streams, spring seeps, ponds, or swamps, or in lakes near wave‐ washed shores, occurring in leaf litter, among coarse rubble, or in soft organic sediment. They are predators on a wide variety of macroinverte­ brates and require 1–5 years to complete devel­ opment, with larvae passing through up to 12 instars (Flint et al. 2008). They eventually crawl out of the water to fashion unlined pupation chambers in soil and litter near the larval habi­ tat, under rocks, and sometimes in soft, rotting shoreline logs or stumps or in dry stream beds (Brigham 1982a, Neunzig and Baker 1991). Adult mating and egg‐laying activity can be diurnal or nocturnal; apparently adults do not feed (Flint et al. 2008). 8.1.11  Nerve‐winged Insects (Neuroptera)

Most species of Neuroptera (or Planipennia) are terrestrial. However, the larvae of Nevrorthidae and Sisyridae are aquatic. Larvae of at least the European Neurorthus species of Nevrorthidae are eurythermic, living in creeks and small rivers with temperatures ranging from 2.0 to 23.8 °C; unlike Sisyridae, they pupate under water and apparently complete one life cycle each year (Zwick 1967, Malicky 1984). Larvae of the Sisyridae feed on freshwater sponges, with sty­ let‐like mouthparts that are a coaptation of their mandibles and maxillae. Eggs, pupae, and adults are terrestrial. Larval development is accom­ plished in three instars; Climacia areolaris (Hagen) produces as many as five generations

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each year (White 1976). Usually, a cluster of a few tiny eggs are deposited in crevices or depres­ sions on objects overhanging the water, such as the undersides of leaves in forks of leaf veins, and are covered by a tent of three or four layers of white, silken threads. Hatchlings drop through the water surface and swim in search of sponges, where they settle for the remainder of their development (Pennak 1978). They pierce the sponge cells and suck their contents without imbibing the dangerous silicate spicules, some­ times cyclically feeding for a few minutes then wandering for the next several minutes. Larvae camouflage themselves with pieces of sponge impaled on the sharp spines protruding from their bodies, and respire with gills folded beneath the abdomen. They eventually swim or crawl to shore and then walk as much as 15 m inland to pupate in a double‐layered silken cocoon in the shelter of a bark or rock crevice. After a few days, they emerge as adults, mate, and lay eggs for about two weeks, apparently sustained by pollen and nectar (Brigham 1982b). 8.1.12  Scorpionflies (Mecoptera)

The Nannochoristidae are the only scorpion­ flies with species that have aquatic larvae, which occur only in the Australasian and Neotropical regions. The long, slender, wireworm‐like lar­ vae live in mud and prey on larvae of midges (Diptera: Chironomidae) (Pilgrim 1972). 8.1.13  Beetles (Coleoptera)

The beetles evidently evolved into freshwater habitats several times, with freshwater species occurring globally in a wide range of lentic and lotic habitats or at the margins of these habitats; some beetles occur in marine intertidal situations (White and Roughley 2008). These independent evolutionary events in their various stages of tran­ sition to aquatic habitats have resulted in a variety of living strategies for the eggs, larvae, pupae, and adults. Truly aquatic forms generally have aquatic eggs, larvae, and adults, and terrestrial pupae (e.g., Elmidae). Some truly aquatic taxa have only aquatic eggs and larvae, with terrestrial pupae and

adults (e.g., Psephenidae). In others, only the adults are aquatic (e.g., Dryopidae, Hydraenidae). Feeding habits are variable, with larvae or adults of the same species sometimes differing in feed­ ing habits; predation, herbivory (either vascular plants or algae scraped from rocks), and detri­ tivory are common (White and Roughley 2008). Respiration by adults is generally by air bubble or plastron (permanent air film), whereas respira­ tion by larvae is generally transcuticular (with or without gills) or involves piercing plant tissues (Resh et al. 2008). Eggs are laid in various situa­ tions and hatch in 1–2 weeks. Development of larvae is usually accomplished with 3–8 instars in 6–8 months (White and Roughley 2008). Pupae usually develop in 2–3 weeks (White and Roughley 2008), although some overwinter (e.g., Chrysomelidae: Donacia) (P. Zwick, personal communication). Most beetles are univoltine in temperate regions (White and Roughley 2008), but can have more than one generation per year in tropical or subtropical climates. 8.1.14  Caddisflies (Trichoptera)

Essentially all caddisflies are aquatic. Their eggs, larvae, and pupae occur in a wide variety of freshwater habitats, and adults fly and rest in nearby terrestrial habitats. Most species are oviparous. Each distinctively shaped egg mass contains tens to hundreds of eggs, which are covered with a polysaccharide, spumalin, and the eggs are deposited on substrates suspended above the water or at the water’s edge, or are submerged under water after deposition by swimming or crawling females (Unzicker et al. 1982). Larvae typically develop through five instars, completing growth in two months to two years, with most life cycles univoltine (Wiggins 1996). First‐instar diapause has been reported for species in temporary pools (Wiggins 1973) and fifth‐instar aestivation for species in temporary streams (Wiggins 1996). Larval habits, habitats, and feeding strategies are strongly correlated with their architectural behavior, facilitated by use of labial silk (Mackay and Wiggins 1979). Five general architectural

8  Biodiversity of Aquatic Insects

strategies for case‐making or retreat‐making are recognized (Wiggins 2004). 1)  Rhyacophiloidea are free‐living, building a dome‐like shelter in the last instar for pupa­ tion, which occurs in an interior cocoon; 2)  Glossosomatidae build a portable dome‐like shelter precociously in all larval instars, transporting it much like a turtle wears its shell – the transverse ventral strap is removed and the resulting dome cemented with silk to a stone for pupation, which occurs in an interior cocoon; 3)  Hydroptilidae make, in only the last instar, a usually portable purse‐like depressed or compressed case with silk and often various mineral or plant inclusions  –  the case is attached to the substrate and the ends are sealed for pupation, which occurs in an inte­ rior cocoon; 4)  species of the suborder Integripalpia make a portable case that is essentially tubular, com­ posed of silk and mineral or plant ­material – the case is usually attached to the substrate and porous silken sieve plates seal the ends for pupation without a cocoon; 5)  species of the suborder Annulipalpia make a stationary retreat of silk that often has a filter­ ing function to remove suspended nutrient particles from the water – a separate dome‐ like shelter is constructed usually of mineral material for pupation, without a cocoon. Larval habits include swimming in the water column, burrowing in the substrate, or clinging, sprawling, or climbing on substrate surfaces (Wiggins and Currie 2008). Larvae of various species feed as shredding and piercing herbi­ vores, shredding and collecting detritivores, gougers of wood, filterers of food particles from the water column, grazers on substrate biofilm, predators, and parasitoids (Wells 1992, Wiggins and Currie 2008). After 2–3 weeks as a pupa, the insect typically uses large mandibles to cut through the shelter and any cocoon, and then swims to the water surface or crawls out of the water (Unzicker et al. 1982), where it emerges in less than a minute as

an adult and flies into the sheltering riparian vegetation. Adults live for a few days to three months (Unzicker et al. 1982), subsisting on nec­ tar and water obtained with imbibing mouth­ parts (Crichton 1957). They fly most readily in early evening after sunset, but some are noctur­ nal and others are diurnal (Unzicker et al. 1982). Mating is facilitated by pheromones (Wood and Resh 1984), by substrate vibrations (Ivanov and Rupprecht 1992), and by swarming dances (Solem 1984, Ivanov 1993). Sperm transfer is accomplished with male and female end‐to‐end, facing in opposite directions while standing on shoreside substrate (Ivanov and Rupprecht 1993). 8.1.15  Moths (Lepidoptera)

Most species of Lepidoptera are terrestrial her­ bivores. Many species feed on the emergent parts of plants that grow in the water. Most spe­ cies of the crambid subfamily Acentropinae are truly aquatic, with eggs, larvae, and pupae fully submerged in water. Some acentropine caterpil­ lars are herbivores of many freshwater plant species (Brigham and Herlong 1982), whereas others live under silk tents on rocks and scrape biofilm from the rock surfaces (Solis 2008). Caterpillars of other families may feed above the water on floating or emergent aquatic plants. 8.1.16  Flies (Diptera)

Most Diptera are aquatic in the broadest sense, requiring a humid environment for larval devel­ opment. Eggs, larvae, and pupae of the families of Diptera that develop only when submerged in wet environments have evolved into these habi­ tats at least 19 times independently (Wiegmann and Yeates 2015). These insects live in almost every type of aquatic habitat, including coastal marine and brackish waters and brine pools; shallow and deep lakes; ponds; thermal springs; natural seeps of crude petroleum and waste oil; alkaline lakes and ponds; marine beach zones; stagnant or temporary pools and puddles; water in bromeliads, pitcher plants, and artificial con­ tainers; and slow‐ to fast‐flowing streams and rivers (Courtney et al. 2008).

211

212

Insect Biodiversity: Science and Society

Much of human history has been affected by the role of flies in disease transmission, both in determining the outcomes of war and in retard­ ing economic development. Many of the carri­ ers of these disease agents develop in freshwater habitats, especially lakes, ponds, streams, and artificial containers with small amounts of water, such as discarded open cans and old tires. At the same time, in aquatic ecosystems, flies often have a key role in food webs, con­ suming large amounts of detritus and serving as the primary food source for other fresh­water organisms (Courtney and Merritt 2008). In freshwater habitats, larvae are planktonic in the water column, burrowers in the substrate,

or clingers or sprawlers on substrates (Courtney et al. 2008). Their feeding strategies are as diverse as those of caddisflies, including shredding living and dead plant tissue, gouging wood, filtering suspended food particles from the water column, collecting bits of food from the substrate, grazing on biofilms, and preying on or parasitizing other macroinvertebrates (Courtney et al. 2008).

8.2 ­Species Numbers Table 8.1 provides the number of species cur­ rently known for the various orders of aquatic

Table 8.1  Major orders (and Diptera families) of aquatic insects, with estimates of the known number of species. Taxon

Number of known species

Reference

Ephemeroptera

 3,436

M. Sartori, personal communication

Odonata

 5,956

Suhling et al. 2015

Plecoptera

 3,562

DeWalt et al. 2015

Aquatic Orthoptera

   190

Cover and Bogan 2015

Aquatic Blattodea

   40

Cover and Bogan 2015

Aquatic Heteroptera

 4,738

D. Polhemus, personal communication

Megaloptera

   350

Cover and Bogan 2015

Aquatic Neuroptera

   128

Cover and Bogan 2015

Aquatic Mecoptera

     8

Ferrington 2008

Aquatic Coleoptera

16,604

Jäch and Balke 2008

Aquatic Hymenoptera

   150

Bennett 2008

Trichoptera

15,042

Morse 2015

Aquatic Lepidoptera

   740

Mey and Speidel 2008

Diptera:

51,197

—

‐ Ceratopogonidae

 5,902

Courtney et al., this volume

‐ Chaoboridae

    89

Courtney et al., this volume

‐ Chironomidae

 7,290

Courtney et al., this volume

‐ Corethrellidae

   111

Courtney et al., this volume

‐ Culicidae

 3,725

Courtney et al., this volume

‐ Dixidae

   197

Courtney et al., this volume

‐ Simuliidae

 2,177

Adler and Crosskey 2015

‐ Thaumaleidae

   183

Courtney et al., this volume

8  Biodiversity of Aquatic Insects

Table 8.1  (Continued) Taxon

‐ Ptychopteridae ‐ Tanyderidae ‐ Blephariceridae ‐ Deuterophlebiidae

Number of known species

Reference

80

Courtney et al., this volume

40

Courtney et al., this volume

330

Courtney et al., this volume

14

Courtney et al., this volume

‐ Nymphomyiidae

8

Courtney et al., this volume

‐ Axymyiidae

9

Courtney et al., this volume

‐ Aquatic Scatopsidae

5

Haenni in Wagner et al. 2008

1,988

Wagner in Wagner et al. 2008

‐ Aquatic Psychodidae ‐ Tipuloidea

15,770

Courtney et al., this volume

‐ Aquatic Stratiomyidae

928

Woodley 2011

‐ Athericidae

133

Courtney et al., this volume

‐ Oreoleptidae

1

Courtney et al., this volume

49

Courtney et al., this volume

‐ Tabanidae

4,434

Courtney et al., this volume

‐ Dolichopodidae

3,182

R. L. Hurley, personal communication

‐ Pelecorhynchidae

‐ Empididae ‐ Lonchopteridae ‐ Aquatic Phoridae ‐ Aquatic Syrphidae ‐ Coelopidae ‐ Aquatic Dryomyzidae ‐ Aquatic Sciomyzidae ‐ Heterocheilidae ‐ Canacidae ‐ Heleomyzidae ‐ Ephydridae ‐ Aquatic Muscidae Total

671 2 17 1,341 35 3 194 2 323 12

Sinclair in Wagner et al. 2008 Bartak in Wagner et al. 2008 Disney 2004 Rotheray in Wagner et al. 2008 Courtney et al., this volume W. Mathis, personal communication Vala et al., 2013 W. Mathis, personal communication Courtney et al., this volume W. Mathis, personal communication

1,251

Zatwarnicki in Wagner et al. 2008

701

A. Pont, personal communication

102,141

insects. In some cases, no more than about 20% of the species are currently known to science, with a substantial majority yet to be discovered. Geographically, the tropical and subtropical regions include most of the as‐yet‐unknown spe­ cies of aquatic insects. Schmid (1984), for exam­ ple, estimated that 50,000 species of ­caddisflies occur in the world (of which only 30% are

—

c­ urrently described), with 40,000 of those spe­ cies occurring in the tropics and subtropics of southern Asia. The density of caddisfly species in the Oriental region is about twice that of the next‐most‐densely speciose region (Neotropical) (Morse 1997), and species discovery continues in the Oriental region (e.g., Yang and Morse 2000) without any sign of waning.

213

214

Insect Biodiversity: Science and Society

8.3 ­Societal Benefits and Risks The benefits and risks of aquatic insect biodi­ versity cannot be appreciated unless that biodi­ versity is known. Many species of aquatic insects remain unknown to science, and many that have been collected have yet to be described. Species accumulation curves suggest that we have not yet approached an asymptote, so many addi­ tional, as‐yet‐unknown species remain to be collected, especially in tropical and subtropical waterways (Morse 2002). In biomonitoring programs to assess water quality, one of the major impediments is a lack of ability to identify larvae at the species level. Larvae are most commonly collected in stream assessments, but the taxonomy of most groups began with the adults, often with just one gen­ der. For this reason, larvae are poorly known, with no more than about 50% of the species rec­ ognizable as larvae in regions where most spe­ cies are otherwise known to science, and often less than 5% of the species are recognizable as larvae in regions where species are less well known (Morse 2002). When trying to find herbivores that can con­ trol invasive aquatic weeds, the countries from which the weeds originally came often must be explored. In many such searches, herbivores are found that could serve this purpose, but they are often undescribed species. Description and naming is usually the first step toward discover­ ing the bionomics of a species, its potential hosts, and environmental requirements  –  data that are necessary before deciding whether to import the species into a non‐native country. Similarly, medically important species, espe­ cially in tropical regions, often are poorly known to science. To learn the biology of these vectors of disease agents sufficiently to devise appropri­ ate control measures, their diversity and identi­ ties must be discovered. At least three additional reasons for discover­ ing biodiversity in aquatic insects pertain to widespread human values, including (i) our nat­ ural affiliation with the diversity of living things,

(ii) our moral obligations to protect species, and (iii) our innate curiosity about our amazingly diverse natural world (Kellert 1996). With respect to the first of these values, Wilson (1984) in his Pulitzer‐Prize‐winning treatise on “Biophilia” argued that we have a natural affilia­ tion with the diversity of living things, reflecting our evolutionary origins surrounded by them. Many people feel an intense reverence and sense of peace when immersed in a natural setting with high species diversity and abundance (Fuller et al. 2007). Many people also recognize a moral obligation, generally derived from their religious traditions, to be good stewards of bio­ logical diversity. Such people are convinced that “all creatures great and small” are innately deserving of protection from harm or extinction (Hamilton and Takeuchi 1991, Berry 2000, Lodge and Hamlin 2006). From both of these perspectives, discovery of biodiversity is implicit because appreciation and stewardship of biodi­ versity require knowledge of it. The third of these values lies in the need to satisfy our inborn curiosity about the world around us, including the species inhabiting it, with all of their won­ derful and amazing shapes and colors and behaviors and functions. A drive to learn as much as possible about the other species with which we share our planet is as fundamental to who we are as humans as any of our other innate characteristics. A high diversity of aquatic insect species is of value to people for a variety of other reasons, but four are particularly important, including the role of insects in food webs, in biomonitoring, in fishing, and in control of noxious weeds. A few species of aquatic insects pose some risks, as well. 8.3.1  Societal Benefits of Aquatic Insect Diversity in Food Webs

In food webs, aquatic insects capture, use, and make available to other freshwater organisms nutrients that otherwise would be unavailable. In general, they do this by processing nutri­ ents  from coarse particulate organic matter

8  Biodiversity of Aquatic Insects

(CPOM, > 0  μ3) and from fine particulate organic ­matter (FPOM,  500 base pairs of the cytochrome oxidase subunit I gene (COI)) in the Barcode of Life Data System (BOLD: http://www.boldsystems.org) from 1613 to 6905. The barcoding diversity and coverage were examined using the barcoding index number (BIN) system in BOLD detailed by Ratnasingham and Hebert (2013). BINs can approximate spe­ cies diversity well, but are discordant with cur­ rent taxonomy in roughly 10% of cases (Ratnasingham and Hebert 2013). According to Ratnasingham and Hebert (2013), these limita­ tions are due to four main factors: taxonomic error, sequence contamination, problems with the BIN calculation methodology, and lack of COI‐sequence variation due to introgression or their evolutionarily young age. In our observa­ tions, misidentification of specimens is also a confounding factor when working with the BOLD data, as samples come from multiple sources and are not all identified by experts. For this study, barcodes were only considered if they

met the 500 base‐pair threshold for quality, fol­ lowing Ratnasingham and Hebert (2013). The barcoding coverage for the beetles of Canada and North America is summarized in Table 11.4, Fig. 11.3, and Fig. 11.4. The number of BINs divided by the number of known spe­ cies approximates barcoding coverage well, with a few caveats. First, the number of known spe­ cies is only an approximation for most North American families, as there are still many gaps in basic taxonomic knowledge of these groups. The number of known species is less than the actual number of species for most families because many North American families have not undergone thorough taxonomic revisions and many beetle species remain undescribed. In addition, the number of BINs contains a degree of error for the reasons mentioned above, and overestimates or underestimates the actual number of species sampled roughly 10% of the time. Beyond this, barcoding sampling of North American beetles is still in its early stages and lacks coverage of much of the observed varia­ tion in described species. Our results show that 49.7% of described Canadian beetle species and 27.4% of North American beetle species have been barcoded in BOLD. The percentage is significantly higher for Canada, reflecting the specific efforts there and the lower diversity at northern latitudes. Our general observations of the coverage are what one might expect: easily collected taxa (abundant, easily observed, and with a wide dis­ tribution) are well represented, whereas diffi­ cult to collect taxa (rare, cryptic habits, and with limited distribution) are poorly repre­ sented. The former is exemplified by the Silphidae and Geotrupidae (76.7% and 78.6% North American coverage, respectively), as these families are relatively well known and have low diversity in North America, and most spe­ cies are fairly widespread, readily observed and collected, and easily attracted to traps. The lat­ ter is exemplified by the Histeridae and Ripiphoridae (3.9% and 5.9% North American coverage, respectively), as these families are also reasonably well known taxonomically but have

—

Sphaeriusoidea

—

Hydrophiloidea

Archostemata

Myxophaga

Adephaga

Polyphaga

Scarabaeoidea

Staphylinoidea

Superfamily

Suborder

4

4,370

Staphylinidae

Passalidae

30

Silphidae 27

324

Leiodidae

28

11

Agyrtidae

Pleocomidae

117

Ptiliidae

Geotrupidae

67

Hydraenidae

435

513

Dytiscidae

Histeridae

3

Amphizoidae 258

14

Noteridae

1

67

Haliplidae

Hydrophilidae

2,402

Carabidae

Sphaeritidae

4 8

Trachypachidae Rhysodidae

56

Gyrinidae

1 3

Hydroscaphidae Sphaeriusidae

4 1

Cupedidae

1

22

0

939

23

87

2

30

5

17

0

124

196

2

1

15

929

3

2

33

1

0

1

4

North America North species America BINs

Micromalthidae

Family

25.00

78.57

0.00

21.49

76.67

26.85

18.18

25.64

7.46

3.91

0.00

48.06

38.21

66.67

7.14

22.39

38.68

37.5

50.00

58.93

33.33

0.00

100.00

100.00

North America percentage coverage

1

12

0

1,682

26

182

8

49

27

136

1

151

284

3

2

34

989

2

2

34

0

0

1

3

Canada species

0

8

0

736

18

71

1

29

4

8

0

79

162

2

1

10

581

1

2

25

0

0

0

3

Canada BINs

(Continued)

0.00

66.67

0.00

43.76

69.23

39.01

12.50

59.18

14.81

5.88

0.00

52.32

57.04

66.67

50.00

29.41

58.75

50.00

100.00

73.53

0.00

0.00

0.00

100.00

Canada percentage coverage

Table 11.4  Estimated number of Coleoptera species for North America and Canada, with the associated number of DNA‐barcoding BINs and the calculated percent regional barcoding coverage.

Suborder

Byrrhoidea

Buprestoidea

Dascilloidea

Scirtoidea

Superfamily

Table 11.4  (Continued)

3 28 34 16 19 1 1

Heteroceridae Psephenidae Ptilodactylidae Chelonariidae Eulichadidae

13

Dryopidae Limnichidae

99

Elmidae Lutrochidae

35

762

Buprestidae Byrrhidae

7

Schizopodidae

5 5

50

Scirtidae Rhipiceridae

12

Clambidae Dascillidae

11

1,700

Scarabaeidae Eucinetidae

5 8

Hybosoridae

35

Ochodaeidae Glaphyridae

3 26

Lucanidae

Glaresidae Diphyllostomatidae

43 25

Trogidae

0

0

10

6

16

0

0

0

25

21

171

0

1

0

34

3

6

586

1

4

6

10

0

4

11

North America North species America BINs

Family

0.00

0.00

52.63

37.50

47.06

0.00

0.00

0.00

25.25

60.00

22.44

0.00

20.00

0.00

68.00

25.00

54.55

34.47

12.50

80.00

17.14

38.46

0.00

16.00

25.58

North America percentage coverage

0

0

4

4

28

3

1

6

32

26

177

0

1

0

25

7

7

221

1

1

4

14

0

2

15

Canada species

0

0

6

2

8

0

0

0

7

18

91

0

0

0

31

3

6

143

0

1

1

8

0

0

4

Canada BINs

0.00

0.00

150.00

50.00

28.57

0.00

0.00

0.00

21.88

69.23

51.41

0.00

0.00

0.00

124.00

42.86

85.71

64.71

0.00

100.00

25.00

57.14

0.00

0.00

26.67

Canada percentage coverage

Suborder

471

Ptinidae

Cucujoidea

2 9 3 82 55

Biphyllidae Erotylidae Monotomidae

Melyridae Sphindidae

520

Cleridae Byturidae

59 243

Trogossitidae

Cleroidea

75

Bostrichidae 2

2

Endecatomidae

Lymexylidae

117

1

Jacobsoniidae Dermestidae

4

Nosodendridae

473

Cantharidae 9

10

Omethidae Derodontidae

124

Lampyridae

0

3 23

Telegeusidae Phengodidae

37

76

Lycidae

21

11

28

0

5

1

85

44

11

1

48

20

0

29

0

0

5

116

0

48

9

436

20 965

17

0

Throscidae

Eucnemidae

0

8

Elateridae

2 85

Cerophytidae

8 1

Artematopodidae Brachypsectridae

1

Callirhipidae

0

North America North species America BINs

Family

Lymexyloidea

Bostrichoidea

Derodontoidea

Elateroidea

Superfamily

20.00

34.15

0.00

55.56

50.00

16.35

18.11

18.64

50.00

10.19

26.67

0.00

24.79

0.00

0.00

55.56

24.52

0.00

38.71

39.13

0.00

48.68

45.18

105.00

20.00

0.00

0.00

100.00

0.00

North America percentage coverage

27

28

1

6

1

53

52

22

1

98

24

1

49

0

2

8

154

0

32

1

0

29

386

8

38

0

0

5

0

Canada species

8

14

0

4

1

23

22

2

1

31

7

0

24

0

0

4

92

0

24

2

0

24

238

17

14

0

0

5

0

Canada BINs

(Continued)

29.63

50.00

0.00

66.67

100.00

43.40

42.31

9.09

100.00

31.63

29.17

0.00

48.98

0.00

0.00

50.00

59.74

0.00

75.00

200.00

0.00

82.76

61.66

212.50

36.84

0.00

0.00

100.00

0.00

Canada percentage coverage

Suborder

Tenebrionoidea

Superfamily

Table 11.4  (Continued)

51 36 1,184

Tenebrionidae

140

Latridiidae

Zopheridae

61

Corylophidae

Ripiphoridae

481

Coccinellidae

189

45

Endomychidae

Mordellidae

19

Cerylonidae

50

18

Bothrideridae

26

2

Smicripidae

Melandryidae

173

Nitidulidae

Tetratomidae

11

Kateretidae

84

52

Laemophloeidae

1

122

Phalacridae

Ciidae

3

Passandridae

Archeocrypticidae

8

Cucujidae

26

32

Silvanidae

Mycetophagidae

145

Cryptophagidae

350

11

3

96

27

7

15

0

11

67

13

147

8

3

0

0

72

4

5

14

0

5

6

50

North America North species America BINs

Family

29.56

30.56

5.88

50.79

54.00

26.92

17.86

0.00

42.31

47.86

21.31

30.56

17.78

15.79

0.00

0.00

41.62

36.36

9.62

11.48

0.00

62.50

18.75

34.48

North America percentage coverage

141

19

11

75

43

20

29

0

16

64

16

161

16

8

4

0

101

8

13

8

1

8

16

73

Canada species

69

4

2

59

26

6

10

0

8

58

13

109

6

3

0

0

57

3

3

10

0

5

5

46

Canada BINs

48.94

21.05

18.18

78.67

60.47

30.00

34.48

0.00

50.00

90.63

81.25

67.70

37.50

37.50

0.00

0.00

56.44

37.50

23.08

125.00

0.00

62.50

31.25

63.01

Canada percentage coverage

12 2 7 50 20 229 48 49

Mycteridae Boridae Pythidae Pyrochroidae Salpingidae Anthicidae Aderidae

Curculionoidea 2 51 152 84 41 2,794

Belidae Attelabidae Brentidae Dryophthoridae Brachyceridae Curculionidae

25,106

15 88

1,869

Chrysomelidae Nemonychidae

4

Orsodacnidae

Anthribidae

9

Megalopodidae

Chrysomeloidea Cerambycidae

6,894

474

25

17

87

25

0

22

8

487

1

3

301

61

5

13

7

1

1

55

6

6

27.46

16.96

60.98

20.24

57.24

49.02

0.00

25.00

53.33

26.06

25.00

33.33

31.42

79.59

4.17

26.64

25.00

26.00

100.00

50.00

8.33

12.97

6.90

60.00

100.00

0.00

8,237

823

19

27

49

14

0

20

8

598

1

7

368

22

10

65

15

22

6

2

4

47

13

9

2

1

4,096

274

11

7

50

13

0

13

6

266

1

3

198

36

1

27

4

13

6

1

1

25

4

5

2

0

49.73

33.29

57.89

25.93

102.04

92.86

0.00

65.00

75.00

44.48

100.00

42.86

53.80

163.64

10.00

41.54

26.67

59.09

100.00

50.00

25.00

53.19

30.77

55.56

100.00

0.00

Numbers originate from Arnett and Thomas (2000), Arnett et al. (2002), and Marske and Ivie (2003) for North American species; Bousquet et al. (2013) for Canadian species; and the Barcode of Life Data System (BOLD: http://www.boldsystems.org) for North American and Canadian barcoding index numbers (BINs).

Total

39

424

Meloidae

958

87

Oedemeridae

Scraptiidae

2

10

Stenotrachelidae

2

2

Synchroidae

0

1

Prostomidae

388

Insect Biodiversity: Science and Society 0

50

100

150

200 Throscidae Phengodidae Scraptiidae

Ptilodactylidae Phalacridae, Scirtidae Brentidae Pythidae, Artematopodidae, Cupedidae, Trachypachidae, Synchroidae, Orsodacnidae, Byturidae, Lymexylidae, Hybosoridae, Attelabidae, Latridiidae Eucinetidae, Lycidae, Corylophidae Mordellidae, Lampyridae, Nemonychidae, Gyrinidae Silphidae, Coccinellidae, Geotrupidae, Sphindidae, Amphizoidae, Anthribidae, Scarabaeidae, Cryptophagidae, Cucujidae, Elateridae, Melandryidae Cantharidae, Ptiliidae, Pyrochroidae, Carabidae, Brachyceridae, Lucanidae, Dytiscidae, Nitidulidae, Stenotrachelidae, Cerambycidae, Meloidae, Hydrophilidae, Buprestidae

Erotylidae, Mycetophagidae, Derodontidae, Psephenidae, Noteridae, Rhysodidae, Boridae, Dermestidae, Tenebrionidae, Chrysomelidae, Staphylinidae, Melyridae, Clambidae, Megalopodidae, Cleridae, Anthicidae Leiodidae, Endomychidae, Cerylonidae, Kateretidae, Eucnemidae, Ciidae, Curculionidae, Ptinidae, Silvanidae, Oedemeridae Tetratomidae, Monotomidae, Haliplidae, Bostrichidae, Heteroceridae, Salpingidae, Trogidae, Dryophthoridae, Mycteridae, Ochodaeidae, Laemophloeidae, Elmidae, Zopheridae Ripiphoridae, Hydraenidae, Agyrtidae Aderidae, Trogossitidae, Histeridae Dryopidae, Bothrideridae, Limnichidae, Nosodendridae,Ischaliidae, Glaresidae, Lutrochidae, Biphyllidae, Passandridae, Endecatomidae, Prostomidae, Sphaeritidae, Glaphyridae, Rhipiceridae, Passalidae, Micromalthidae

Figure 11.3  Percentage (aggregated in 10% increments) of Canadian Coleoptera species included in the Barcode of Life Data System (BOLD: http://www.boldsystems.org). Percentage coverage is the number of barcoding index numbers (BINs) for a family divided by the number of known species (from Table 11.4). Percentage coverage values of more than 100% indicate poorly known groups in need of further taxonomic and survey research.

11  Biodiversity of Coleoptera 0

50

25

100

75

Throscidae Artematopodidae, Pythidae, Cupedidae, Synchroidae, Micromalthidae Scraptiidae

Geotrupidae, Silphidae, Hybosoridae Scirtidae, Amphizoidae Cucujidae, Brachyceridae Gyrinidae, Derodontidae, Sphindidae, Brentidae, Byrrhidae, Stenotrachelidae Ptilodactylidae, Nemonychidae, Melandryidae, Eucinetidae, Mordellidae Latridiidae, Hydrophilidae, Lycidae, Attelabidae, Elateridae, Heteroceridae, Trachypachidae, Boridae, Byturidae, Lymexylidae Nitidulidae, Mycetophagidae Psephenidae, Rhysodidae, Dytiscidae, Lucanidae, Carabidae, Lampyridae, Phengodidae, Kateretidae

Megalopodidae, Sphaeriusidae, Erotylidae, Scarabaeidae, Cryptophagidae, Zopheridae, Coccinellidae, Cerambycidae Tenebrionidae, Elmidae, Trogidae, Ptiliidae, Pyrochroidae, Chrysomelidae, Anthicidae, Bostrichidae, Leiodidae, Tetratomidae Cantharidae, Dermestidae, Dryophthoridae, Corylophidae, Staphylinidae, Haliplidae, Buprestidae, Anthribidae, Salpingidae, Clambidae, Orsodacnidae, Passalidae Endomychidae, Ciidae, Cleridae, Agyrtidae, Trogossitidae, Silvanidae, Cerylonidae, Glaresidae, Melyridae, Curculionidae, Ochodaeidae, Eucnemidae, Monotomidae, Rhipiceridae Glaphyridae, Meloidae, Ptinidae, Phalacridae Mycteridae, Laemophloeidae, Ripiphoridae, Oedemeridae, Noteridae, Hydraenidae

Histeridae, Aderidae Limnichidae, Pleocomidae, Bothrideridae, Dryopidae, Omethidae, Schizopodidae, Dascillidae, Nosodendridae, Lutrochidae, Biphyllidae, Diphyllostomatidae, Ischaliidae, Passandridae, Telegeusidae, Belidae, Cerophytidae, Endecatomidae, Smicripidae, Archeocrypticidae, Brachypsectridae, Callirhipidae, Chelonariidae, Eulichadidae, Hydroscaphidae, Prostomidae, Sphaeritidae, Jacobsoniidae

Figure 11.4  Percentage (aggregated in 5% increments) of North American Coleoptera species included in the Barcode of Life Data System (BOLD: http://www.boldsystems.org). Percentage coverage is the number of barcoding index numbers (BINs) for a family divided by the number of known species (from Table 11.4). Percentage coverage values of more than 100% indicate poorly known groups in need of further taxonomic and survey research.

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many species with cryptic habits; they either burrow in substrates or are myrmecophiles (Histeridae), termitophiles (Histeridae), or par­ asitoids (Ripiphoridae). As such, many species in these families have short activity periods as adults and are difficult to collect without taxon‐ specific techniques. Other examples of taxa with no barcode coverage are the families Pleocomidae and Diphyllostomatidae, both of which are endemic to the West Coast of North America, with small distributions, and are not generally found unless collectors specifically seek them. Of the 129 North American beetle families, 27 (21%) are not yet represented with high‐quality barcoding data in BOLD, but most of these families are known only from one to three species with restricted distributions. For the Canadian fauna, there was an early initiative from 2006 to 2010 to do a barcode inventory of the beetles of Churchill, Manitoba (Woodcock et al. 2013). The resulting data set was augmented by the Biodiversity Institute of Ontario through intensive sampling around Guelph, Ontario, Canada, and additional sam­ pling mainly in national parks across Canada. In 2011, a joint effort between the Biodiversity Institute of Ontario and the CNC was initiated to barcode Canadian beetle taxa using pinned specimens in the collection. A first run through all taxa was completed in 2014, with additional sampling still ongoing. The results of these combined efforts yielded 50% barcoding cover­ age of Canadian beetle species. This level of coverage is higher than for all of North America to the point where most common or widespread species are represented by barcodes. Barcode coverage of 50% of described species or more has been achieved for 57 of the 112 families of Canadian beetles, including diverse families such as the Carabidae, Cerambycidae, and Elateridae. Significant gaps in coverage remain for three of the most diverse families: Chrysomelidae, Curculionidae, and Staphylinidae, which have less than 50% bar­ code coverage for Canadian species. The gaps in coverage could be efficiently addressed by tar­ geting these groups for future work.

Some families are so poorly known that general barcode efforts have already found many more BINs than the number of described species. This is so for the families Scirtidae, Scraptiidae, and Throscidae, which have 105.0%, 84.8%, and 68.0% barcoding coverage for North America and 212.5%, 180.0%, and 124.0% for Canada. It is obvi­ ous from examining the barcoding data that many more species are present in the focal regions than are indicated by the number of described species. These families and others are fertile ground for taxonomists, and highlight the poor state of tax­ onomy in the backyards of some of the top ento­ mology museum collections in the world. Two North American genera, Phyllophaga and Serica (Scarabaeidae: Melolonthinae), were examined for BIN discordance. They were selected because of their high diversity (212 and 100 North American species, respectively; Evans and Smith 2009), with low variation in external morphology. These two factors make these gen­ era likely to have poor COI lineage sorting between species because their similar morphol­ ogies suggest that their diversity is a result of a recent speciation explosion. The identification of species in these genera can be accurate using the highly diagnostic genitalic characters. Among BOLD specimens, 16 of the 143 Phyllophaga BINs and four of the 36 Serica BINs were tagged as discordant, with more than one species based on morphology included (both approximately 11%). This percentage is in line with the findings of Ratnasingham and Hebert (2013) and probably represents the high end of expected BIN discordance error for a group with high recent speciation and poor lineage sorting (whereby descendants of an ancestor species inherit different subsets of variants of the ances­ tral mitochondrial genome). A good case study for Coleoptera would be to determine whether this percentage changes when more species and more specimens within species are sampled. DNA Barcoding Detects New Invasive Species Any

inventory work can detect new taxa for a focal region, including new species, range exten­ sions, or invasive species. Our analysis of the

11  Biodiversity of Coleoptera

barcoding data for North American Coleoptera detected a new invasive species in Canada. Anthribus nebulosus (Anthribidae) is a preda­ tor of scale insects (Hemiptera: Sternorrhyncha), that was intentionally introduced to Virginia, United States, in 1978–79. It is thought to have been introduced elsewhere in North America because of its disjunct distribution (Hoebeke and Wheeler 1991). This Eurasian species also has been recorded from southern New England (Hoebeke and Wheeler 1991) and adjacent regions of Pennsylvania and New Jersey (http:// bugguide.net/node/view/278376/data). The bar­ coding records from in and around Guelph, Ontario, Canada, were unexpected because this species had not been observed to spread rap­ idly  and was not first detected in Canada near known localities in the United States. It is unclear whether this disjunct distributional record is a  result of a local introduction or an unde­ tected  general expansion of the species range. Specimens of A. nebulosus were collected in and near Guelph in three separate collecting events  and barcoded as part of general survey and inventory efforts. The barcoding data were  included in overall Coleoptera and Curculionoidea analyses and were a match within a BIN including identified specimens from Germany. Robert Anderson (Canadian Museum of Nature, Ottawa, Ontario, Canada) confirmed the identification of Guelph speci­ mens. Additional specimens from Ontario in the same BIN were collected in Rouge River National Urban Park and on Beausoleil Island (collectively new country and provincial records). A false‐positive record for an invasive species resulted from a BIN from the root weevil genus Polydrusus (Curculionidae: Entiminae), which is widespread globally. Four native and three invasive species are known from North America (Anderson 2002). Specimens from Point Pelee, Guelph, and Rouge River, Ontario, Canada, were collected as part of a general survey to build the barcode library. Our analysis of bar­ coding data revealed that these specimens shared a BIN with German specimens identi­ fied as Polydrusus corruscus. This is a Eurasian

willow‐feeding species (Salix), not previously known from North America. The Ontario specimens deposited in the Biodiversity Institute of Ontario were examined and identi­ fied as Polydrusus impressifrons, an invasive species previously recorded from North America. The error seems to have originated from misidentified German specimens. This case shows the need to verify identifications of specimens in BOLD before using its results to infer new records of invasive species or other discoveries. DNA Barcoding Reexamines Species Limits of Holarctic Taxa  Species with a Holarctic distribution are

fairly common. Depending on their range and dispersal histories, Nearctic and Palearctic pop­ ulations of apparent Holarctic species might have been isolated long enough for lineage sort­ ing to occur in fast‐evolving gene regions and for the two populations to diverge enough to be considered separate species. Barcoding can be a rapid way to test for such cryptic species. When the Palearctic and Nearctic specimens are sorted to separate BINs, these species should be studied further to determine whether they are different species, using an integrative taxonomic approach. If the barcoding results are supported by morphological, host plant, behavioral, or other characters, then broad‐based support has been achieved and the two species should be considered distinct and valid. The barcoding survey and inventory work in North America and Eurasia has examined numerous Holarctic beetle species. Barcoding has detected two separate BINs (one North American and the other Eurasian) for some spe­ cies that were formerly considered Holarctic. Species in this category include Ampedus nigrinus (Elateridae), Dictyoptera aurora (Lycidae), Grypus equiseti (Brachyceridae), Tournotaris bimaculata (Brachyceridae), and Dryocoetes autographus (Curculionidae: Scolytinae). These species should be further investigated to deter­ mine whether other data sets support splitting them into separate North American and Eurasian species.

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Looking at one specific example, Wood (1982) commented that with D. autographus, “The American specimens tend to have the frons more sparsely granulate, the strial punctures slightly larger and not as deep, and the elytral declivity slightly more convex than the European material. The differences are slight, variable, and not suitable for statistical analysis; there­ fore, I prefer to follow Bright (1963) and recog­ nize only one species.” These recognized morphological differences coupled with the barcoding results suggest a possible basis for considering the Palearctic and Nearctic popula­ tions as two separate species. Also detected were two examples of species with three different BINs for populations in Eurasia, Alaska, and Canada: Berninelsonius hyperboreus (Elateridae) and Eutrichapion viciae (Brentidae). These examples could indi­ cate multiple cryptic species, or perhaps a slow postglacial range expansion with subsequent population isolation and DNA lineage sorting. More evidence is required to determine the number of species present. Adventive beetle species in North America also were analyzed, and some had separate BINs for their North American and Eurasian popula­ tions. These species include Brachypterus urticae (Kateretidae), Anthocomus equestris (Melyridae), Ischnopterapion loti (Brentidae), and Tanysphyrus lemnae (Brachyceridae). More research is needed to explain these genetic dis­ tinctions. Possible explanations include misi­ dentifications (as described for Polydrusus), and the possibility that the source populations include multiple cryptic species (e.g., Rhyssemus and Aphodius (Scarabaeidae). It is also possible that the adventive population originated from a source population with an as‐yet‐undetected haplotype (i.e., BIN). DNA Barcoding is Part of the Integrative Taxonomic Approach to Delimiting Species  Barcoding and

DNA sequence analysis have become a key component of the integrative taxonomic approach to delimiting species. One example is the recent recognition of the scarabs Rhyssemus

germanus and Rhyssemus puncticollis as ­separate species, both occurring in Europe and the latter also occurring in North America. Rhyssemus germanus was described from Germany, and Brown described R. puncticollis much later from Canada. In his description of R. puncticollis, Brown (1929) did not mention R. germanus or any other Palearctic species, imply­ ing that this species was endemic to the Nearctic region. Brown (1950) later synonymized his own species under R. germanus, stating that “this species has not been reported previously from America under the name germanus, but comparison of the types of puncticollis with European specimens shows the names to be synonymous.” The assumption that R. germanus was an invasive species to North America, with R. puncticollis as a synonym, was supported by Gordon and Cartwright (1980) and others until recently. Rößner (2012) and Kral and Rakovič (2012) recognized consistent morphological differ­ ences between R. germanus and R. puncticollis and revalidated the latter as a valid species, which they record from Germany and the Czech Republic. Barcoding data corroborate the reval­ idation of R. puncticollis, showing separate BINs for R. germanus (German specimens) and R. puncticollis (German and Ontario specimens). Independent confirmation robustly supports the hypothesis of two separate and valid species. This new evidence allows researchers to assess whether the true R. germanus occurs in North America and whether R. puncticollis is actually invasive to North America. Four synonyms based on European specimens need to be reex­ amined to determine whether they apply to R. germanus or R. puncticollis. Another case involves the cryptic dung‐feed­ ing scarab species Aphodius fimetarius and Aphodius pedellus. Until recently, these two species were together named A. fimetarius, thought to be native to Europe and invasive to North America. Wilson (2001) found two chro­ mosomal karyotypes in the specimens from Europe and presented subtle morphological characters to support the hypothesis of two

11  Biodiversity of Coleoptera

cryptic species. This work was supported and expanded by Miraldo et al. (2014), who included specimens from across the entire range, exam­ ined COI mtDNA data, and made an in‐depth morphological analysis along with the karyo­ typic analysis. Barcoding data from BOLD corroborate the findings of Miraldo et al. (2014), with two clear BINs for A. fimetarius from Europe and California and A. pedellus from Europe and Canada. Aphodius fimetarius and A. pedellus are now understood to be cryptic species; both species occur in Europe and North America and both may be invasive to North America. This example highlights how integrative taxonomy and barcoding can reveal cryptic species among common, widespread taxa. DNA Barcoding Identifies Taxonomic Gaps in Groups with Underestimated Biodiversity  The families

Scirtidae, Scraptiidae, and Throscidae were iden­ tified above as groups where barcoding exposed much hidden species richness. At the generic level, a few spectacular examples are Ptiliolum (Ptiliidae), Cyphon (Scirtidae), Trixagus (Throscidae), and Anaspis (Scraptiidae). Ptiliolum is known from five ­species in Canada (Bousquet et  al. 2013), but pre‐barcoding estimates found “numerous undescribed species occurring in northern and western United States and Canada” (Hall 2000). We found five BINs of Ptiliolum from Alberta and Saskatchewan, Canada, although only one species is known from Alberta and none from Saskatchewan (Bousquet et  al. 2013). As Hall (2000) indicated, this genus requires taxo­ nomic study because there are many undescribed North American species. The genus Cyphon is also in need of taxo­ nomic revision. Young (2002) commented that the genitalic characters are diagnostic but that the external morphology is homogenous among species so that every specimen requires dissec­ tion to confirm identifications. This situation has probably led to the poor taxonomy of this group. The barcoding data yield 21 BINs from North America, and Young (2002) mentions 27 described species. The geographic distribution

of the described species disagrees with that of the BINs, and there are many more BINs than there are described species in Canada, indicat­ ing many undescribed North American species. The genus Trixagus was last revised by Yensen (1975) and has six known species in North America, according to Johnson (2002), who cautioned that “this family is in need of general study at all levels.” Using the barcoding data, we found 13 clear North American Trixagus BINs. This genus is at least twice as diverse in North America as the taxonomic literature indicates. Because most of the barcoding samples were taken from Canada, we can anticipate more undetected BINs and species in the generally more diverse United States. Yensen (1975) com­ mented that there was much variation in his species definitions, suggesting several cryptic species, as do the barcoding data. The North American Throscidae need a complete taxo­ nomic overhaul. Even with the moderate and general focus of the barcoding to date, the num­ ber of North American throscid BINs in BOLD already exceeds the number of known species. This family would be an excellent focal taxon for any taxonomist interested in describing many new North American species. Anaspis has 13 known North American spe­ cies but has never undergone a taxonomic revi­ sion, and authors have disagreed on whether the genus should be divided into four genera (Pollock 2002). Our barcoding data have recov­ ered 13 BINs from North America, but few specimens from these BINs match any of the described species; they also differ in distribu­ tion from the described species. Thus, several North American species in this genus remain undescribed. Overall, building the barcode library for North American Coleoptera has reached a point where the data are useful in many ways. Most common or widespread species have been barcoded, so clear matches are likely for any new, unidentified specimens compared with BOLD. The barcoding data also help users detect invasive species, re‐examine species delimitations, identify cryptic species through

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microhabitats, and are distributed over small geographical areas. Beetles of oceanic islands, isolated dunes, caves, mountains, and other eco­ logical islands fit into this category. Currently, 791 species appear on the International Union for Conservation of Nature (IUCN) Red List of Threatened Species, of which 12 are listed as extinct, 17 as critically endangered, 47 as endan­ gered, and 45 as vulnerable (Table 11.5). Species on the Red List belong to 22 families. Habitat destruction and the introduction of invasive spe­ cies continue to threaten most natural ecosys­ tems and their myriad beetle species (Spence and Spence 1988, Kamoun 1996, Martikainen and Kouki 2003, Munks et al. 2004, Abellan et al.

integrative ­taxonomy, and expose gaps in taxo­ nomic knowledge. The barcode library remains far from complete, so the next steps are to con­ tinue to identify and target taxa with poor cov­ erage. This challenge to find DNA‐quality specimens will increase, as the bulk of the remaining taxa are cryptic species with small geographical ranges.

11.4  Threatened Beetles Many beetles are vulnerable to local and global extinction. These beetles often have low powers of dispersal (flightless), occur only in specific

Table 11.5  Number of Coleoptera species on the IUCN (2015) Red List of Threatened Species, by family. Suborder

Superfamily

Adephaga

—

Polyphaga

Staphylinoidea Scarabaeoidea

Family

CR

EN

VU

NT

LR/NT

LC

DD

Total

Carabidae

1

2

2

2

—

1

—

—

8

Dytiscidae

6

2

8

6

—

—

—

—

22

Leiodidae

—

—

—

1

1

—

—

—

2

Silphidae

—

1

—

—

—

—

—

—

1

Lucanidae

—

4

6

4

1

1

4

—

20

Scarabaeidae

—

2

15

15

20

—

302

232

586

Buprestoidea

Buprestidae

—

—

1

—

—

—

—

—

1

Byrrhoidea

Elmidae

—

—

—

1

—

—

—

—

1

Elateroidea

Eucnemidae

—

—

—

1

3

—

7

4

15

Elateridae

—

—

3

2

7

—

6

38

56

Bostrichoidea

Bostrichidae

—

—

—

—

1

—

2

—

3

Ptinidae

—

—

—

—

1

—

—

—

1

Cleroidea

Trogossitidae

—

—

1

1

—

—

1

3

6

Cucujoidea Tenebrionoidea

Erotylidae

—

—

—

1

—

—

2

6

9

Cucujidae

—

—

—

—

1

—

—

1

2

Mycetophagidae

—

—

—

—

1

—

—

1

2

Tenebrionidae

—

—

—

3

—

—

—

—

3

Anthicidae

—

—

1

—

—

—

—

—

1

Chrysomeloidea

Cerambycidae

—

1

9

8

3

—

8

8

37

Curculionoidea

Anthribidae

—

4

—

—

1

—

—

—

5

Curculionidae Total

EX

5

1

1

—

—

—

3

—

10

12

17

47

45

40

2

335

293

791

CR, critically endangered; DD, data deficient; EN, endangered; EX, extinct; LC, least concern; LR/NT, lower risk–near threatened; NT, near threatened; VU, vulnerable. The order of families follows that in Table 11.1.

11  Biodiversity of Coleoptera

2005, Davis and Philips 2005, Bouchard et  al. 2006, Talley and Holyoak 2006). Because the tax­ onomy and distribution of most beetles remain unknown, we argue that the number of species currently listed as at‐risk represents a gross underestimation of the number that should be targeted for conservation.

11.5 Conclusions Beetles are a diverse group of arthropods that occur in most non‐marine habitats (and a few marine ones). Their influence on science and society is great. Beetles provide essential eco­ logical services and are used as tools in many scientific endeavors, some with large effects on humans. On the other hand, beetles continue to have negative effects on vital industries such as agriculture and forestry. Studies on beetle bio­ diversity and the conservation of their habitats are necessary to ensure the sustainability of nat­ ural ecosystems and critical human activities.

Acknowledgments We thank P. D. N. Hebert and the staff of the Biodiversity Institute of Ontario for their col­ laboration on the beetles of North America bar­ coding project.

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11  Biodiversity of Coleoptera

Smith, A. B. T., D. C. Hawks and J. M. Heraty. 2006. An overview of the classification and evolution of the major scarab beetle clades (Coleoptera: Scarabaeoidea) based on preliminary molecular analyses. Coleopterists Society Monographs 5: 35–46. Smith, D. M. and J. D. Marcot. 2015 The fossil record and macroevolutionary history of the beetles. Proceedings of the Royal Society B 282: 20150060. Smith, K. G. V. 1986. A Manual of Forensic Entomology. Cornell University Press, Ithaca, NY. 205 pp. Sole, C. L., C. H. Scholtz and A. D. S. Bastos. 2005. Phylogeography of the Namib Desert dung beetles Scarabaeus (Pachysoma) MacLeay (Coleoptera: Scarabaeidae). Journal of Biogeography 32: 75–84. Sörensson, M. 1997. Morphological and taxonomical novelties in the world’s smallest beetles, and the first Old World record of Nanosellini (Coleoptera: Ptiliidae). Systematic Entomology 22: 257–283. Spangler, P. J. and W. E. Steiner, Jr. 2005. A new aquatic beetle family, Meruidae, from Venezuela (Coleoptera: Adephaga). Systematic Entomology 30: 339–357. Spector, S. 2006. Scarabaeine dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae): an invertebrate focal taxon for biodiversity research and conservation. Coleopterists Society Monographs 5: 71–83. Spence, J. R. and D. H. Spence. 1988. Of ground‐ beetle and men: introduced species and the synanthropic fauna of western Canada. Memoirs of the Entomological Society of Canada 144: 151–168. Stolz, U., S. Velez, K. V. Wood, M. Wood and J. L. Feder. 2003. Darwinian natural selection for orange bioluminescent color in a Jamaican click beetle. Proceedings of the National Academy of Sciences USA 100: 14955–14959. Stork, N. E. 1999a. The magnitude of biodiversity and its decline. Pp. 3–32. In J. Cracraft and M. Novacek (eds). The Living Planet in Crisis: Biodiversity, Science and Policy. American Museum of Natural History, NY.

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12 Biodiversity of Hymenoptera John T. Huber Natural Resources Canada, Canadian Forestry Service, c/o Canadian National Collection of Insects, Arachnids and Nematodes, Ottawa, Ontario, Canada

The past five years have seen changes in the number of recognized families of Hymenoptera (Table 12.1, Table 12.2) and a considerable increase in general knowledge, from descriptions of numerous new taxa and detailed biological information on many species ­ to  improved tools for their study. The Hymenoptera volumes of Zoological Record for 2005–09 listed more than 16,000 references. For 2010–14, 3000–4000 references per year were listed, totaling just over 17,500. Only a tiny fraction of these, mostly published since 2009, are cited below, and the choice is somewhat arbitrary, with emphasis on comprehensive publications. The most widely recognized hymenopterans – ants, bees, and wasps or hornets – have long been part of art, ritual, and folklore worldwide (Chauvin 1968; Hanson and Gauld 1995, 2006; Turillazza and West‐Eberhard 1996). But the order Hymenoptera contains far more species and diversity than ants, bees, and wasps. Other common names for some hymenopterans are paper wasp, potter wasp, yellow jacket, bumble bee, velvet ant, wood wasp, and horntail. These names have a narrower meaning than “wasp” or “ant” but are still collective names for several species in a single genus. Most

taxa lack English group names, although they can have anglicized group names based on their scientific name (e.g., ichneumon wasp). Common names are given to a few identifiable species of Hymenoptera, usually pests. If they have a common name, it is usually for species that have secondarily reverted to plant feeding or pollinating habits, such as gall wasp and fig wasp, or pest species widely dispersed by human agency, such as the Argentine ant, Linepithema humile (Mayr). Bees have been recorded by humans since the Stone Age, as shown by cave paintings (Gore and Lavies 1976, Valli and Summers 1988). The first recorded human casualty due to a wasp sting, 4500 years ago, was King Menes, Pharaoh of Egypt (Spradberry 1973). Fig wasps, despite their small size and inconspicuous habits, were known to the ancient Greeks and Egyptians (Kevan and Phillips 2001). Most Hymenoptera, however, belong to groups mostly unknown to the general public. These are mostly small (less than 5 mm long), parasitic species that go about their business unnoticed by all but the insect taxonomist, biological control specialist, or dedicated ­naturalist, and are often unnamed, even scientifically.

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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Table 12.1  Numbers of described species of extant Hymenoptera, listed by superfamily and family. Family

Number of valid described extant species*

Anaxyeloidea (1)

Anaxyelidae

1

Superfamily (number of species)

Symphyta (8,073 total) Cephoidea (160)

Cephidae

160

Orussoidea† (90)

Orussidae

90

Pamphilioidea (333)

Megalodontesidae

42

Pamphiliidae

291

Siricoidea (111)

Siricidae

111

Tenthredinoidea (7,169)

Argidae

897

Blasticotomidae

12

Cimbicidae

182

Diprionidae

136

Pergidae

442

Tenthredinidae

5,500

Xiphydrioidea (146)

Xiphydriidae

146

Xyeloidea (63)

Xyelidae

63

Ampulicidae

200

Andrenidae

2,917

Apidae

5,749

Colletidae

2,547

Crabronidae

8,773

Halictidae

4,327

Heterogynaidae

8

Megachilidae

4,096

Melittidae

187

Sphecidae

724

Apocrita (145,994 total) Apoidea (29,541)

Stenotritidae

21

Ceraphronoidea (603)

Ceraphronidae

304

Megaspilidae

299

Chalcidoidea (22,784)

Agaonidae

762

Aphelinidae

1,078

Azotidae

92

Chalcididae

1,469

Cynipencyrtidae

1

Encyrtidae

4,058

Eriaporidae

22

12  Biodiversity of Hymenoptera

Table 12.1  (Continued) Superfamily (number of species)

Chrysidoidea (6,780)

Cynipoidea (3,157)

Diaprioidea (2,109)

Evanioidea (1,130)

§

Ichneumonoidea (44,385)

Family

Number of valid described extant species*

Eucharitidae

427

Eulophidae

4,969

Eupelmidae

931

Eurytomidae

1,453

Leucospidae

134

Mymaridae

1,437

Ormyridae

125

Perilampidae

284

Pteromalidae

3,544

Rotoitidae

2

Signiphoridae

78

Tanaostigmatidae

93

Tetracampidae

44

Torymidae

900

Trichogrammatidae

881

Bethylidae‡

2,588

Chrysididae

2,500

Dryinidae

1,605

Embolemidae

39

Plumariidae

22

Sclerogibbidae

20

Scolebythidae

6

Austrocynipidae

1

Cynipidae

1,412

Figitidae

1,571

Ibaliidae

20

Liopteridae

153

Diapriidae

2,048

Ismaridae

29

Maamingidae

2

Monomachidae

30

Aulacidae

185

Evaniidae

449

Gasteruptiidae

496

Braconidae

19,439

Ichneumonidae

24,281 (Continued)

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Table 12.1  (Continued) Superfamily (number of species)

Family

Number of valid described extant species*

Megalyroidea (43)

Megalyridae

43

Mymarommatoidea (10)

Mymarommatidae

10

Platygastroidea (5,385)

Platygastridae

5,385

Proctotrupoidea (448)

Austroniidae

3

Heloridae¶

10

Pelecinidae

3

Peradeniidae

2

Proctorenyxidae

2

Proctotrupidae

403

Roproniidae

20

Stephanoidea (342)

Vanhorniidae

5

Stephanidae

342

Trigonaloidea (92)

Trigonalidae

92

Vespoidea (29,185)**

Bradynobaenidae

188

Formicidae

12,199

Mutillidae

4,302

Pompilidae

4,855

Rhopalosomatidae

72

Sapygidae

66

Scoliidae

560

Sierolomorphidae

11

Tiphiidae

2,000

Vespidae

4,932

* Aguiar et al. (2013), slightly updated. † L. Vilhelmsen (personal communication, July 2014). ‡ C. Azevedo (personal communication, July 2014). § Yu et al. (2012). ¶ L. Masner (personal communication, August 2014). ** Peters et al. (2017).

12.1 ­Evolution and Higher Classification Hymenoptera first appear in the fossil record in the middle Triassic, about 230  mya (Kukalová‐Peck 1991). By the late Jurassic (155 mya), the major groups were established (Heraty et  al. 2011). The primitive lineages were plant feeding; the parasitoid mode of life

and stinging Hymenoptera did not appear until about 210 and 155 mya, respectively (Grimaldi and Engel 2005). Some groups are extinct (Table 12.2), and today several small, archaic, and rarely collected hymenopteran families are found mainly or exclusively in the southern hemisphere. Nonetheless, the order diversified tremendously over the past 150 million–200 million years.

12  Biodiversity of Hymenoptera

Table 12.2  Numbers of described species of extinct Hymenoptera (many in families that are still extant), listed by superfamily and family. Family

Number of valid extinct species*

Anaxyeloidea (32)

Anaxyelidae

32

Cephoidea (44)

Cephidae

6

†

Sepulcidae

38

Orussidae

3

†

10

†

†

Karatavitidae

6

Pamphilioidea (26)

Megalodontesidae

1

Pamphiliidae

5

†

20

†

1

†

8

†

1

†

14

†

Sinosiricidae

1

Siricidae

13

Argidae

7

Blasticotomidae

1

Cimbicidae

19

Superfamily (number of species)

Symphyta (382 total)

Orussoidea (13)

Paroryssidae

Karatavitoidea (6)

Xyelydidae

Siricoidea (38)

Daohugoidae Praesiricidae Protosiricidae Pseudosiricidae

Tenthredinoidea (130)

Xyeloidea (93)

Diprionidae

2

†

Electrotomidae

1

Tenthredinidae

79

†

Xyelotomidae

21

Xyelidae

93

Ampulicidae

8

Andrenidae

11

†

Angarosphecidae

44

Apidae

87

Colletidae

2

Crabronidae

29

Halictidae

22

Megachilidae

34

Melittidae

4

Apocrita (2,024 total) Apoidea (244)

(Continued)

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Table 12.2  (Continued) Superfamily (number of species)

Family

Number of valid extinct species*

†

1

†

Paleomelittidae

1

Mellitosphecidae

Sphecidae

1

†

†

Belytonymidae

17

Ceraphronoidea (41)

Ceraphronidae

2

Megaspilidae

12

†

2

†

Stigmaphronidae

25

Agaonidae

4

Aphelinidae

1

Chalcididae

5

Encyrtidae

3

Eucharitidae

1

Eulophidae

3

Eupelmidae

5

Eurytomidae

3

Leucospidae

1

Mymaridae

20

Perilampidae

1

Pteromalidae

20

Tanaostigmatidae

1

Tetracampidae

9

Torymidae

13

Trichogrammatidae

3

Bethylidae

13

Chrysididae

9

Dryinidae

19

Embolemidae

9

†

1

†

Plumalexiidae

1

Sclerogibbidae

2

Scolebythidae

7

Cynipidae

11

Figitidae

11

†

Gerocynipidae

5

Ibaliidae

2

Belytonymoidea (17)

Radiophronidae

Chalcidoidea (94)

Chrysidoidea (61)

Falsiformicidae

Cynipoidea (33)

12  Biodiversity of Hymenoptera

Table 12.2  (Continued) Superfamily (number of species)

Family

Number of valid extinct species*

Liopteridae

2

†

1

†

Stolamissidae

1

Diapriidae

22

Protimaspidae

Diaprioidea (26)

†

Spathiopterygidae

4

†

Ephialtitidae

60

Evanioidea (86)

†

1

†

Anomopterellidae‡

9

Aulacidae

18

Evaniidae

19

†

Praeaulacidae

39

Braconidae

206

Ephialtitoidea (60)

Ichneumonoidea (427)

Andreneliidae

Ichneumonidae

216

†

Praeichneumonidae

5

Megalyroidea (5)

Megalyridae

40

Mymarommatoidea (14)

†

1

†

Gallorommatidae

3

Mymarommatidae

10

Platygastroidea (45)

Platygastridae

45

Proctotrupoidea (132)

Austroniidae

1

Alvarommatidae

Heloridae

14

†

39

†

1

†

Mesoserphidae

33

Pelecinidae

8

Peradeniidae

1

Proctotrupidae

26

Roproniidae

5

†

†

Serphitidae

9

Stephanoidea (8)

Stephanidae

8

Trigonaloidea (16)

†

Maimetshidae

11

Trigonalidae

5

Formicidae

620

Mutillidae

12

Pompilidae

16

Iscopinidae Jurapriidae

Serphitoidea (9)

Vespoidea (699)

(Continued)

425

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Table 12.2  (Continued) Superfamily (number of species)

incertae sedis ?near Chalcidoidea

§

Family

Number of valid extinct species*

Rhopalosomatidae

4

Sapygidae

1

Scoliidae

17

Sierolomorphidae

1

Tiphiidae

17

Vespidae

11

†

1

Khutelchalcididae

incertae sedis Apocrita

†

3

incertae sedis Apocrita

†

1

incertae sedis Apocrita

†

3

Archaeocynipidae Eostephanitidae Kuafuidae

† Superfamilies and families no longer extant. * Aguiar et al. (2013). ‡ Li et al. (2013). § Gibson et al. (2007).

Sharkey (2007) and Sharkey et al. (2012) gave historical overviews of the higher phylogeny and classification of the Hymenoptera. Both extant and extinct Hymenoptera were classified into two broad groups, the Symphyta and Apocrita (Ronquist 1999a, Davis et  al. 2010). The Symphyta (sawflies, wood wasps, and horntails) include the most primitive hymenopterans and comprise almost 5% of the extant Hymenoptera. Exploiting woody habitats was probably important in the early evolution of the Hymenoptera (Turrisi et  al. 2010). Symphyta grade into the Apocrita through the Orussidae, the only symphytan family with parasitic larvae and an antennal cleaner closely resembling that in the Apocrita (Vilhelmsen 2001, 2003). Most symphytans have a conspicuous, free‐living, caterpillar‐like larva that feeds on leaves, shoots, and cones; the relatively few stem‐ and wood‐ boring species have a more grub‐like larva. Because certain symphytans occasionally can be serious pests of trees and shrubs, they have received considerable attention from foresters, horticulturists, and home gardeners. The Apocrita include about 96% of the Hymenoptera and are subdivided into the Aculeata (stinging hymenopterans), which include familiar

species such as ants, social wasps, and bees, and the Parasitica, a diverse and abundant group of usually small, inconspicuous species, most of which parasitize insects and spiders. Unlike true parasites, which spend their entire life inside or on a host and do not usually kill it, the Parasitica have free‐living adults whose larvae develop singly or gregariously on or in a single host individual, eventually killing it; they are better called parasitoids instead of parasites. The larvae of the Apocrita are usually grub‐like and not free living. The Apocrita and Aculeata are monophyletic groups (Rasnitsyn and Zhang 2010, Heraty et al. 2011), as are the free-living sawflies (Eusymphyta) and a major subgroup of the Parasitica (the Parasitoida) (Peters et al. 2017). However Relationships among hymenopteran families and superfamilies are still not completely resolved.

12.2 ­Numbers of Species and Individuals Hymenoptera have diversified into various morphological forms and ways of life and might be the largest order of insects (Gaston 1993, Austin and Dowton 2000), although currently the order

12  Biodiversity of Hymenoptera

ranks third or fourth after Coleoptera, Lepidoptera, and Diptera (Stork 1997). Pagliano and Scaramozzino (1990) counted approximately 125,000 described species and more than 17,000 generic names but, based on species‐area relationships, Ulrich (1999) estimated that the number of species could be 1 million. Aguiar et  al. (2013) updated the figures to 152,565 extant and 2406 extinct species (subspecies were not included) in 8423 extant and 685 extinct genera. Slightly more than 154,000 extant and 2400 extinct species are now recognized (Table 12.1,Table 12.2). Most described species are distributed in temperate areas, where a far higher proportion of the fauna has been described, compared with tropical areas (Gaston 1993). Bassett et  al. (2007) included two hymenopteran families in their survey results for a biodiversity study in Panama: Braconidae with 2500 individuals ­collected, representing about 80 species (31% identified to species at the time of publication), and Formicidae with about 50,000 individuals, representing 291 species (57% identified to species). An estimated number of species for Panama was given for the Formicidae (301 species) but not for the Braconidae. Even though only two hymenopteran families were treated among the major focal taxa studied, the information tabulated reflects the poor taxonomic knowledge of the Parasitica compared with the Aculeata. Noyes (2012) provided evidence from his collecting of the Chalcidoidea in Costa Rica that Hymenoptera are probably the largest insect order. In a six‐hour period of intensive sweeping, Noyes (2012) estimated that 790 species of Chalcidoidea (1286 total species of Hymenoptera) were collected. Among the five temperate regions that Gaston (1993) compared, the best known fauna is that of the United Kingdom, where an estimated 82% of the species are named, and the most poorly known is Switzerland, where only 21% are named. For Europe as a whole, 13,211 species (excluding Ichneumonoidea) have been described (Mitroiu et al. 2015). When the species of Ichneumonoidea are added, this figure

still will represent only about 10% of the described world fauna. Not all the remaining species in these areas need to be described because they might have been described from nearby countries, but the numbers demonstrate that even in temperate zones the proportions of named species can be relatively low. Gaston’s (1993) figures are optimistic because taxonomists estimate that in groups such as the small parasitic wasps much less than 10% of the species have been described worldwide. For example, Fernández‐Triana et  al. (2014) described 186 new species of Apanteles (Braconidae: Microgastrinae) from Guanacaste National Park, Costa Rica; previously, only 19 species were known from Mexico and all of Central America. Other examples within the Braconidae are those of Marsh et al. (2013) for Heterospilus (Doryctinae) of Costa Rica, with 280 species (277 new), and Butcher et al. (2012) for Aleiodes (Rogadinae) of Thailand, with 179 new species. The number of individuals of hymenopterans at the family or superfamily level that can be collected at a given locality varies considerably. Three surveys in Europe – two in forests for all Hymenoptera and one in agroecosystems for the Parasitica only – indicate relative numbers. Martínez de Murgía et  al. (2001) collected 78,229 specimens representing 12 superfamilies and 35 families in Malaise traps in a mixed deciduous‐coniferous forest at an elevation of about 600 m in north‐central Spain. The numbers of specimens in the three major divisions of the Hymenoptera were 440 (0.6%) Symphyta, 1270 (1.6%) Aculeata, and 76,519 (97.8%) Parasitica. The Parasitica contained the following: Ichneumonoidea, 31,110 (39.8%); Proctotrupoidea, 19,990 (25.6%); Chalcidoidea, 13,097 (16.7%); Ceraphronoidea, 5395 (6.9%); Platygastroidea, 5287 (6.8%); and Cynipoidea, 1640 (2.1%). Two families, the Ichneumonidae and Diapriidae, constituted 57% (43,903 specimens) of the Parasitica. Mederos‐López et  al. (2012) collected 7796 Hymenoptera representing 37 families in 14 superfamilies in Malaise traps in northeastern Spain in a Mediterranean mixed forest at an elevation of 290 m. This

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f­orest was drier than the forest studied by Martínez de Murgía et al. (2001), and the proportion of Aculeata specimens was higher: 23 (much less than 0.4%) Symphyta; 1111 (16.0%) Aculeata; and 5799 (83.6%) Parasitica. They also studied the proportion of specimens collected at 12 m, about mid height in the canopy, compared with that in the understory near ground level. The Malaise trap in the understory yielded 88.9% of the total specimens, dominated by three families, the Diapriidae, Braconidae, and Formicidae. Schmitt (2004) surveyed the Parasitica using 1 m2 light boxes on the ground in cereal fields, fallow fields, and variously managed grasslands. The 23,781 specimens collected represented six superfamilies and 24 families: Platygastroidea, 8986 (37.8%); Chalcidoidea, 8815 (37.1%); Ichneumonoidea, 2860 (12.0%); Ceraphronoidea, 1966 (8.3%); Proctotrupoidea, 1005 (4.2%); and Cynipoidea, 149 (0.6%). Results for the Parasitica are not strictly comparable because of different collecting methods, but the numbers indicate tendencies in the relative proportions of the major groups. Noyes (1989a) treated a tropical area in Sulawesi, Indonesia, and concluded that the diversity of all families of Hymenoptera there, except possibly Symphyta and the gall‐forming Cynipidae, was almost certainly greater than in the United Kingdom. The diversity of the Parasitica as a whole seems to be greater in tropical than in temperate areas, although tropical areas vary considerably. The Aculeata and Symphyta are generally collected in smaller numbers than are the Parasitica, due partly to the collecting techniques but also because of the inverse correlation between number of specimens and body size. No passive collecting methods are efficient at collecting social Hymenoptera, especially the many soil‐dwelling groups such as ants. Individual workers can be collected in traps but, because colonies are patchy, most individuals are missed unless by chance a trap is placed next to a colony. Consequently, the number of individuals of social species is greatly underestimated. Ants occur in huge numbers in all areas

except the highest latitudes. Bees and social wasps are also abundant in the tropics. Hölldobler and Wilson (1994) cited a study by German ecologists near Manaus, Brazil, who estimated that ants, termites, stingless bees, and polybiine wasps accounted for 80% of the insect biomass and one‐third of the biomass of all animals in the area. Even when termites are excluded, the vast numbers and correspondingly high total weight of the social Hymenoptera, compared with other animals, are astonishing. As discussed by Hölldobler and Wilson (1990), ants alone might represent 10–15% of the entire biomass in terrestrial ecosystems and about 8 million individuals in a hectare of Amazonian forest soil.

12.3 ­Morphological and Biological Diversity Hymenopteran morphology is so diverse that some species might not be recognized as Hymenoptera (Fig. 12.1, Fig. 12.2). The structure of any particular body part, such as mandibles, is remarkably varied, as shown by scanning electron micrographs of one group only, the ants (Bolton 1994, 2000). Body color covers the visible spectrum, and color combinations and patterns are often remarkable, partly because showy, contrasting colors such as yellow or red and black (Manley and Pitts 2007, Buck et  al. 2008) effectively advertise that stinging Hymenoptera are dangerous and best left alone. In size, extant Hymenoptera range from 0.13 to 75.0  mm in body length (Mymaridae and Pelecinidae, respectively). If the extended ovipositor and antennae are included, females of Megarhyssa species (Ichneumonidae) are up to 20 cm long, making them the world’s longest hymenopterans, although they are still slender bodied, a characteristic of most species of the Parasitica. Titans such as Pepsis species (Pompilidae) with a body length up to 66 mm and a wingspan of 110 mm are among the heaviest species. Adult life span is only a few days or even a few hours for many small parasitoid

12  Biodiversity of Hymenoptera

(a)

(b)

Figure 12.1  Dicopomorpha echmepterygis Mockford, paratype (Mymaridae). (a) Entire body, lateral. (b) Ventral (with fungal hypha coming out of mouth opening). Images by Klaus Bolte.

s­ pecies, to almost 28 years for queens of some ant species. The nesting structures created by some Aculeata also vary tremendously, ranging from dainty clay pots to massive yet intricate paper nests and enormous, complex underground or above‐ground dwellings. An above‐ground wasp nest 7 m long was discovered in an abandoned house in the Canary Islands, breaking a previous record of 3.7 m long and 1.75 m in diameter on a farm in New Zealand. Both nests were constructed by Vespula spp. (Vespidae). Most Hymenoptera are solitary, but among truly social species (ants, some wasps, and bees) colonies of millions of individuals occur. The largest are the supercolonies of the Argentine ant, Linepithema humile (Mayr) (Vogel et  al. 2010) and the little fire ant, Wasmannia auropunctata (Roger) (Tindo et al. 2012), both native to Latin America but now widely distributed. General texts with comprehensive treatments of Hymenoptera are by Marshall (2006) and Triplehorn and Johnson (2005) for North America and by Naumann (1991) for Australia. Books devoted exclusively to the entire order for a particular region are by Gauld and Bolton (1996) for the United Kingdom, Hanson and Gauld (1995, 2006) for Costa Rica, and Fernández

and Sharkey (2006) for the Neotropical region. Other important works include a discussion of hymenopteran diversity and importance (LaSalle and Gauld 1993), overviews of the Symphyta (Benson 1950), biology of the Parasitica (Quicke 1997) and solitary Aculeata (O’Neill 2001), and family identification keys and diagnoses for the world (Goulet and Huber 1993).

12.4 ­Importance to Humans 12.4.1  Food and Other Products

By far the most important food produced by any hymenopteran is honey, which is harvested from several bee species. Other honeybee products  –  bee wax, propolis, and royal jelly  –  also are important, for example in the production of cosmetics. The larvae of social bees or wasps and the repletes of certain ant species (Wilson 1971) are eaten by some peoples. Specialty products, such as mead (honey beer), liquor distilled from honey, and chocolate‐coated ants, are commercially available. Oak galls, induced by some species of Cynipidae, were used in Europe during the Middle Ages for tanning, ink production, and sometimes medicine.

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Figure 12.2  Kikiki huna, habitus. Kikiki huna (Mymaridae) is the smallest known winged insect. Image by J. Read.

12.4.2  Stings and Bites

The first serious encounter most people have with the Hymenoptera is personal and usually memorable. Every year thousands of people receive the unwanted attention of bees, wasps, or ants. More often than not, more than one individual, and often many, attend to the unfortunate victim, especially when an entire nest or colony has inadvertently been disturbed. Depending on the species, a single individual can deliver one or several stings, bites, or sometimes both, as with bulldog ants in Australia and

fire ants in the western hemisphere. The insect is not, of course, “angry,” although that might be debatable. Rather it or, correctly, she  –  only females have stingers and most do the biting – is defending herself or her nest from what is perceived as a threat to life or colony. Regardless, the memory of the event is usually long‐lasting and results in the victim being more cautious whenever hymenopteran nests are in the vicinity. Most stings and bites occur precisely because the person does not know and accidentally steps on an individual hymenopteran or inadvertently

12  Biodiversity of Hymenoptera

approaches a nest hanging in a bush, above a door, or under a balcony or veranda. Less often, the individual knows a bee or wasp is around and starts flailing wildly at it  –  an action that increases the chances of being stung (Schmidt and Boyer Hassen 1996). Stings can cause local or systemic hypersensitive reactions that lead to death (Schmidt 1986, Schmidt 1992, Goddard 1996, Levick et  al. 2000, McGain et  al. 2000, Voss et al. 2016). A survey of about 2000 physicians in the southern United States in 1988 indicated that 22,755 patients had been treated for reactions to fire ant stings; 2% of them suffered from anaphylactic shock (Goddard 1996). Although most females of the Aculeata are capable of stinging in self‐defense, the solitary, predatory species use their stingers almost exclusively to deliver venom to paralyze insect or spider prey. Humans, therefore, are rarely stung by solitary wasps and their venom does not cause pain, although notable exceptions occur in the Bethylidae, Mutillidae, and Pompilidae. Some Pepsis species and the bullet ant Paraponera clavata (Fabricius) deliver the most painful stings known (Schmidt 2016). Schmidt’s (2004) advice to any unfortunate victim stung by one is to “lie down and scream.” The intense pain, however, lasts only a few minutes. The venoms and stings of highly social (eusocial) Hymenoptera are painful because they are used for colony defense against vertebrate predators (Schmidt 1990) and a painful sting discourages those predators, including humans, that raid bee colonies for honey. A few species of the Parasitica also can “sting.” The relatively large, nocturnal, orange species of Ophion and Enicospilus (Ichneumonidae) can deliver a painful jab with the tip of their short, sharp ovipositor. The importance of bee and wasp stings has resulted in the commercial production of life‐saving antivenins. Pharmacological research on venoms might yield other kinds of useful medications (Beleboni et al. 2004). Hymenoptera have biting mouthparts that they use for feeding, capturing prey, building nests or, when necessary, defense. In tropical

countries, stingless bees defend their nests from human intruders by swarming over the body, pinching the skin, and pulling the hair. One species in tropical America also ejects a burning liquid from its mandibles (Wilson 1971). When ants bite a person, they may not let go even when decapitated. This has been put to use by indigenous tribes in Latin America and Africa where species of various ant genera, including Atta (leaf‐cutter ants), Eciton (army ants), and Dorylus (driver ants), can be used to keep wounds closed. Hundreds of ant bites occurring simultaneously can have a considerable effect (Moffett 1986).

12.5 ­Ecological Importance Hymenoptera occur in all terrestrial habitats and some aquatic ones (Bennett 2008b). They have crucial ecological roles, as summarized by Gauld et  al. (1990), LaSalle and Gauld (1993), Hanson and Gauld (1995, 2006), and, for ants, by Hölldobler and Wilson (1994) and Fisher and Cover (2009). Grissell (2001) wrote eloquently about the importance of insects, including Hymenoptera, in home gardens, where many people are likely to observe them. Pollination by bees, fig wasps, and pollen wasps is the most beneficial role of the Hymenoptera, without which many plants, including most crops, would disappear. Parasitism and predation of insects are important activities of many Hymenoptera, which prevent many insect species from becoming crop and forest pests. When food webs are intensively investigated, many Hymenoptera are found to be involved, and the webs can be complex (Eveleigh et al. 2007). The role of polydnaviruses, a group of viruses found so far only in some Ichneumonoidea and Nasonia (Pteromalidae), has implications for biological control because of their action in inhibiting wasp‐egg encapsulation and manipulating host development to allow wasp development and emergence (Beckage 1998, Herniou et al. 2013). Polydnaviruses are also of considerable interest to basic research in virology

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(Frederici and Bigot 2003). Wolbachia, a genus of bacteria that is sexually transmitted and inherited through the female line, is widespread in insects (Werren and Windsor 2000) and strongly skews sex ratios in various parasitic wasps. Finding ways to manipulate or eliminate the bacteria might affect the biological control potential of their host insects (Floate at al. 2006). Ants play an immensely important part in soil formation by mixing and aerating it. They also are the predominant scavengers of other organisms their own size, and thus help to recycle dead insects, which they carry back to their nests as food. Ants alter the abundance and distribution of flowering plants, especially in arid areas, by transporting seeds and discarding some of them uneaten around nests or by protecting some plant species from plant‐feeding insects. Hymenoptera have serious nuisance or deleterious roles as well. Some ants feed on seeds, and since ancient times they have been reported as grain pests. Some chalcid wasps develop inside seeds of conifers and other plants, reducing the numbers of viable seeds for plantation forestry. Symphyta and many ants feed on leaves or burrow in wood; they are among the most serious defoliators of conifers in temperate regions and of broad‐leaved trees in the tropics, respectively. Some leaf‐cutter bees can be nuisance defoliators of garden plants. Ants protect sap‐sucking insects from parasitism by other insects, allowing them to increase in numbers sufficiently to cause serious plant damage. Many ant species have become worldwide nuisance insects in human dwellings and on agricultural land, where livestock may be adversely affected. Gall‐forming chalcids (LaSalle 2005) and gall wasps (Kjellberg et  al., 2005) deform or kill plants, and wood‐tunneling carpenter bees damage wood dwellings. Numerous animals and plants depend on Hymenoptera for their own existence. For example, more than 300 species representing a wide range of organisms are associated with one species of army ant, Eciton burchellii Westwood (Rettenmeyer et al. 2011).

12.6 ­Conservation The deleterious effects of some species are greatly outweighed by their beneficial roles. Hymenoptera, particularly bees, need to be conserved or augmented (New 2012) for efficient pollination of many plant species, especially crops, and to promote natural and biological control of pest or potential pest insects (Consoli et  al. 2010). To date, almost all Hymenoptera conservation efforts treat bees (Goulson 2009, Dicks et  al. 2010) and ants, but Parasitica also might need conservation (Shaw and Hochberg 2001). Attempts at doing this are underway in Europe (Gauld et  al. 1990) and elsewhere, but more should be done.

12.7 ­Fossils Beautifully preserved Hymenoptera in amber inclusions or as impressions in rock continue to be discovered. Penny and Jepson (2014) list the major insect fossil deposits, many of which yield Hymenoptera. Specimens in amber and in rock date back to the Cretaceous Period (144–65 mya; Grimaldi and Engel 2005, Engel et  al. 2013, Rasnitsyn et  al. 2015) and the Jurassic Period (197–145 mya; Wang et al. 2012, 2014a, 2014b) of the Mesozoic Era. Major amber‐bearing deposits of the Paleogene Period (65–24 mya) in the Cenozoic Era also occur (Wang et  al. 2014) and are important for tracing faunal turnovers. Some fossils help to clarify higher relationships by showing transitional forms (Krogmann and Nel 2012). Although dating of impression fossils is still uncertain and controversial, their discovery helps significantly in estimating divergence times of different lineages (Ronquist et al. 2012). Many insects diversified with flowering plants, which arose about 140–110 mya and became the dominant group of vascular plants on Earth by 90–80 mya. The first pollinators were likely beetles; it is perhaps not surprising that the earliest known parasitic lineage, the

12  Biodiversity of Hymenoptera

Orussoidea, and probably also the earliest lineages of Parasitica, parasitize beetles, although they might have parasitized other Symphyta in wood instead of, or in addition to, beetles. The Parasitica that attack cockroach egg cases are also old, because their hosts are an ancient group. Because the Symphyta include the oldest lineages in Hymenoptera and were the only members of the order around to be preserved, their fossil record is the longest among Hymenoptera, extending back to the time when their plant hosts, particularly ferns and conifers, were dominant. The Symphyta have a much higher proportion of extinct families than do the Apocrita. Eleven of 25 families (almost 50%) of the Symphyta are entirely extinct, and fossils in all but two extant families (Pergidae and Xiphydriidae) are known, whereas in the Apocrita, 27 of 119 (about 23%) of the families are entirely extinct, although fossils in all but 16 extant families are known (Table 12.1, Table 12.2). The limits of extinct families are debatable, so the numbers of recognized extinct families of Hymenoptera vary. Thus, Rasnitsyn et al. (2015) listed for the Cretaceous only 12 named families, eight undetermined families in known superfamilies, and two undetermined Hymenoptera, none of which is represented in the extant fauna. In Table 12.1, 34 named families (some of which might be Tertiary) and four undetermined families are listed. Extinct Hymenoptera as impression fossils in rock range in body length from about 0.91 mm (Mymaridae) in the Parasitica to about 55 mm (extinct Praesiricidae) in the Symphyta  –  these examples date from about 46 mya and 126 mya, respectively (Huber and Greenwalt 2011, Gao et  al. 2013). Among the Aculeata, queens of Titanomyrma (Formicidae) were up to 6 cm long (Archibald et  al. 2011). Antropov et  al. (2014) characterized an entire fossil fauna, that of the Isle of Wight (Late Eocene). Based on 1460 specimens (1220 ants), 118 species in 20 families were recognized. Grimaldi et al. (1997) reviewed the genera of Formicoidea (Formicidae, the extinct Armaniidae, and one taxon of u ­ ncertain

­lacement) for the Cretaceous Period, and p LaPolla et  al. (2013) reviewed the fossil Formicidae across all periods. These are, respectively, the only recent studies of an entire fossil fauna for a given locality, for an entire superfamily across all localities for a given geological time period (Cretaceous in this case), and for a family through its entire fossil history.

12.8 ­Collecting, Preservation, and Study Techniques If we seem to know much about the Hymenoptera, it is due mainly to technological advances over the past 50 years that facilitate their collection, preservation, and study. General techniques for collecting insects almost invariably result in the capture of huge numbers of Hymenoptera. Passive collection methods, such as pan traps (Abrahamczyk et  al. 2010, Saunders et al. 2013), Malaise traps (Darling and Packer 1988), flight‐intercept traps (Masner and Goulet 1981), and pitfall traps (Skvarla 2014) set in a variety of habitats, and active methods, such as car nets (Peck and Cook 1992) and sweeping vegetation using a triangular net (Noyes 1982), yield enormous numbers of specimens representing a great diversity of species. Methods developed for other orders of insects, such as light traps (Winter 2000), window traps (Peck and Davies 1980) and, for flightless ­species, Winkler funnels (Besuchet et al. 1987), also yield certain taxa not often collected by other methods. Several studies compare different collecting methods for the Hymenoptera (Noyes 1989b, Campbell and Hanula 2000, Bartholomew and Prowell 2005, Wells and Decker 2006, Roulston et  al. 2007, Mazon and Bordera 2008). To obtain the greatest diversity of taxa, a variety of collection methods is needed, and the greater the diversity of microhabitats sampled, the better. Rearing specimens provides the most useful biological information for the Parasitica and Symphyta and is essential information if parasi-

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toids are being considered for use as biological control agents (Heraty, this volume). Apart from obtaining correct host associations from known hosts, rearing provides reliable association of the sexes. Rearing larvae of the Symphyta allows association with adults, if the problem of overwintering the pupae can be surmounted. Almost all Hymenoptera need a source of energy, mainly for flight in winged species and egg maturation in females of many species. Nectar is a well‐ known source, but honeydew or tree sap is perhaps important for some taxa; such taxa can be attracted to artificial baits of various kinds, for example, to control ants in buildings. Having collected enormous numbers and diversity of Hymenoptera, it is necessary to extract them from bulk samples, preserve them appropriately in the short or long term for study,  and identify them. No formal publications ­summarize procedures for efficiently sorting Hymenoptera, especially the smallest specimens, from bulk samples. The steps for complete retrieval of even the smallest specimens are fairly straightforward. First, the larger insects are separated by gently shaking them in a container of 70% ethanol, using a coarse‐mesh screen cage made of galvanized metal or similar material (Fig. 12.3a). The large insects are then dumped into a white enamel pan so that specimens can be searched for by eye. Insects that fall through the coarse‐mesh cage are then screened through mid‐ and fine‐mesh screens, respectively. The successive samples of mid‐ and small‐sized insects are poured into a fine‐mesh net (Fig. 12.3a), washed gently under tap water to remove dirt, and placed into a clean container of 70% ethanol for sorting. Each fraction is sorted separately spoonful by spoonful under a low‐power dissecting microscope, preferably using a rectangular dish (Fig. 12.3b) with parallel, raised divisions to avoid going over the same area twice. Immediately segregating the specimens into higher taxa – for example, Aculeata, Symphyta, and Parasitica, or Ichneumonidae, Braconidae, and Chalcidoidea  –  makes the specimens more accessible and available to interested specialists for extraction, prepara-

tion, and study of particular taxa. Because efficient sorting results in large numbers of specimens, the chance of finding teratological specimens is greatly increased. Gynandromorphs are perhaps the most interesting of these because they can help to associate the sexes; they have been found throughout the Hymenoptera (Popovici et al. 2014b). Preservation techniques have changed over time and are often simple, although some were not widely practiced until the advent of molecular taxonomy. Traditionally, specimens were pinned or were card or point mounted. If killed in liquid fixative, less sclerotized specimens often shrivel, making their study difficult. Critical point drying (Gordh and Hall 1979) or chemical drying (Heraty and Hawks 1998) of specimens initially collected into a liquid (water, ethanol, and propylene glycol) results in higher‐ quality specimens that are easier to study because there is no collapse of body parts. Preservation in high concentrations of ethanol (preferably 95% or higher) and cold storage in freezers results in specimens that are suitable for molecular work, and preserves body color well for decades; however, high ethanol content tends to make specimens more brittle and is not recommended if the specimens are simply to be pinned or card mounted. DNA extraction before slide mounting in Canada balsam for small specimens results in better slide preparations and has the added advantage of providing molecular data for species diagnosis and an independent character set that helps to resolve phylogenetic relationships. Despite the availability of large hymenopteran collections in public institutions, a high proportion of specimens remain unstudied in detail, mainly due to the lack of sufficient taxonomists interested in the small, parasitic species. Study techniques are more diverse than in the past and increasingly require specialized equipment, knowledge, and time, so many papers that combine independent lines of evidence ­ (­ integrative taxonomy) are multi‐authored. Krogmann and Vilhelmsen (2006) and Vilhelmsen (2011) used scanning electron microscopy to

12  Biodiversity of Hymenoptera

(a)

(b)

Figure 12.3  (a) Cages, trays and fine‐mesh net for sorting bulk samples of insects. Also shown, coarse fraction of insect material in coarse‐mesh cage. (b) Results of finer scale sorting through finer‐mesh cages.

study the mesosomal skeleton of Chalcidoidea, and head‐capsule characters and their phylogenetic implications in Hymenoptera, respectively. Vilhelmsen et al. (2010a) combined photographs, scanning electron micrographs, and phylogenetic methods to analyze internal and external features of the mesosoma of selected Apocrita. Statistical techniques (Baur and Leuenberger 2011, László et  al. 2013) have been applied to resolve closely related species that have long been undetected by other ­methods. Conversely, such

techniques also have been used to show infraspecific morphological variation (Popovici et  al. 2013), sometimes resulting in new synonymies (Popovici et  al. 2011). Gokhman (2009) and Gokhman and Gumovsky (2009) studied karyotypes to provide information on higher relationships and species differences in the Chalcidoidea. Molecular data alone (Pilgrim et al. 2008, Munro et al. 2011) or in combination with morphological data  (Carpenter and Wheeler 1999, Debevec et al. 2012, Heraty et al. 2013, Prous et al. 2014)

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provide new insights into phylogenetic relationships within the Hymenoptera. Although the microscope was invented in the 1600s, it is during the past 50 years in particular, when the scanning electron microscope began being used to study insects (in the 1960s) and light microscopes of increasing quality were developed, that the study of smaller‐bodied Hymenoptera became easier. Better lighting systems and digital imagery (Mullins 2011, Brecko et al. 2014) have contributed to morphological work of the largest (Schiff et al. 2013) to the smallest (Huber and Noyes 2013) Hymenoptera, especially of the Parasitica, whether extant (Mikó et al. 2007, Talamas and Buffington 2014) or extinct (Krogmann 2013). Digital images using stacking software programs to combine numerous single‐focus images into high‐quality composite images of particular morphological structures or entire specimens are replacing scanning electron micrographs, although the latter are still useful for detailed morphological study of minute specimens. The latest light microscope used in morphological work is the confocal microscope (Ernst 2011, Popovici et  al. 2014b). X‐ray microtomography provides a new way to study fossils in amber, and X‐ray cine‐tomography has been used to study morphological dynamics in millimeter‐size insects (Kamp et  al. 2013). Traditional techniques are still important to clarify structure and to standardize morphological terms. Examples include the use of detailed line drawings of anatomical structures such as the mesofurca and mesopostnotum in Hymenoptera (Heraty et al. 2004), drawings and photographs of Malpighian tubules in Platygastridae (Popovici and Johnson 2012), and analysis of general morphology for Cynipoidea (Ronquist and Nordlander 1989) and Opiinae (Braconidae) (Karlsson and Ronquist 2012). DNA barcoding and genomics provide additional data that are useful for identifying species and developing well‐founded phylogenies (Sperling, this volume). Riedl et  al. (2013) discussed a way to speed up the process of describ-

ing large numbers of new species. For parasitoid and phytophagous species, rearing from known hosts is recommended because of the biological data obtained (Arias Penna 2014). The backbone of hymenopteran taxonomy, however, still remains morphology. Yoder et  al. (2010) and Seltmann et  al. (2012) developed the online Hymenoptera Anatomy Ontology Portal (HAO: http://portal.hymao.org/projects/32/public/ ontology/) to define and illustrate morphological terms. Balhoff et al. (2013) provide a semantic model for species descriptions.

12.9 ­Taxonomic Diversity Taxonomic and biological information on the main hymenopteran groups is given below. Older taxonomic and biological literature is listed under the appropriate family by Goulet and Huber (1993) and, for Central and South America, by Fernández and Sharkey (2006). The number of new genus‐group and family‐group taxa, respectively, listed in the 2010–14 Hymenoptera volumes of Zoological Record is as follows: 2010, 63/8; 2011, 106/13; 2012, 65/6; 2013, 54/4; and 2014, 87/4. In the description of new species, especially the small, parasitic ones, no end is in sight. Each year, hundreds of extant or extinct new species are described and numerous, previously described species are synonymized. This probably reflects reality – there really are huge numbers of new species still to be described – but it is also true that many are described poorly or are not described in the context of revisionary works. Thus, too many are re‐described more than once, resulting in more than one name for the same species until someone eventually places the redundant names in synonymy. It is almost impossible for a taxonomic study of the entire order to be treated in a single publication for a single country or large region. The only recent example is for Greenland, which has a small hymenopteran fauna of about 200 species (Böcher et  al. 2015). Species numbers are given in Table 12.1 and Table 12.2.

12  Biodiversity of Hymenoptera

12.9.1 Symphyta

Adult symphytans in 14 families (six superfamilies) are relatively well known taxonomically for the western hemisphere, but much less so for the tropical eastern hemisphere. The larvae of all families need taxonomic work at the species level, particularly because they are the most conspicuous and damaging stage. Blank et  al. (2006) compiled papers on ecology, taxonomy, faunistics, and checklists. Taeger et  al. (2010) cataloged the species. Schulmeister (2003) proposed a higher classification based on male genitalia. Nyman and Malm (2015) proposed a phylogeny of symphytan family groups based on molecular analysis. Wang et al. (2015) investigated inter‐ relationships of the Pamphilioidea. Schiff et al. (2013) treated the world genera and New World species of the Siricidae. Prous et  al. (2014) treated the genera of Nematinae, perhaps the last remaining complex of genera within the Tenthredinidae, and proposed a new generic classification. The Siricidae, Anaxyelidae, and Xiphydriidae have larvae that bore in wood. The Blasticotomidae bore in ferns, and the Cephidae bore in stems of grasses, Rubus, Rosa, Ribes, and soft Salix shoots. The Orussidae parasitize wood‐boring larvae, primarily those of beetles (Vilhelmsen 2003). The Xyelidae include the most primitive living Hymenoptera; the larvae feed on leaves or pollen‐ producing cones of pines. The remaining ­families – Megalodontesidae, Pamphiliidae, Ten­ thredinidae, Argidae, Cimbicidae, Diprionidae, and Pergidae  –  have leaf‐feeding or leaf‐mining larvae. 12.9.2 Parasitica

Most species in the 12 superfamilies of the extant Parasitica are parasitoids of insects and spiders. The next five superfamilies, each with only one included extant family (except the Evanioidea, with three), are relatively small but diverse in morphology, hosts, and habits. They contain an unusual number of rare, archaic species, many of them associated with wood. Apart

from the Evaniidae, they are not important economically but are scientifically important in biology and conservation, and for inferring phylogenies. The last seven superfamilies include the most commonly encountered species, many of them important in the natural and biological control of pest insects. 12.9.2.1 Stephanoidea

Aguiar (2004) cataloged the Stephanidae, which consists of rarely collected, solitary ectoparasitoids of wood‐boring insect larvae, mainly beetles (Buprestidae and Cerambycidae). Engel et al. (2013) described a fossil genus and discussed implications of this taxon with regard to the age of the Stephanidae and the order Hymenoptera. 12.9.2.2 Megalyroidea

Shaw (1990a) discussed the phylogeny of Megalyridae. Most species are primarily associated with ancient tropical forests; the group is most diverse in Eucalyptus and Acacia habitats of Australia (Shaw 1990b). Vilhelmsen et  al. (2010a) discussed the past and present distribution of the genera and their phylogenetic relationships. 12.9.2.3 Trigonaloidea

Carmean and Kimsey (1998) treated the genera of the Trigonalidae. Most species are parasitoids of moths or social wasps; some are hyperparasitoids through parasitic flies (Tachinidae). Female trigonalids lay thousands of minute eggs on vegetation, where some are eaten by caterpillars; the larvae of the trigonalids hatch and either consume the caterpillar or wait until the caterpillar is parasitized by a tachinid fly and then consume the tachinid instead. Smith and Tripotin (2012) and Chen et  al. (2014) revised the species of Madagascar and China, respectively. 12.9.2.4 Mymarommatoidea

The Mymarommatidae include few described extant species. Most are less than 0.5 mm long. Members of this enigmatic worldwide group have a unique wing structure and two‐segmented petiole (Gibson et al. 2007). Vilhelmsen

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and Krogmann (2006) studied the skeletal anatomy of one species. Their biology is unknown, but Huber et al. (2008) suggested that they parasitize Psocoptera eggs. 12.9.2.5 Evanioidea

Three disparate families are included in this superfamily. Jennings and Austin (2004) reviewed the biology and host relationships of the Aulacidae and Gasteruptiidae. Aulacids are parasitoids of wood wasps (Xiphydriidae) and beetles (Buprestidae and Cerambycidae). Smith (2001) cataloged the family, and Turrisi et al. (2009) discussed aulacid phylogeny and generic concepts. The Evaniidae, or ensign wasps, so called because their abdomens in profile ­resemble semaphore flags (they also waggle their abdomens up and down as they walk), are solitary predators inside cockroach oothecae. Deans and Huben (2003) provided keys to the genera, and Deans (2005) and Deans et  al. (2014) cataloged the species. Mikó et al. (2014) illustrated a unique wing‐folding mechanism in species of two genera. The Gasteruptiidae, with six genera in two subfamilies, are parasitoids of bees and pollen wasps. Jennings and Austin (2002) treated the genera and species of the Hyptiogastrinae. 12.9.2.6 Ichneumonoidea

Two families comprise this superfamily, the Braconidae and the Ichneumonidae. It is by far the largest superfamily, with almost 2600 genera. Yu et  al. (2012) cataloged the information on this superfamily from more than 33,000 scientific papers. Quicke (2015) reviewed the biology, systematics, evolution, and ecology. Braconidae  Although fewer in number of species and generally smaller bodied than the Ichneumonidae, the Braconidae are morphologically more diverse and better studied because a greater proportion of the species are important to agriculture and have been used in biological control. Species of the 35 or so currently recognized subfamilies range from 1 to 40 mm in length. Sharanowski et  al. (2011) proposed a molecular phylogeny of the subfamilies. The

Braconidae commonly parasitize the larvae of butterflies and moths, beetles, and flies, but hosts in other orders also are known. They can be endo‐ or ectoparasitoids, solitary or gregarious; some are polyembryonic, a few are hyperparasitoids, and even fewer are phytophagous (Wharton 1993). Wharton et al. (1997) provided keys to the more than 400 genera of the western hemisphere and summarized the biology for each subfamily. Yu et  al. (2012) cataloged the species. Whitfield et al. (2004) provided a family overview, suggesting that there are about 40,000–50,000 species worldwide, although this is probably an underestimate. Rodriguez et  al. (2013) e­stimated that for the Microgastrinae alone there are 17,000 to more than 46,000 species. Guanacaste National Park in Costa Rica, with a land area of only 1200 km2, has an accurate count of almost 1200 species of Microgastrinae, about 300 of which have been described (Fernández‐Triana et al. 2014). Stigenberg et al. (2015) treated the higher classification of the Euphorinae. Ichneumonidae  Gauld et  al. (2002) recognized

37 subfamilies based on morphology, whereas Quicke et  al. (2009) recognized 39 subfamilies based on a combination of morphology and a ribosomal molecule. Yu et  al. (2012) cataloged the species. Veijalainen et al. (2012, 2013) showed that the diversity of the Ichneumonidae is far greater than previously thought, with the number of tropical species previously being greatly underestimated. Although most specimens are moderate in size, the Oriental Megarhyssa glori­ osa (Matsumura) has a body length of 5.4 cm and an ovipositor up to 7.5 cm long, and the Nearctic Megarhyssa atrata (Fabricius) has a body length of about 4 cm, with an ovipositor length up to 16 cm. Rousse et al. (2016) treated the phylogeny of Ophioninae. Bennett (2015) treated the higher classification of Tryphoninae and summarized the known biology of Ichneumonidae. He estimated that about 30% of ichneumonid species are ectoparasitoids and about 70% are endoparasitoids. The overwhelming majority of species feed as larvae on or within the larvae or pupae of

12  Biodiversity of Hymenoptera

other holometabolous insects or on immature or adult spiders; less than 1% are predators. Most species parasitize the larvae and pupae of moths and butterflies (Lepidoptera). Others parasitize the prepupae or pupae of aculeate Hymenoptera or wood‐boring beetles. Certain subfamilies are restricted to a particular family or an unusual order of hosts. For example, species of Diplazontinae (Klopfstein et al. 2011) parasitize the Syrphidae (Diptera), and species of Agriotypinae (Bennett 2001) are ectoparasitoids of the prepupae and pupae of caddisflies (Trichoptera) in fast‐­running streams. The long respiratory filament of an Agriotypus pupa that pokes out of the host case is unique. Despite their abundance and widespread occurrence in most habitats (more common in forests than in grasslands and agricultural habitats), comparatively few ichneumonids have been used successfully in biological control, although they must be important in natural control. For example, Choristoneura budworms, which include some of the most devastating forest pests in North America, are parasitized by more than 110 species of Ichneumonidae (Huber et  al. 1996, Bennett 2008a). 12.9.2.7 Cynipoidea

This superfamily contains five extant families (Ronquist 1999b, Ronquist et  al. 2015). The Austrocynipidae, Ibaliidae, and Liopteridae together contain few, relatively large, rarely collected, archaic species that parasitize insect larvae, usually in wood. The single species of Austrocynipidae develops in Araucaria cones. Ronquist (1995) revised the genera of Liopteridae, and Nordlander et al. (1996) revised the species of Ibaliidae. The numerous, diverse, and yet poorly known Figitidae are endoparasitoids mostly of dipteran larvae, but also of Neuroptera (Buffington et  al. 2007), and some are hyperparasitoids of Aphididae and Psyllidae through the Chalcidoidea and Braconidae (Ferrer‐Suay et  al. 2012). The species of Cynipidae, the gall wasps and their inquilines (Liljeblad and Ronquist 1998, Ronquist et  al. 2015), are phytophagous and have been known

since ancient times because of their often conspicuous, strangely shaped, or brightly colored galls formed on various parts of plants, especially oaks and roses (Csóka et  al. 2005). Van Noort et  al. (2015) reviewed the Afrotropical Cynipoidea. Liu et al. (2007) reviewed the phylogeny and geological history of Cynipoidea. 12.9.2.8 Proctotrupoidea

This morphologically and biologically diverse superfamily consists of seven extant families, of which the Proctotrupidae contains most of the species. The remainder (Heloridae, Pelecinidae, Peradaeniidae, Proctorenyxidae, Roproniidae, and Vanhorniidae) are small, relict families, each with few species. The Proctotrupidae (Townes and Townes 1981) are parasitoids of beetle larvae in soil or rotting wood. The Heloridae parasitize larvae of lacewings. Johnson and Musetti (1999) revised the species of Pelecinidae, which parasitize June beetles, and Johnson (1992) cataloged the Proctotrupoidea s.l., the Platygas­ troidea (excluding Platygastridae), and the Ceraphronoidea. 12.9.2.9 Platygastroidea

The species of this superfamily are usually small and most (except Platygastrinae) are egg parasitoids. Masner (1976) and Masner and Huggert (1989) provided keys to the genera of the Scelionidae (when it was still treated as a family) and part of the Platygastridae, respectively. Although generic concepts have changed considerably since then, no updated keys are yet available. Austin et al. (2005) reviewed the current state of knowledge for the superfamily. Vlug (1995) cataloged the Platygastridae. The Telenominae, which in­clude the most important species for biological control of econo­ mically important pests, especially moths, represent the greatest taxonomic challenge. 12.9.2.10 Diaprioidea

This superfamily contains one large family, the Diapriidae, and four small families: Austroniidae, Ismaridae, Maamingidae, and Monomachidae (Sharkey et  al. 2012). Most species of the

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Diapriidae are parasitoids of flies, but some morphologically bizarre species occur in army ant or termite nests. Masner and García (2002) treated the genera of Diapriinae in the western hemisphere. The Belytinae (Diapriidae) parasitize fungus gnats and make up a huge proportion of parasitic Hymenoptera in forests at ground level. Johnson and Musetti (2004) revised the Monomachidae of the western hemisphere, which parasitize soldier flies. Early et al. (2001) treated the Maamingidae, which are restricted to New Zealand.

for Chalcidoidea as a whole and Eulophidae, one of the three largest families within the Chal­ cidoidea, respectively. Keys to chalcid genera exist for only two continents: Australia (Bouček 1988, excluding four families) and North America (Gibson et al. 1997). Noyes (2002) cataloged the world chalcid fauna and summarized the taxonomic, biological, morphological, and distributional information from more than 39,000 literature references. Aspects of chalcid morphology, biology, and economic importance for five family‐level taxa are given here.

12.9.2.11 Ceraphronoidea

Agaonidae (Agaoninae)  All the species of the

Dessart and Cancemi (1986) provided keys to the genera for the two extant families, the Megaspilidae and Ceraphronidae. Johnson and Musetti (2004) cataloged the species and summarized their biology. Species of both families parasitize hosts in several insect orders. 12.9.2.12 Chalcidoidea

This superfamily of 22 extant families (Fig. 12.4) consists mostly of small to minute parasitic wasps and has greater biological diversity than any other superfamily. Askew (1971), Bouček (1988), Gauld and Bolton (1996), and Grissell and Schauff (1997) gave general accounts of chalcid biology. Whereas most chalcids are parasitoids of insects and spiders, species in six families have reverted to plant feeding in galls or seeds (LaSalle 2005), and some are important pests. The small size of chalcids means they are mostly overlooked and relatively poorly studied despite their abundance in most habitats and their importance in biological control. Only three of the 22 families have common names: fig wasps (Agaonidae: Agaoninae), seed chalcids (Eury­ tomidae), and fairyflies (Mymaridae). Perhaps deservedly so, the chalcids are considered the most difficult group to identify to family; chalcid taxonomists themselves cannot always agree on family limits. Munro et al (2011) analyzed the phylogeny of the superfamily, using two ribosomal genes. Heraty et al. (2012) and Burks et al. (2011) did the same, using combined molecular and morphological characters

Agaoninae are obligate pollinators of the 700‐ plus species of figs (Ficus), an important component of tropical forests. The mutualistic interactions between the Agaoninae and figs are a textbook example of coevolution (Kjellberg et al. 2005). Males are wingless (Fig. 12.5b) and have some of the most unusual morphology among Hymenoptera, including slender, snake‐ like forms that literally swim inside figs and humpbacked turtle‐like forms that fight each other when females become rare. Females are winged (Fig. 12.5a) and disperse to other, conspecific fig trees, pollinating them. Thus, fig wasps are responsible for a yearly, multimillion dollar crop of Smyrna figs (Sisson 1970) and the survival of all the other fig species. However, the great majority of edible figs come from varieties of Ficus carica, the common fig, which do not require pollinators.

Eucharitidae  Members of this family are exclu-

sively parasitoids of ants. They have some of the most peculiar structural features among chalcids, with a thick, often heavily sculptured and brightly colored cuticle with bizarre backwards‐ facing protuberances on the thorax. Heraty (2002) revised the world genera and Heraty (2012) cataloged the species.

Eurytomidae  Seed chalcids attack a wide range of hosts as parasitoids or predators of insects, or as plant feeders, and sometimes as both. Gall formers in grass stems and seed feeders in various plant families include some serious pests of

12  Biodiversity of Hymenoptera

Figure 12.4  Lateral habitus views of representative families of Chalcidoidea (Hymenoptera). Top row: Tanaostigma stanleyi LaSalle (Tanaostigmatidae), Encyrtus fuscus (Howard) (Encyrtidae), Signiphora sp. (Signiphoridae). Second row: Brachymeria tibialis (Walker) (Chalcididae), Leucospis affinis Say (Leucospidae), Rotoita sp. (Rotoitidae). Third Row: Ormyrus vacciniicola Ashmead (Ormyridae), Kapala sulcifacies (Cameron) (Eucharitidae), Perilampus hyalinus Say (Perilampidae). Bottom Row: Elasmus atratus Howard (Eulophidae), Eulophus orgyiae (Fitch) (Eulophidae), Epiclerus nearcticus Yoshimoto (Tetracampidae). Images by Klaus Bolte. (See color plate section for the color representation of this figure.)

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(a)

(b)

Figure 12.5  Pleistodontes addicotti Wiebes (Agaoninae). (a) Female. (b) Male. Images by Klaus Bolte.

a­gricultural crops, whereas those that attack the  eggs or larvae of insects are beneficial (DiGiulio 1997). Mymaridae  Fairyflies are well named because of their minute size and delicate, long‐fringed wings. They are the most commonly collected chalcids, presumably because almost all parasitize host eggs, the most abundant stage of their host insects. The diminutive 0.13 mm long males of Dicopomorpha echmepterygis Mock­ ford (Fig. 12.1) are wingless and eyeless, their antennal segments are coalesced into melon‐ shaped blobs, their mouthparts have apparently vanished leaving only a hole, their tarsi are lost, and the only part of the pretarsus that remains is the pad between the claws, greatly modified into a suction cup, presumably to hang onto

females. The smallest winged species capable of active flight is Kikiki huna Huber (Fig. 12.2) with a body length of about 0.16 mm and forewing length of about 0.18 mm for the smallest specimen (Huber and Noyes 2013). Trichogrammatidae  These minute parasitoids

of the eggs of other insects, particularly of the Lepidoptera, are best known because of the genus Trichogramma. Certain species are mass produced by the millions around the world on factitious hosts for biological control against lepidopteran pests of many crops. An entire journal was devoted to Trichogramma until it expanded its scope to include other egg parasitoids (Hertz et al. 2004). Although many aspects of Trichogramma biology are understood, the species are taxonomically well known only

12  Biodiversity of Hymenoptera

for  North America. The rest of the Tricho­ grammatidae remain poorly known. Pinto (2006) provided keys for the genera of the western hemisphere. 12.9.3 Aculeata

The Hymenoptera that sting belong here, classified in three superfamilies: Chrysidoidea, Vespoidea, and Apoidea (Brothers 1999). Pilgrim et al. (2008), however, showed that the Vespoidea are paraphyletic and proposed new relationships of the component families and subfamilies. They divided the Aculeata into eight superfamilies: Apoidea, Chrysidoidea, Formicoidea, Pompiloidea, Tiphioidea, Thyn­ noidea, and Vespoidea, based on molecular evidence. For convenience, the former subdivision (three superfamilies) is followed here. The sting is secondarily lost in most Chrysididae and various other species, so they cannot actually sting. O’Neill (2001) treated the behavior and natural history of the solitary species. Wilson (1971) treated all the social groups, with an analysis of all aspects of sociality. Despite their relatively small numbers, the approximately 13,000 truly social (eusocial) species have had a disproportionate role in human affairs, both economically and scientifically. Sociality has evolved several times in the Hymenoptera (Linksvayer and Wade 2005, Hughes et  al. 2008): once in the ants, all of which are eusocial, and the rest in the Vespoidea and Apoidea, in which a relatively small proportion are eusocial (about 1085 wasp species (Vespidae), about 1000 bee species (Apidae and Halictidae), and the genus Micro­ stigmus (Crabronidae)). Attenborough (2005) provided an entertaining account of the lives of some of them. 12.9.3.1 Chrysidoidea

This superfamily consists of three moderately species‐rich families (Bethylidae, Chrysididae, and Dryinidae) and four small, rare ones (Embolemidae, Plumariidae, Sclerogibbidae, and Scolebythidae). Azevedo (1999) gave keys to the species of Scolebythidae, all of which are

assumed to parasitize wood‐boring beetles. Olmi (1995, 2005) keyed and revised the species of Embolemidae and Sclerogibbidae, respectively. Members of these two families are ectoparasitoids of leafhoppers and related groups, and of nymphal and adult webspinners, respectively. The Plumariidae are restricted to dry areas of southern Africa and southern South America. Males are winged and females are wingless, subterranean, and rarely collected. Azevedo et al. (2011) cataloged the entire superfamily for the Malagasy subregion. Chrysididae  These insects are the peacocks of the Hymenoptera world, rivaled in brilliance only by the orchid bees (Euglossinae) and some Chalcidoidea. Most species are iridescent green, blue, or coppery‐red, or combinations of these. Rosa and Xu (2015) illustrated some of their spectacular colors. Members of the largest genus, Chrysis, with at least 1000 described species (almost half the family total), are known popularly as cuckoo wasps in North America, or gold wasps or ruby‐tailed wasps in Europe, where many species have a coppery‐red abdomen. Most species are parasitoids or cleptoparasitoids (insects that steal the prey or provisionings of another insect) in the nests of bees and other wasps, hence the name cuckoo wasp. Adults are capable of rolling into a ball when the wasp owner of a burrow they enter tries to sting them. Because they have hard cuticle and can withdraw their antennae and legs tightly against the body, they cannot be stung by the burrow owner, which grabs them by the wings and ejects them from the burrow. The Amiseginae and Loboscelidiinae (Kimsey 2012) parasitize eggs of walking sticks, and the Cleptinae parasitize sawfly prepupae. Kimsey and Bohart (1990) revised the genera and listed the species. Brothers (2011) discussed the phylogeny of the superfamily. Madl and Rosa (2012) cataloged the species of the Ethiopian region. Because cuckoo wasps are popular among collectors on account of their brilliant colors, almost 2500 references are available on the family (Agnoli and Rosa 2015).

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Dryinidae  This family contains females that are usually wingless and ant‐like, but with pincer‐ like protarsal claws, and winged males that usually lack pincer‐like claws. The species are ectoparasitoids of leafhoppers and their relatives (Olmi 1984). Bethylidae  This is the largest chrysidoid family

and consists mostly of inconspicuous, brown or black, tropical species that are common in forest litter but are also abundant in deserts. They parasitize the Lepidoptera and Co­­leoptera. Some species attack stored‐product pests and consequently may be found in homes. Sexual dimorphism is slight to extreme, and the usually wingless females can be confused with ants. Gordh and Móczár (1990) cataloged the world fauna. Carr et al. (2010) investigated the family’s phylogeny, and Alencar and Azevedo (2013) reclassified the Epyrini. The family dates back to the early Cretaceous (Azevedo and Azar 2012).

has given them the common name “cow killer” in North America. Lelej and Brothers (2008) cataloged the genera. Pompilidae  Known as spider wasps, pompilids

are commonly seen running erratically on sand or bare earth, flicking their usually dark‐colored wings. Most species are predators of spiders, including the largest ones, the tarantulas. Species of Pepsis, spectacular wasps commonly called tarantula hawks, are strongly dimorphic, and many species form complex mimicry groups, both Batesian and Müllerian. The taxonomic popularity of Pepsis has resulted in numerous species being described many times. Vardy (2000, 2002, 2006) synonymized 374 names among the 133 species treated. Waichert et al. (2015) classified the 4900 species in five subfamilies.

This superfamily contains five small, relatively rare families (Bradynobaenidae, Rhopalo­ somatidae, Sapygidae, Scoliidae, and Sierolo­ morphidae), and five large, almost ubiquitous families (Formicidae, Mutillidae, Pompilidae, Tiphiidae, and Vespidae), discussed below.

Tiphiidae  Taxonomic problems in this cosmopolitan family are similar to those of the Mutillidae because of the strong sexual dimorphism in many species. Separate keys to each sex are often needed, but these are often not congruent, such that the number of genera for males differs from that for females; the names applied to each sex also can differ (Kimsey and Wasbauer 2006). The species are solitary ectoparasitoids on larvae of soil‐dwelling beetles, especially scarabs.

Mutillidae  Members of this family are known

Vespidae  After the bees and ants, this family of

12.9.3.2 Vespoidea

as velvet ants because the usually wingless females are covered with dense, brightly colored hairs and resemble colorful ants (Manley and Pitts 2007). Velvet ants are ectoparasitoids of the enclosed larvae and pupae of other insects, especially the Aculeata. Many occur in arid areas, searching on sand for their soil‐inhabiting hosts. Because of sexual dimorphism, it is not easy to match conspecific, or even congeneric, males and females unless they are captured during mating. The separate keys to genera of males and females do not necessarily coincide. One sex often is more rarely collected than the other, so identification keys are based almost exclusively on either males or females. The powerful sting of females

wasps is the best known of the Hymenoptera because of its social species, the often spectacular paper nests (Wenzel 1998), and the ability to defend the nests by stinging. Three of the six ­recognized subfamilies  –  Vespinae or yellowjackets and hornets (Carpenter and Kojima 1997), Polistinae or paper wasps (Carpenter 1996a, b; Kojima and Carpenter 1997; Carpen­ ter 2015a, b), and Stenogastrinae or hover wasps  (Carpenter and Kojima 1996, Turillazzi 2012) – include all the social wasps, about one‐ fifth of the species. The Eumeninae, Eupara­ ginae, and Masarinae (Carpenter 2001) contain solitary species only. Although checklists or catalogs are available for the species of most subfamilies, the subfamily Eumeninae has only

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the species of the Ethiopian region cataloged (Carpenter et  al. 2009, 2010). Pickett and Carpenter (2010) summarized views on the origin of sociality in the Vespidae and provided a new phylogenetic analysis. Da Silva et al. (2014) provided further support for the single origin of eusociality in the Vespidae. Kimsey and Carpenter (2012) provided keys for the 22 North American species of the Vespinae (about 75 worldwide). Social wasps are central to the study of behavioral evolution because the Polistinae (paper wasps) mark a clear transition between solitary and highly eusocial behavior. Most observations have involved Polistes, a cosmopolitan genus of about 200 species (Turilazzi and West‐Eberhard 1996). Members of Polistes are well suited for experimental and theoretical investigations of social behavior because their relatively small, open‐colony size and ease of location (often on human constructions) allow for detailed observations (Pickett and Wenzel 2004). The solitary Eumeninae or potter wasps, so‐called because of the beautiful clay pots constructed by Eumenes, represent the largest subfamily, with more than 3500 species. Spradberry (1973) discussed the natural history of some of them. Recent generic keys exist only for the Eumeninae of the western hemisphere (Carpenter and Garcete‐Barrett 2003, Carpenter 2004). Hermes et  al. (2014) proposed a tribal classification within Eumeni­nae. The Masarinae, or pollen wasps, with about 300 species, are unusual among the Vespoidea because all provision their nests with pollen. They occur in Mediterranean and arid climates and are most diverse in southern Africa, which contains more than half of the described species (Gess 1996). Formicidae  Ants rival the bees in being the

best‐known Hymenoptera. Hölldobler and Wilson (1990) estimated 20,000 species in total, although at present there are about 15,800 valid species and subspecies (AntWeb 2015). Extant species range in size from about 1 mm (some species of Carebara) to 3 cm (males and queens of some Dorylus or driver ant species in Africa and Dinoponera species in South America). The

family is thought to have arisen in the Lower Cretaceous (Grimaldi et  al. 1997, Ward 2007). All species form colonies that vary from a few individuals to millions, depending on the species, and some supercolonies are estimated to contain hundreds of millions of individuals spread over many square kilometers. Queen ants can have extremely long lives, the record being almost 28 years in one captive colony. Bolton (1994, 2003) keyed the genera and reclassified and keyed the subfamilies and tribes, respectively. Bolton et  al. (2006) cataloged the species. Agosti and Johnson (2003) suggested new taxonomic approaches to ant taxonomy, and Ward (2007) summarized the higher classification. Three popular accounts of ants (Hölldobler and Dawson 1984; Hölldobler and Wilson 1994, 2009) illustrate their diversity. Their effect on Earth’s ecosystems and human society is immense (Majer et al. 2004, Lach and Hooper‐Bui 2010), especially in the tropics, where most species occur. Sarnat and Economo (2012) provided a taxonomic synthesis for an entire, albeit small, country (Fiji). Fisher and Cover (2009) gave a concise treatment of the genera for North America. Numerous parallels with human society have been made, including the best (agriculture) and worst (slavery, thievery, and warfare) of human activities. Different species can be: 1)  harvesters/gatherers (the seed harvester, Messor barbarus (L.), is perhaps the species referred to in Proverbs 6: 6 (Kloets and Kloets 1959)); 2)  farmers/herders (many species collect honeydew from sap‐sucking insects and protect them from predators); 3)  mushroom growers (leaf‐cutting ants make fungus gardens in their underground nests, with chemical control of unwanted fungi and garden sanitation resulting in refuse piles outside the nest); 4)  hunters/scavengers (epitomized by the army and driver ants); 5)  building engineers (epitomized by wood ants and leaf‐cutter ants).

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Passera and Aron (2005) and Wilson (2010) gave accounts of ant behavior, social organization, and evolution. Food storage using living bodies of their own species swollen with a sweet liquid that is drawn upon during times of scarcity is unique to ants. Slavery among ants usually involves one species making slaves of another, but a few species make slaves of members of their own species from different colonies. 12.9.3.3 Apoidea

Two informal groups are conveniently recognized in this superfamily, the Apiformes (sometimes called Anthophila (= flower‐loving – much too general a name)) or bees and the Spheciformes or solitary (except Microstigmus) wasps, formerly classified as Sphecoidea but now classified within the Apoidea. Debevec et al. (2012) showed that bees probably arose from within the Crabronidae, one of the spheciform families. Some of the solitary species of spheciformes are gregarious and nest in large numbers in sandy or bare soil, but generally they are poorly known. Bohart and Menke (1976) treat the classification and biology of the Spheciformes. Pulawski (2015) cataloged the species, currently classified as four families (Heterogynaeidae, Ampulicidae, Sphecidae, and Crabronidae). All the Spheci­ formes are carnivorous. Females provision their nests with a wide variety of insects, paralyzed and placed in larval cells, in holes in wood, into the ground, or in mud constructions of their own making. As predators, they are presumably beneficial, destroying many insects including potential pests. The bees are treated separately by Cardinal in volume 2.

12.10 ­Summary and Conclusions Our present knowledge of the Hymenoptera  – ants and bees in particular, but also sawflies, and parasitic, predatory, and plant‐feeding wasps  – has advanced considerably over the past 5–10 years, especially through molecular techniques and digital imagery, which have elucidated relationships among the taxa. Enor­mous gaps,

however, still exist. The taxo­nomically and bio­­ logi­ cally best‐known faunas remain those of Australia, Europe, and North America, primarily because most Hymenoptera taxonomists live in these areas, but this situation is changing as the faunas of the Neotropical and Oriental regions are being studied by taxonomists from those regions. The classification of the Hymenoptera at the family level is relatively well understood and agreed upon (except for the Chalcidoidea), although considerable debate still occurs about relationships and classification of extinct species. Species‐level taxonomy is poor to good for most Aculeata and Symphyta (at least half the species are described), particularly for the small families, but it is still abysmal for the Parasitica, particularly the larger superfamilies, in which less than 10% of the fauna is estimated to be described. For most species, especially in the Parasitica, biological knowledge is poor or absent. Conservation efforts, for bees and ants in particular, are becoming more routine (New 2012) but need to be carried out more vigorously within the larger context of habitat conservation and sustainable agriculture and forestry. So far, no recent hymenopteran is known to have gone extinct, although human activity might have reduced the numbers of many species or extirpated them from various regions (Godsoe 2004). Finally, the morphological and biological diversity, and the economic and scientific value of the Hymenoptera need more promotion so that more people can learn to appreciate and enjoy them rather than ignore or fear them.

­Acknowledgments I thank C. Azevedo (Vitória, Brazil) and D. Brothers (Pietermaritzburg, South Africa) for providing me with recent references in their groups of expertise. My colleagues A. Bennett, G. Gibson, H. Goulet, and J. Fernández‐Triana (Canadian National Collection of Insects, Arachnids and Nematodes, Agriculture and Agri‐ Food Canada, Ottawa) read a draft of this chapter and made useful suggestions and corrections.

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13 Diversity and Significance of Lepidoptera: A Phylogenetic Perspective Paul Z. Goldstein Systematic Entomology Laboratory, Plant Science Institute, Agriculture Research Service, US Department of Agriculture, c/o Smithsonian Institution, Washington, DC, USA

The Lepidoptera – moths, butterflies, and skippers – represent one of the three most species‐ rich insect orders and the largest evolutionary radiation of herbivorous animals (Scoble 1992, Wahlberg et al. 2013). The Jurassic origins of the Lepidoptera make it the youngest of the five mega‐diverse insect orders, the others being Coleoptera, Diptera, Hymenoptera and Hemiptera – all except the last united within the Holometabola. Although most lepidopterans are confined to vegetative substrates and display perhaps the narrowest collective diet breadth of these groups, most of the higher phylogenetic diversity arose in association with the diversification of flowering plants during the Cretaceous (Powell et  al. 1999, Grimaldi and Engel 2005), paralleled by the diversification and spread of mammalian predators and insect parasitoids. Their morphological, physiological, and behavioral innovations for capitalizing on chemically defended food plants and for avoiding and deterring predators have made Lepidoptera major components of the evolutionary landscape, and they represent an important nexus for studying the history of life. Lepidopteran larvae, whether exposed feeders that graze externally or concealed as leaf miners, leaf rollers, and stem borers, stand out among the holometabolous insects as conspicuous participants in the evolutionary dynamics of defensive behaviors, crypsis, and

aggressive mimicry. Ecologically, butterflies and moths constitute a primary food source for diurnal and nocturnal vertebrate insectivores, serve as hosts for innumerable specialist insect parasitoids, and have important roles as pests and pollinators, acting as both agents and objects of natural selection. Having coevolved with predators and host plants, butterflies, moths, and their larvae represent a significant component of terrestrial biodiversity, and their herbivory has influenced the evolution of plant defensive mechanisms. They are an important forum for exploring ecological and evolutionary questions surrounding the mechanics of speciation, natural selection, and mimicry, and the roles of chemistry and climate shifts in the evolution of life histories. From the societal standpoint, lepidopterans provide obvious resources, silk being perhaps the most obvious of these, but they also number among the most destructive and economically important forest and agricultural pests. Many species are candidates for combating invasive plants and, along with beetles, moths represent one of the most commonly tapped orders for biocontrol agents (Weed and Casagrande 2011). Because they respond quickly to environmental change, including climatic and atmospheric shifts and landscape alteration, Lepidoptera serve as a means of detecting systemic threats to

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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biological resources and as an early‐warning ­system for ecological degradation. They include some of the more well‐known threatened and endangered species. Butterflies and moths also include some of the most conspicuous and beautiful insects, and represent a common gateway group through which children and young adults develop an understanding of natural history and of entomology in particular. More broadly, butterflies and moths have figured prominently in religious and spiritual frameworks and as symbols of beauty, frailty, and spirit in the works of artists and writers for millennia (Nazari 2014). Yet there is a duality in how Lepidoptera are perceived. The charisma of butterflies is perhaps matched by a more mundane and darker mystique surrounding their nocturnal relatives. Beyond their banal use in metaphor (“moths to a flame”) and their association with closet and wardrobe pests, moths are often used to represent agents of the macabre in popular culture, as in films such as Silence of the Lambs or The Mothman Prophecies. Lepidopterists have embraced this mythos, generating common names and taxonomic appellations associated with darkness and death, as in “death’s‐ head hawkmoth.” Reflecting the duality of popular perception is an asymmetry in the popular understanding of lepidopteran taxonomy and diversity: butterflies are rarely understood as simply a derived subset of moths, nested within more than 40 other superfamilies. The common question “What’s the difference between butterflies and moths?” brings shudders to zoologists in the same way as asking the difference between rabbits and mammals. But most importantly for present purposes, the relationships among many of these groups, including butterflies, remain poorly understood and are often controversial. I first briefly outline the more conspicuous ways in which Lepidoptera intersect with human society via culture, agriculture, and natural resource conservation, and particularly the roles they play in the scientific study of evolutionary and ecological phenomena. Next, I review some of the current directions and challenges, ­epitomized in the study of Lepidoptera, when it comes to documenting and understanding species diversity. In

the chapter’s remaining core, I review current understanding of how species diversity is distributed across major lepidopteran groups and some of the more conspicuous biological innovations with which evolutionary bursts of diversification might have been associated – the various groups’ evolutionary highlights, so to speak, from within the context of their phylogeny as we understand it. Because lepidopteran classification remains in flux, I also highlight the more significant recent changes in classification, reflecting advances in the inference of lepidopteran phylogeny. Although the emphasis of this discussion is phylogenetic, I also stress the geographic distribution of lepidopteran species richness, and the research directions, challenges, and opportunities that a better understanding of that richness presents.

13.1 ­Relevance of Lepidoptera: Science Lepidoptera have provided signature examples of numerous biological phenomena and, in many cases, the impetus for the development of inquiry, including the physiology of metamorphosis and diapause, the existence of mimicry and aposematism, chemical ecology and coevolution, mutualisms and tri‐trophic interactions, the chemical mediation of diet breadth and dietary specialization, and the mechanics of speciation and sexual selection. Early demonstrations of natural selection were grounded in empirical research of butterflies and moths, and in many of these arenas, Lepidoptera have enjoyed sustained pre‐eminence. The discovery of lock and key mechanisms in moth genitalia (Eberhard 1985, Shapiro and Porter 1989, Mikkola 2008, reviewed by Masly 2012) and of sphragides (“chastity belts”), which are widely distributed in  butterflies (Ehrlich and Ehrlich 1978), have ­illuminated the mechanisms of sexual selection and  sperm competition, respectively. The respective roles of pheromone chemistry, ­phenology, and diurnality promise to be equally valuable in the study of disruptive selection and allochronic speciation.

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Lepidoptera have provided some of the most high‐profile examples of both diffuse and strict coevolution. The more well‐studied examples include the mimicry complex among Heliconius butterflies (Nymphalidae; Gilbert 1984, Brower 1996), dioptine prominent moths (Notodontidae; Miller 1996, 2009), and other winged insects, many of which share passion flowers (Passifloraceae) as larval hosts. Yucca and yucca moths (Prodoxidae) include some of the few demonstrable examples of strict coevolution, if not cospeciation (reviewed by Pellmyr 2003). The study of Lepidoptera has illuminated the chemical mediation of diet breadth and dietary specialization over evolutionary time, and the role of chemistry in the origins of aposematism mimetic systems. Some of these studies have in turn led to advances in our understanding of insect vision and bioacoustics in larval and adult insects. Genes responsible for butterfly vision have been shown to be under positive selection where wing patterns are involved in both Müllerian mimicry and kin recognition (Briscoe et al. 2010, Bybee et al. 2012). So‐called “singing caterpillars” (DeVries 1991) communicate with ants by means of acoustic signaling as a defense against parasitoids, and acoustic aposematism seems to have evolved independently in multiple lepidopteran groups (Brown et  al. 2007). Adult sphingid and saturniid moths have evolved means of foiling bat sonar to avoid bat predation (Barber and Kawahara 2013, Barber et al. 2015), and adults of the most diverse lepidopteran groups (Noctuoidea and Pyraloidea) are not only equipped with sonar‐detection but also, in some cases, have themselves evolved acoustic aposematism (Barber and Connor 2007, Conner and Corcoran 2012, Corcoran et  al. 2009), warding off their would‐be predators with sound instead of, or in addition to, bright colors. Because they can be sampled readily, butterflies and moths are common foci of community ecology and faunistic studies. Likewise, as they have been well‐collected and documented in many regions (especially North America and Europe), Lepidoptera from these areas are among the most readily identified and vouchered, and have

a unique role in the development of genomic collections and phylogenomic studies. In North America, DNA barcodes have been obtained for more than 95% of the macrolepidopteran fauna (Zahiri et al. 2014). To the extent that fresh specimens can be determined reliably in the field, genome‐grade tissues may be amassed more efficiently than for many invertebrate groups, and phylogenomic progress is likely to be rapid in Lepidoptera. Perhaps more than any insect group, Lepidoptera feature prominently among species under legal protection and in various conservation programs and habitat restoration projects. Although a great deal of effort and research has focused on the conservation of particular species or assemblages of butterflies and moths, Lepidoptera have an important role in highlighting systemic threats to natural areas and aiding the assessment of conservation priorities. Growing recognition of the sheer magnitude of biological diversity has necessitated a more refined approach to conservation than focusing exclusively on individual species, and Lepidoptera present themselves as useful tools, rather than simply targets, of conservation efforts. The utility of Lepidoptera in evaluating the stability of biological communities derives, in many areas, from how well known the faunas are and from the availability of comparative data to assess rarity and uniqueness. But more generally, butterflies and moths have long been recognized to respond rapidly to climate and landscape‐level changes, anthropogenic and otherwise. In the past decade, observers have noted the northward spread of species, an increase in the number of generations per year, and the contraction of species restricted to high‐altitude or montane habitats, apparently in response to climatic temperature shifts and prolongation of growing seasons (reviewed by Parmesan 2006).

13.2 ­Relevance of Lepidoptera: Society Lepidoptera account for some of the most economically and agriculturally significant examples

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of forest, agricultural, and stored‐product pests, many of them outbreak and invasive species. The accidental introduction of forest pests and our responses to them have had repercussions for native faunas. The introductions of the gypsy moth Lymantria dispar and the browntail moth Euproctis chrysorrhoea (both Erebidae), and more recently the winter moth Operophtera brumata (Geometridae), have incurred enormous costs to North American forests. The systemic non‐target impacts of pesticide deployment (e.g, of dichlorodiphenyltrichloroethane (DDT) and carbaryl (Sevin)) and of parasitoids introduced as biocontrol agents, such as the fly Compsilura concinnata (Tachinidae; Boettner et  al. 2000), have likewise been immeasurable. Caterpillars, especially those of Noctuidae, Tortricidae, and Pyraloidea, are some the most frequently intercepted agricultural pests and elicit quarantine actions on fresh produce and stored products entering the United States from abroad. Specialist lepidopteran herbivores are frequently screened in the development of biocontrol programs to target invasive plants, such as the Brazilian pepper tree Schinus terebinthifolius (Manrique et  al. 2012) and black swallow‐wort Vincetoxicum spp. (Hazelhurst et  al. 2012), the latter of which has been implicated in declines of monarch butterflies by acting as a potential oviposition sink (Casagrande and Dacey 2007). The unchecked, transcontinental spread of the pyralid moth Cactoblastis cactorum, originally employed as a biocontrol agent for prickly pear Opuntia in Australia, now threatens numerous cactus species (Stiling 2002).

13.3 ­Diversity and Diversification: A Clarification of Numbers and Challenges This chapter is devoted largely to documenting the state of our understanding of species diversity. “Biodiversity” is a term that gained popularity after Wilson (1988) used it to refer to the panoply of taxonomic, biological, and behavioral richness, but its definition has since grown

somewhat vague. As Wilson himself decried in a different context while championing the use of a more rarely used word (consilience), loss of precision accompanies popularity of usage, and words often see their intended meaning diluted through overuse. Biodiversity may have become such a word, in that its meaning  –  and relevance – are at risk of being overshadowed by its caché. Nevertheless, the quantification of biological diversity has been the subject of many empirical and theoretical works from faunistic, ecological, genetic, and phylogenetic perspectives. In view of its varied usage, I use the term biodiversity sparingly but embrace its vagueness to convey meaning that transcends raw numbers of species and includes as wide a breadth as possible of behavioral, ecological, and genetic richness. That said, and with full recognition that the meaning of biodiversity defies simple quantification, I stress that any interpretation of species richness rests ultimately on some criterion for what constitutes a species in the first place and, as is the case elsewhere in biology, such issues abound in entomology generally and in Lepidoptera particularly. The centuries‐old debate over the ontology of species has been largely metaphysical and often semantic, focused on how best to define entities assumed to have some essentialist nature beyond or independent of our detection. And as with all metaphysical debates, this one has led nowhere except to demonstrate that scientists operating under different premises inevitably reach different conclusions. Rather than perpetuate or recapitulate such discussions here, I will for the sake of clarity (and, from this point forward, brevity) presume a certain fundamental consensus on the idea that at least broadly consistent criteria for diagnosing species enable our ability to explore them scientifically and classify them efficiently. Whatever their essence, species occupy unique roles in the taxonomic hierarchy as benchmarks that differentiate the empirical, phylogenetic framework of classification from the study of microevolutionary change within populations. This distinction, while easily blurred by the increasingly routine use of molecular genetic

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tools in taxonomic and phylogenetic studies, bears directly on our appreciation of species richness in Lepidoptera, nowhere more apparently than in the use of mitochondrial DNA barcodes to identify cryptic species. In perhaps no order of insects has the use of DNA barcodes been more extensively applied than in the Lepidoptera (Hajibabaei et  al. 2006, Rougerie et al. 2014). As has been the case in other insect groups, such studies have uncovered species diversity far exceeding that already described. The focus below is confined to assessing how species diversity is distributed among recognized higher lepidopteran taxa, and how these components of lepidopteran biodiversity are associated with behavioral and morphological innovations.

13.4 ­State of Lepidopteran Systematics and Phylogenetics Biological species richness defies one‐dimensional abstraction. Our tendency as biologists is to equate evolutionary “success” with species richness, as if it reflects longevity or endurance – we often equate a net increase in speciation with some notion of collective fitness, and not simply with a propensity for rapid reproductive isolation that generates many species, but short‐lived ones. Species‐rich groups are commonly attributed to one or more evolutionary novelties or key innovations, but these are rarely tested empirically. A complementary view is that each extant species represents a historically unique entity, not only a unique collection of behaviors and adaptations but a genome that has evolved and survived the filter of extinction events and bears clues for deciphering biological and evolutionary history through its relationships with other organisms. This is the essence of comparative biology: that biological classification represents not simply a collection of unique identifiers used for determining specimens, nor simply a mnemonic system of categorization and information storage, but a set of testable hypotheses of relationships

reflecting historical events. Comparative analysis of shared behavioral, anatomical, and physiological features enables us to understand their mechanics and to disentangle independent origins of superficially similar attributes from those attributable to singular ancestral events. The historical dimension of taxonomy and classification underlies its power not only to arrange, but also to explain biological diversity, but there lingers a more one‐dimensional view of systematics as a technical discipline confined to the formulaic business of describing and naming species. As growing threats to biological diversity have been accompanied by dwindling resources available to document it, so too has concern that the pace of taxonomic progress is inadequate to document biological diversity before most of it disappears. Often, such arguments involve the so‐called taxonomic impediment as an obstruction to scientific progress. For better or worse, Lepidoptera are among those taxa at the forefront of lively discussions and debates over ways to overcome the taxonomic impediment  –  commonly misinterpreted as a shortcoming in the field of systematics, as opposed to an indication of the sheer magnitude of biological diversity remaining to be described. The past decade has seen proposals to amend or upend the Linnaean system of hierarchical classification in favor of molecular taxonomy, to bypass nomenclatural codes in favor of democratized registries, and to replace rigorous diagnoses with heuristic distance‐based measures that impede comparative analysis. Some have even used the rate of species and subspecies descriptions to argue that taxonomy is flourishing (Costello et al. 2013), again as if the endeavor of systematics is a one‐dimensional descriptive exercise devoid of empirical strength. As in other groups with conspicuously patterned organisms, butterflies and some of the more showy moth groups have received a great deal of taxonomic attention at the species level, which perhaps has diverted attention from higher‐level phylogenetic research toward what is seen as the taxonomic impediment. Although most practicing systematists have come to eschew

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the description of subspecies, historical proliferation of subspecific and infrasubspecific epithets in Lepidoptera has been conspicuous and these efforts have been viewed by some as having drained attention and potential expertise from comparative higher‐level studies. Kristensen et al. (2007) suggested that the study of higher‐level lepidopteran relationships (among superfamilies, for example) has been compromised by the group’s charisma. He articulated two mutually reinforcing tendencies in which (i) lepidopteran wing scales – the feature responsible for the beautiful but distracting color patterns  –  obscure important structures relevant to deciphering phylogenetic relationships except at the species level, and (ii) the more promising entomologists most likely to overcome this hurdle are discouraged from working on Lepidoptera because of the anti‐ intellectual stigma associated with aesthetically pleasing insects. Notwithstanding the observations of Kristensen et  al. (2007), it should be acknowledged that the difficulty encountered in generating robustly supported hypotheses of relationship among lepidopteran superfamilies has likely been amplified by the fact that much of lepidopteran evolution took place rapidly; many of the primary events were compressed, and major groups might have arisen rapidly and diversified simultaneously. Most lepidopteran superfamilies are thought to have originated in the Cretaceous, well before the extinction event that triggered the end of the Mesozoic Era roughly 66 mya. However, many of the major macroheteroceran (macrolepidopteran) superfamilies are thought to have arisen close to this mark, either in the upper stages of the Cretaceous Period or in the lower Tertiary, and most have undergone radiations in the past 60 million years, paralleling those of major flowering plant groups. Latitudinal migration of land masses, changes in atmospheric gas concentrations, and periodic ice ages are likely to have brought about shifts in lepidopteran diapause that coincided with changes in the availability of food plants, creating phenological filters. Certain species radiations might not have been simply precipitated by

evolutionary novelties in their ancestral food plants, but accelerated by changes in dominant vegetation responding to climatic change (Goldstein and Fibiger 2005), such as the origin of C4 grasses and the spread of grasslands during the Miocene (Toussaint et al. 2012). It is interesting to observe parallel debates over which side of the Cretaceous–Paleogene boundary major groups of Lepidoptera and other organisms (bats, for example) evolved. But in some cases the question is currently untestable, either because lepidopteran fossils are rare (Sohn et al. 2015) or because we cannot differentiate whether mass extinctions, the causes of mass extinctions, or the biological vacuum resulting from mass extinctions enabled the fixture of major evolutionary innovations to which species radiations are commonly attributed. We also do not know how such extinctions may have set the stage for rapid diversification within groups already equipped with the underlying mechanics for adaptation. Regardless of our ability to pinpoint such origins, it is possible to identify the relative order of events, even if rapid diversification of many dominant life forms occurred simultaneously. For this reason, molecular data have been looked to as potential saviors of lepidopteran phylogeny re-construction. And although they remain promising, methods of temporal dating has proven frustrating, and classifications based exclusively on molecular phylogenetic evidence remain suspect as long as clear morphological characters cannot be adduced to support them.

13.5 ­General Overview The considerable progress in elucidating higher‐ level relationships – establishing robust support for some of the major clades and identifying problematic “wild card” taxa as priorities for future research – has also incurred equally considerable taxonomic flux within and among superfamilies. This flux is likely to continue as the higher‐level phylogenetic arrangement remains unstable in several key areas. Few major groups of Lepidoptera have enjoyed s­ imultaneous

13  Diversity and Significance of Lepidoptera

stability in rank, composition, and higher‐level assignment (e.g., to a superfamily or infraorder). Most lepidopteran families and superfamilies described in the past 25 years, as well as major changes in rank, are scattered throughout the order. The composition and rank of groups within the Gelechioidea have been the least stable of all the superfamilies. Notwithstanding the composition of the Papilionoidea (butterflies and their relatives), flux in the recognition of family rank within the Macroheterocera has been most pronounced within the Noctuoidea. To summarize matters effectively, it is necessary first to clarify some terminology surrounding the classification of large and small moths, butterflies, and skippers. Primary divisions in traditional, pre‐Hennigian classification schemes differentiated butterflies from everything else, recognizing Rhopalocera (butterflies and skippers, bearing clubbed antennae) and paraphyletic Heterocera (moths, bearing varied antennal morphologies). These reflect popular conventions used to tell brightly colored day‐flying animals from more drab, nocturnal ones. Most of these shortcuts have numerous exceptions and oversimplify the fundamental diversity in each of these groupings. Within Heterocera, a cascade of additional groupings existed based on important but imperfect characters such as wing coupling (Jugatae versus Frenatae), wing venation (Homoneura versus Heteroneura), separation of the gonopore from the copulatory orifice (Monotrysia versus Ditrysia), and, most loosely, size (Microlepidoptera versus Macrolepidoptera). Such classifications persisted long after they were recognized as unnatural. By convention, “Microlepidoptera” refers to roughly 75% of the moth families, including all the primitive superfamilies. The prefixes “macro” and “micro” are especially confusing misnomers, given the existence of large (e.g., Hepialoidea) moths within the primitive superfamilies traditionally thought of as micros and the diversity of small moths (e.g., Micronoctuinae) in multiple superfamilies of higher Ditrysia. Because the placement of butterflies has remained unstable, the term “Macrolepidoptera” has gradually fallen out of

usage and been replaced by “Macroheterocera,” reflecting the removal of butterflies. One large superfamily, the Pyraloidea, remains terminologically or colloquially orphaned in this scheme, considered neither macrolepidopteran (except by some microlepidopterists) nor microlepidopteran (except by some macrolepidopterists). Although the composition of Macroheterocera has been ambiguous with respect to other groups (e.g., Drepanoidea, Doidae, and Mimallonidae), it seems to have stabilized (Regier et  al. 2013; Table 13.1). The more well‐supported traditional groupings of Lepidoptera have corresponded to conspicuous but not necessarily unreversed morphological features. To the extent that our understanding of these features has been refined, they continued to form the foundation for lepidopteran classification. Major morphological innovations that we interpret as uniquely derived correspond to synapomorphies for a series of subordinal, infraordinal, and rankless clade names applied to nested, progressively less‐ inclusive groups of one or more superfamilies (Fig. 13.1, Table 13.1). Many of the major morphological innovations are associated with adult and larval feeding habits (morphology of the haustellum or proboscis, and endophytophagy versus external feeding in larvae); wing venation (primitively homoneurous, or identical in configuration between fore‐ and hindwings versus the more derived heteroneurous condition); wing‐coupling mechanisms (e.g., the presence of forewing jugum in homoneurous moths versus retinaculo‐frenate mechanisms in higher Lepidoptera); the mechanics of the reproductive system; and, within higher Lepidoptera, the configuration of tympanal ears. Many of the gross anatomical novelties occurred early in the evolution of the order: the evolution of the haustellum in the glossatan superfamilies from mandibulate ancestors; of modified wing scales in the ancestral Coelolepida and the musculated haustellum preceding innovations associated with differentiated flight mechanics and wing‐coupling mechanisms in the Heteroneura; and the massive radiation accompanying the origin of the

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Table 13.1  Classification of the Lepidoptera. Order LEPIDOPTERA Linnaeus, 1758

No. of genera No. of spp.

Suborder ZEUGLOPTERA Chapman, 1917 (1 superfamily) 1

Micropterigoidea Herrich‐Schäffer, 1855 (265 spp.) 1

Micropterigidae Herrich‐Schäffer, 1855

21

265

1

2

1

10

5

30

1

1

2

5

1

6

4

14

Suborder AGLOSSATA Speidel, 1977 (1 superfamily) 2

Agathiphagoidea Kristensen, 1967 (2 spp.) 2

Agathiphagidae Kristensen, 1967

Clade ANGIOSPERMIVORA Regier et al., 2015 Suborder HETEROBATHMIINA Kristensen & Nielsen, 1983 (1 superfamily) 3

Heterobathmioidea Kristensen & Nielsen, 1979 (10 spp.) 3

Heterobathmiidae Kristensen & Nielsen, 1979

Suborder GLOSSATA Fabricius, 1775 (6 infraorders, all following) Infraorder DACNONYPHA Hinton, 1946 (1 superfamily) 4

Eriocranioidea Rebel, 1901 (30 spp.) 4

Eriocraniidae Rebel, 1901

Clade COELOLEPIDA Nielsen & Kristensen, 1996 (5 infraorders, all following) — Superfamily unassigned (1 spp.) 5

Aenigmatineidae Kristensen & Edwards, 2015

Infraorder ACANTHOCTESIA Minet, 2002 (1 superfamily) 5

Acanthopteroctetoidea* Davis, 1978 (5 spp.) 6

Acanthopteroctetidae Davis, 1978

Infraorder LOPHOCORONINA Common, 1990 (1 superfamily) 6

Lophocoronoidea* Common, 1973 (6 spp.) 7

Lophocoronidae Common, 1973

Clade MYOGLOSSATA* Kristensen & Nielsen, 1981 (3 infraorders, all following) Infraorder NEOPSEUSTINA Davis & Nielsen, 1980 (1 superfamily) 7

Neopseustoidea Hering, 1925 (14 spp.) 8

Neopseustidae Hering, 1925

Clade NEOLEPIDOPTERA* Packard, 1895 (2 infraorders, all following) Infraorder EXOPORIA Common, 1975 (2 superfamilies) 11 8

Hepialoidea Stephens, 1829 (666 spp.) 9

Mnesarchaeidae Eyer, 1924

1

14

10

Hepialidae Stephens, 1829

69

652

13  Diversity and Significance of Lepidoptera

Table 13.1  (Continued) Order LEPIDOPTERA Linnaeus, 1758

No. of genera No. of spp.

Infraorder HETERONEURA Tillyard, 1918 (34 superfamilies, all following) Clade NEPTICULINA Meyrick, 1928 9

Nepticuloidea Stainton, 1854 (1,046 spp.) 11

Nepticulidae Stainton, 1854

13

852

12

Opostegidae Meyrick, 1893

7

194

1

3

Clade EULEPIDOPTERA Kiriakoff, 1948 Clade INCURVARIINA Börner, 1939 10 Andesianoidea Davis & Gentili, 2003 (3 spp.) 13

Andesianidae Davis & Gentili, 2003

11 Adeloidea Bruand, 1850 (583 spp.) 14

Heliozelidae Heinemann & Wocke, 1876

12

124

15

Adelidae Bruand, 1850

5

294

16

Incurvariidae Spuler, 1898

11

51

17

Cecidosidae Bréthes, 1916

5

16

18

Prodoxidae Riley, 1881

9

97

19

Tridentaformidae Davis, 2015

1

1

7

57

3

112

Clade EUHETERONEURA Regier et al., 2015 Clade ETIMONOTRYSIA* Minet, 1984 12 Palaephatoidea Davis, 1986 (57 spp.) 20

Palaephatidae Davis, 1986

13 Tischerioidea Spuler, 1898 (112 spp.) 21

Tischeriidae Spuler, 1898

Clade DITRYSIA Börner 1925 — Superfamily unassigned (104 spp.) —

Family unassigned (25 genera, 100 spp.)

25

100

22

Millieriidae Heppner, 1982

3

4

6

80

14 Tineoidea Latreille, 1810 (3,719 spp.) 23

Eriocottidae Spuler, 1898

24

Psychidae Boisduval, 1829

211

1,246

25

Tineidae Latreille, 1810

321

2,110

26

Meessiidae (Capuse, 1966)

35

248

27

Dryadaulidae Bradley, 1966

1

35

13

53

15 Gracillarioidea Stainton, 1854 (2205 spp.) 28

Roeslerstammiidae Bruand, 1850

(Continued)

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Table 13.1  (Continued) Order LEPIDOPTERA Linnaeus, 1758

No. of genera No. of spp.

29

Bucculatricidae Fracker, 1915

4

297

30

Gracillariidae Stainton, 1854

100

1,855

94

362

16 Yponomeutoidea Stephens, 1829 (1756 spp.) 31

Yponomeutidae Stephens, 1829

32

Ypsolophidae Guenée, 1845

7

163

33

Plutellidae Guenée, 1845

48

150

34

Glyphipterigidae Stainton, 1854

28

535

35

Argyresthiidae Bruand, 1850

1

157

36

Lyonetiidae Stainton, 1854

32

204

37

Attevidae Mosher, 1916

1

52

38

Praydidae Moriuti, 1977

3

47

39

Heliodinidae Heinemann & Wocke, 1876

13

69

40

Bedelliidae Meyrick, 1880

1

16

41

Scythropiidae Friese, 1966

1

1

2

29

2

4

Clade APODITRYSIA Minet, 1983 — Superfamily unassigned (1 family, 29 spp.) 42

Douglasiidae Heinemann & Wocke, 1876

17 Simaethistoidea Minet, 1991 (4 spp.) 43

Simaethistidae Minet, 1991

18 Gelechioidea Stainton, 1854 (18769 spp.) 44

Autostichidae Le Marchand, 1947

72

650

45

Lecithoceridae Le Marchand, 1947

100

1,200

46

Xyloryctidae Meyrick, 1890

60

524

47

Oecophoridae Bruand, 1850

313

3,400

48

Depressariidae (Meyrick, 1883)

114

2,300

49

Cosmopterigidae Heinemann & Wocke, 1876

135

1,792

50

Gelechiidae Stainton, 1854

507

4,700

51

Elachistidae Bruand, 1850

47

901

52

Coleophoridae Bruand, 1850

5

1,400

53

Batrachedridae Heinemann & Wocke, 1876

10

99

54

Scythrididae Rebel, 1901

30

669

55

Blastobasidae Meyrick, 1894

24

430

56

Stathmopodidae Janse, 1917

44

408

57

Momphidae Herrich‐Schäffer, 1857

6

115

58

Pterolonchidae Meyrick, 1918

2

30

59

Lypusidae Herrich‐Schäffer, 1857

3

150

60

Schistonoeidae Hodges, 1998

1

1

13  Diversity and Significance of Lepidoptera

Table 13.1  (Continued) Order LEPIDOPTERA Linnaeus, 1758

No. of genera No. of spp.

19 Alucitoidea Leach, 1815 (235 spp.) 61

Tineodidae Meyrick, 1885

12

19

62

Alucitidae Leach, 1815

9

216

90

1,318

20 Pterophoroidea Latreille, 1802 (1,318 spp.) 63

Pterophoridae Latreille, 1802

21 Carposinoidea Walsingham, 1897 (326 spp.) 64

Copromorphidae Meyrick, 1905

9

43

65

Carposinidae Walsingham, 1897

19

283

2

8

10

126

3

66

6

245

18

406

3

19

1,071

10,387

14

137

22 Schreckensteinioidea Fletcher, 1929 (8 spp.) 66

Schreckensteiniidae Fletcher, 1929

23 Epermenioidea Spuler, 1910 (126 spp.) 67

Epermeniidae Spuler, 1910

24 Urodoidea Kyrki, 1988 (66 spp.) 68

Urodidae Kyrki, 1988

25 Immoidea Common, 1979 (245 spp.) 69

Immidae Common, 1979

26 Choreutoidea Stainton, 1858 (406 spp.) 70

Choreutidae Stainton, 1858

27 Galacticoidea Minet, 1986 (19 spp.) 71

Galacticidae Minet, 1986

28 Tortricoidea Latreille, 1802 (10,387 spp.) 72

Family Tortricidae Latreille, 1802

29 Cossoidea Leach, 1815 (2,881 spp.) 73

Brachodidae Agenjo, 1966

74

Cossidae Leach, 1815

151

971

75

Dudgeoneidae Berger, 1958

6

57

76

Metarbelidae Strand, 1909

18

196

77

Ratardidae Hampson, 1898

3

10

78

Castniidae Boisduval, 1828

34

113

79

Sesiidae Boisduval, 1828

154

1,397

9

32

30 Zygaenoidea Latreille, 1809 (3,296 spp.) 80

Epipyropidae Dyar, 1903

81

Cyclotornidae Meyrick, 1912

1

5

82

Heterogynidae Rambur, 1866

1

10

83

Lacturidae Heppner, 1995

8

120

84

Phaudidae Kirby, 1892

3

15

85

Dalceridae Dyar, 1898

11

80 (Continued)

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Table 13.1  (Continued) Order LEPIDOPTERA Linnaeus, 1758

No. of genera No. of spp.

86

Limacodidae Duponchel, 1845

301

1,672

87

Megalopygidae Herrich‐Schäffer, 1855

23

232

88

Aididae Schaus, 1906

2

6

89

Somabrachyidae Hampson, 1920

4

8

90

Himantopteridae Rogenhofer, 1884

11

80

91

Zygaenidae Latreille, 1809

170

1,036

1

2

93

940

Clade OBTECTOMERA Minet, 1986 31 Whalleyanoidea Minet, 1991 (2 spp.) 92

Whalleyanidae Minet, 1991

32 Thyridoidea Herrich‐Schäffer, 1846 (940 spp.) 93

Thyrididae Herrich‐Schäffer, 1846

33 Hyblaeoidea Hampson, 1903 (18 spp.) 94

Hyblaeidae Hampson, 1903

2

18

95

Prodidactidae Epstein & Brown, 2003

1

1

7

49

32

570

34 Calliduloidea Moore, 1877 (49 spp.) 96

Callidulidae Moore, 1877

35 Papilionoidea Latreille, 1802 (18,768 spp.) 97

Papilionidae Latreille, 1802

98

Hedylidae Guenée, 1858

1

36

99

Hesperiidae Latreille, 1809

570

4,113

100 Pieridae Swainson, 1820

91

1,164

101 Riodinidae Grote, 1895 (1827)

146

1,532

102 Lycaenidae Leach, 1815

416

5,201

103 Nymphalidae Rafinesque, 1815

559

6,152

104 Pyralidae Latreille, 1809

1,056

5,921

105 Crambidae Latreille, 1810

1,018

9,666

27

194

2

6

36 Pyraloidea Latreille, 1809 (15,587 spp.)

Clade MACROHETEROCERA Chapman, 1893 37 Mimallonoidea Burmeister, 1878 (194 spp.) 106 Mimallonidae Burmeister, 1878 38 Drepanoidea Boisduval, 1828 (672 spp.) 107 Cimeliidae Chrétien, 1916 108 Doidae Donahue & Brown, 1987

2

6

109 Drepanidae Boisduval, 1828

122

660

224

1,952

39 Lasiocampoidea Harris, 1841 (1,952 spp.) 110 Lasiocampidae Harris, 1841

13  Diversity and Significance of Lepidoptera

Table 13.1  (Continued) Order LEPIDOPTERA Linnaeus, 1758

No. of genera No. of spp.

40 Bombycoidea Latreille, 1802 (4,723 spp.) 111 Apatelodidae Neumoegen & Dyar, 1894

10

145

112 Eupterotidae Swinhoe, 1892

53

339

113 Brahmaeidae Swinhoe, 1892

7

65

114 Phiditiidae Minet, 1994

4

23

115 Anthelidae Turner, 1904

9

94

116 Carthaeidae Common, 1966

1

1

117 Endromidae Boisduval, 1828

12

59

118 Bombycidae Latreille, 1802

26

185

119 Saturniidae Boisduval, 1837

169

2,349

120 Sphingidae Latreille, 1802

206

1,463

41 Geometroidea Leach, 1815 (23,749 spp.) 121 Epicopeiidae Swinhoe, 1892

9

20

122 Sematuridae Guenée,1858

6

40

123 Uraniidae Leach, 1815

90

686

124 Geometridae Leach, 1815

2,002

23,002

125 Pseudobistonidae Minet, Rajaei & Stüning 2015

1

1

42 Noctuoidea Latreille, 1809 (42,407 spp.)

Total

126 Oenosandridae Miller, 1991

4

8

127 Notodontidae Stephens, 1829

704

3,800

128 Erebidae Leach, 1815

1,760

24,569

129 Euteliidae Grote, 1882

29

520

130 Nolidae Bruand, 1847

186

1,738

131 Noctuidae Latreille, 1809

1,089

11,772

15,414

157,761

Superfamilies (42) and families (131) are numbered in bold and shaded italics, respectively. Estimates of described species and genera follow those of Nieukerken et al. (2011), variously updated from Sohn et al. (2013, Yponomeutoidea), Heikkilä et al. (2014, Gelechioidea), and Regier et al. (2012, Pyraloidea; 2013, Ditrysia; 2014, Tineoidea; 2015, non‐ditrysian superfamilies). The classification presented herein follows that of Nieukerken et al. (2011), excepting the addition of the Angiospermivora as well as certain higher‐level additions and status changes (families newly described, elevated, or synonymized) published more recently. These include the addition of the homoneurous family Aenigmotineidae (Kristensen et al. 2015) and, in the Tineoidea, of Meessiidae and Dryadaulidae, both elevated in Regier et al. 2015); in the Gelechioidea (addition of Depressariidae, redefined by Heikkilä et al. 2014); Adeloidea (addition of Tridentaformidae; Regier et al. 2015); Mnesarchaeoidea (synonymized with Hepialoidea by Regier et al. 2015); Yponomeutoidea (addition of Scythropiidae, elevated by Sohn et al. 2013); and Geometroidea (addition of Pseudobistonidae; Rajaei et al. 2015). Neither the Myoglossata nor the Neolepidoptera are recovered in the analyses of Regier et al. (2015) due to the removal of the Lophocoronoidea from a position basal to each of these groups to one adjacent to the Exoporia (Hepialoidea) and the relocation of Acanthopteroctetidae (Acanthopteroctetoidea) to within the Neopseustoidea, but we retain their arrangement in this table per Nieukerken et al. (2011) for reference. Asterisks (*) refer specifically to these departures from Regier et al. (2015) and Fig. 13.1, where the placement of Lophocoronoidea reflects Regier et al. (2015) and Acanthopteroctetoidea is retained as a superfamily and sister to the Neopseustoidea. Significant questions remain regarding superfamily assignments of certain

(Continued)

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Table 13.1  (Continued) ditrysian families (e.g., of Millieriidae) and family‐level classification, particularly within the Gelechioidea (Heikkilä et al. 2014), and with respect to the composition of Tineoidea, which seems to be paraphyletic with respect to the remaining Ditrysia in recent analyses (Regier et al. 2013, 2015). The composition of the Macroheterocera follows that of Nieukerken et al. (2011) with the addition of the Mimallonoidea, following the results of Mutanen et al. (2010) and Regier et al. (2013). The Prodidactidae were reassigned to the Hyblaeoidea by Kaila et al. (2013), and the placement of this family remains problematic. Classification problems for the Doidae are even more acute: this family was described and treated as a noctuoid but placed within the Drepanoidea by Nieukerken et al. (2011), and was united with the Mimallonidae by Regier et al. (2013). Nonetheless, the Doidae are retained as a family in the Macroheterocera.

ditrysian reproductive system followed by the appearance of exophytophagous larvae and adult tympanal organs that enabled avoidance and deterrence of predators. At this writing (November 2015), 42 superfamilies and 131 families are recognized, including eight families unassigned to superfamily (five early lepidopterans, one early Ditrysian, and two Apoditrysian; Table 13.1) and a smattering of unassigned genera. The most recent global compilation of described lepidopteran genera and species, included in the classification of Nieukerken et  al. (2011), is used as the basis for discussion below and for the numbers in Table  13.1. These do not necessarily reflect species and genera

described or synonymized since 2011. Certain family‐ and superfamily‐level rearrangements published subsequently to Nieukerken et al. (2011) have been incorporated, but not all recently published hypotheses of relationships are accommodated. Those with the most far‐reaching impacts are discussed, including the ongoing rearrangement of the Noctuoidea and the most recent discussions over the placement of butterflies (Mutanen et  al. 2010, Kawahara and Breinholdt 2014). Although a detailed treatment of each superfamily is not attempted here, a perfunctory treatment of the most diverse or conspicuous superfamilies is accompanied by selected family accounts.

Euheteroneura

Heteroneura

Palaephatoidea “MONOTRYSIA”

Eulepidoptera

DITRYSIA (154,554)

Tischerioidea Andesianoidea Adeloidea Nepticuloidea

Coelolepida Glossata Angiospermivora

Acanthopteroctetoidea Neopseustoidea Hepialoidea Lophocoronoidea Eriocranioidea Heterobathmioidea Agathiphagoidea Micropterigoidea

Figure 13.1  Phylogenetic skeleton of basal lepidopteran superfamilies, revised in part following Regier et al. (2015) but retaining Acanthopteroctetoidea and not specifying paraphyly of Palaephatoidea. (Table  13.1 provides further elaboration).

13  Diversity and Significance of Lepidoptera

13.5.1  Primitive Lepidoptera

The most phylogenetically basal of the extant lepidopteran superfamilies (Fig. 13.1) retains several primitive features, including well‐musculated mandibles as adults, lacking the fused galeae (haustellum) that unite the rest of the order; a characteristically rough, fuzzy cephalic vestiture of hair‐like scales; and folded, five‐segmented maxillary palpi (Kristensen 1999a). These basal groups comprise three superfamilies, each assigned its own suborder and each containing a single family, the most speciose of which is the Micropterigidae. The most derived of these superfamilies (Heterobathmioidea) is united with the remaining Lepidoptera under the name Angiospermivora by Regier et al. (2015). The glossatan superfamilies, almost 99.9% of the order, are united by the presence of a coilable haustellum. Primitive glossatans form a grade of six superfamilies with homoneurous wing v­enation and wing‐coupling mechanisms involving jugal lobes. The most basal of these is the Eriocranioidea, the second most diverse of the homoneurous superfamilies; its only family, Eriocraniidae, is Holarctic, with about 30 species characterized by their small size and metallic‐colored wings. Eriocraniids have micro‐trichiated wing surfaces and, along with the Acanthopteroctetoidea and the Lophocoronoidea, have haustella that lack intrinsic musculature. The Acanthopteroctetoidea contain a single family, Acanthopteroctetidae, with five species restricted to western North America. Similarly, the Lophocoronoidea contain one family, Lophocoronidae, and all six of its species are found in Australia. These two superfamilies have been grouped with the remaining Lepidoptera under the infraordinal name Coelolepida on the basis of hollow wing scales (Fig. 13.1; Kristensen 1999b). Neither of the remaining named primary clades within the homoneurous moths, Myoglossata or Neolepidoptera, has withstood recent tests of monophyly by Regier et al. (2015) based on the placement of Acanthopteroctetidae and the Lophocoronidae in more derived positions within the tree (Fig. 13.1; cf. Table 13.1). Both families had been placed by Nieukerken

et  al. (2011) outside “Myoglossata,” purportedly on the basis of a proboscis (haustellum) with intrinsic musculature, but Regier et  al. (2015) relocate the Acanthopteroctetidae within the Neopseustoidea, which previously comprised a single small family distributed in Asia, the Indian subcontinent, and western South America. Regier et al. (2015) place the Lophocoronidae as sister to the ­remaining homoneurous superfamilies, the Mnesarchaeoidea and Hepialoidea, which they synonymized under the latter name. These were traditionally assigned their own suborder (Exoporia), united by the uniquely configured female reproductive system. Female exoporians (hepialoids) have a separate gonopore and copulatory orifice, as do the ditrysian Lepidoptera, but lack an internal ductus seminalis. Spermatozoa deposited in the bursa copulatrix during mating travel along an external seminal groove between the ostium bursae and the ovipore for fertilization (Scoble 1992, Kristensen 1999b). The family Mnesarchaeidae contains fewer than 10 species, all endemic to New Zealand; the far more diverse and conspicuous exoporians are the Hepialoidea, ­ four of  whose component families (Palaeosetidae,  Prototheoridae, Neothoridae, and Anomosetidae) were synonymized by Regier et  al. (2015) under the Hepialidae, or ghost moths, which now contains more than 660 species. Hepialids are internal feeders of woody plants with drastically reduced adult mouthparts; their centers of known diversity are Australia and the Neotropics. They include some of the largest “microlepidoptera.” Exoporians form the basal branch and only homoneurous clade of the Neolepidoptera, a group putatively characterized by crochet‐bearing larval prolegs and adectitious, obtect pupae. However, the exporians were not admitted by the arrangement of Regier et al. (2015) on grounds of their paraphyletic inclusion of the Lophocoronoidea. The heteroneurous “Neolepidoptera” or Heteroneura are united by numerous features, including their wing venation, retinaculo‐frenate mechanism of wing coupling, and loss of the first abdominal sternum (Davis 1999).

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Phylogenetically, the Heteroneura (as well as the Eulepidoptea and Euheteroneura, all subtended by a common node) straddle the monotrysian and ditrysian superfamilies; the heteroneurous  monotrysians span the paraphyletic grade ­comprising the Nepticuloidea, the cosmopolitan Adeloidea (~584 species), the monobasic Andesianoidea endemic to Andean South America, and the ambiguously related Tischerioidea (trumpet moths, 110 species) and Palaephatoidea (57 species). These groups are referred to as the monotrysian heteroneura because they retain a single opening for copulation and oviposition (Davis 1999). Nepticuloids, the most basal heteroneurans, include the smallest lepidopterans, some with forewing lengths of 1.5 mm. The composite families of the Adeloidea have undergone some nomenclatural flux with the inversion of the nominotypical superfamily name from Incurvarioidea. They are, in decreasing order of species richness, the fairy longhorn moths (Adelidae, ~294 species), the Heliozelidae (123 species), the yucca moths (Prodoxidae, ~98 species), the Incurvariidae (~51 species), the Cecidosiidae (16 species), and the recently described monobasic Tridentaformidae. In the configuration of Regier et al. (2015), the Adeloidea and Andesianoidea represent the most basal branch of the Eulepidoptera, characterized in part by the presence of pilifers and precisely coupled galeae (haustellum). The Palaephatidae, which exhibit a Gondwanan ­ distribution (i.e., South America, Australia, and southern Africa), and the widespread Tischeriidae represent the most likely candidates for the sister group of the Ditrysia (Davis 1999, Wiegmann et  al. 2002), with which they are united under the name Euheteroneura by Regier et al. (2015). In contradiction with morphological evidence, Regier et  al. (2015) obtained results suggesting polyphyly of the Palaephatoidea, with South American Palaephatus sister to the Ditrysia and the couplet of Australian palaephatid genera Azaleodes and Ptyssoptera sister to the Tischerioidea, but they refrained from altering the classification pending further analyses.

13.5.2 Ditrysia

The Ditrysia are characterized by a uniquely derived female reproductive system in which a separate gonopore and copulatory orifice are linked internally via the ductus seminalis (as opposed to externally, as in the exoporian configuration) (Fig. 13.2). The Ditrysia include the traditional “Macrolepidoptera” and, with the exception of the Nepticuloidea, they include all of the superfamilies that have more than 1000 described species. The number (14) of major ditrysian superfamilies with more than 1000 species nearly matches the number of minor ones. Twenty families grouped into three diverse superfamilies – Tineoidea, Gracillarioidea, and Yponomeutoidea  –  represent the primitive Ditrysia. One primitive ditrysian family, the Millieriidae, is currently unplaced. 13.5.2.1 Tineoidea

The most diverse of the primitive ditrysian superfamilies includes the bagworms (Psychidae, ~1350 species), a cosmopolitan but primarily Old World group (Davis and Robinson 1999); the fungus moths and clothes moths in the cosmopolitan Tineidae (~2110 species); and the minor Old World family Eriocottidae (~80 species). Recent attention has resulted in the elevation of two tineid subfamilies to family status, the primarily Holarctic Meessiidae (248 species) and the cosmopolitan Dryadaulidae (Regier et al. 2015); and the description of a new monobasic family, the Aenigmatineidae from Australia (Kristensen et al. 2015). Other recent arrangements have reduced the New World family Acrolophidae to subfamily status (Acrolophinae) within the Tineidae (Regier et al. 2014). Adult tineoids are generally recognizable by virtue of dark bristles on the labial palpi; short, disassociated galeae; and erect scales on the frons. Most females bear a pair of ventral abdominal pseudapophyses on A10. The bagworms (Psychidae) are known for their tendency toward female neoteny, in the most extreme cases resulting in pupal mating, and several other features correlated with eruptive

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Noctuoidea

MACROHETEROCERA

Lasiocampoidea Bombycoidea Geometroidea Drepanoidea

OBTECTOMERA

Mimallonoidea Pyraloidea Papilionoidea Pterophoroidea Carposinoidea Epermenioidea Alucitoidea Calliduloidea Hyblaeoidea Thyridoidea Gelechioidea Zygaenoidea Cossoidea Tortricoidea

APODITRYSIA

Galacticoidea Immoidea Choreutoidea Schreckensteinioidea Urodoidea Yponomeutoidea Gracillarioidea Tineoidea

Figure 13.2  Reduction of Regier et al. (2013: figure 3), modified in part by retaining usage of Nieukerken et al. (2011) of Carposinoidea in place of Copromorphoidea. The paraphyly of Tineoidea and the polyphyly of Carposinoidea (= Copromorphoidea) and Palaephatoidea obtained in analyses of Regier et al. (2013, 2015) are not reflected; as in those studies, Whalleyanoidea and Simaethistoidea are not included.

or outbreak species, high fecundity, dispersal via larval ballooning on silken threads, and polyphagous feeding habits (Rainds et al. 2009). 13.5.2.2 Gracillarioidea

The gracillarioids represent a significant radiation of more than 2000 described species of small moths whose larvae are miners of leaves and grasses and can be of significant economic importance. Many gracillariid larvae are hypermetamorphic, with early sap‐feeding instars

exhibiting conspicuously autapomorphic features before reverting to more eruciform or caterpillar‐like forms in later stages. Gracillarioid pupae are characteristically extruded from the cocoon prior to eclosion, and adults bear spines on the abdominal terga and a smoothly scaled frons (Davis and Robinson 1999). Most of the species richness in this group is concentrated in one worldwide family, the Gracillariidae, with more than 100 genera and 1800 described species. This group is in considerable need of study.

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13.5.2.3 Yponomeutoidea

In counterpoint to the gracillarioids, this cosmopolitan superfamily of more than 1756 described species represents the earliest major radiation of moths with externally feeding larvae, distributed among 11 recognized families, including the recently elevated Scythropiidae (Sohn et al. 2013, Lewis et  al. 2015). The largest of these are the Glyphipterigidae or sedge moths (~535 species), Yponomeutidae or ermine moths (~363 species), and Lyonetiidae (~204 species). Among the smaller families is the commonly encountered and brightly colored Attevidae (webworms, ~50 species). The Plutellidae (~150 species) include web‐ building leaf skeletonizers, such as the diamondback moth Plutella xylostella L., which are pests of brassicaceous crops. Adult male yponomeutoids are usually diagnosed by unique pleural lobes surrounding the genitalia (Dugdale et al. 1999a). 13.5.3 Apoditrysia

The remaining 26 ditrysian superfamilies make up the Apoditrysia. The so‐called higher Ditrysia are characterized by shortened apodemes with enlarged bases on sternum II (Minet 1991). A phyletic grade of pre‐obtectomeran apoditrysians is made up of 14 superfamilies dominated  by Gelechioidea (~18,489 species) and Torticoidea (~10,387 species), followed in order of decreasing species richness by the Zygaenoidea (~3296 species), Cossoidea (~2881 species), and Pterophoroidea (~1318 species); the remaining nine superfamilies each contain fewer than 500 described species. The composition of the Apoditrysia remains controversial, in that the large superfamily Gelechioidea is ambiguously placed (Kaila 2004). 13.5.3.1 Gelechioidea

The most diverse of the microlepidopterans, the Gelechioidea, as currently circumscribed, includes more than 18,000 described species distributed in 17 families, the rank and classification of which have been highly unstable. If the estimate of Hodges (1999) that more than 70% of

the gelechioids remain undescribed is accurate, then the Gelechioidea might be the largest lepidopteran superfamily. The largest families are the Gelechiidae (~4700 species), Oeco­phor­idae (3308), Elachistidae (~3201), Cosmo­pterig­idae (1792), Coleo­ phor­ idae (1386), and Lecitho­ ceridae (~1200); the remaining 11 families contain under 1000 described species each. Adult gelechioids can be identified by a combination of characters, first and foremost the overlapping scales on the basal half of the haustellum. Because at least two unrelated groups (Pyraloidea and Choreutoidea) possess a similar feature, the gelechioids can be differentiated by the absence of tympanal organs (present in pyraloids) and the absence of small, naked, partially segmented maxillary palps (present in choreutids). Other gelechioid features include a smoothly scaled head and four‐segmented maxillary palpi folded and parallel with the base of the haustellum, and characteristically upturned and with an elongated third segment (Hodges 1999). Gelechioid larvae can be identified in part by the location of the subdorsal pinaculum above the spiracle on A8; in the Tortricidae the pinaculum usually is anterior to the spiracle. All of the most diverse gelechioid families and almost all the minor families are worldwide in distribution, with various centers of diversity. The Gelechiidae (twirler moths, ~4700 species) represent the largest, most economically important, and least comprehensively studied of the gelechioid families. Gelechiids are small moths with endophagous larvae identifiable in part by the colinear abdominal setae on A9. The Oecophoridae (concealer moths, ~3308 species) have a center of species richness in Australia, and include a number of economically important pests of stored grains, textiles, and various palms (Arecaceae), as well as would‐ be biocontrol agents. The Elachistidae (grass miners, ~3201 species) represent an important group of graminivorous insects with several fossil genera described from Baltic Amber; adults are usually identified by their characteristically upturned feather‐like forewing fringe. The Cosmopterigidae (~1792 species) are a family of

13  Diversity and Significance of Lepidoptera

small, ­ narrow‐winged moths concentrated in the Australian region, with larvae that feed internally on various parts of their food plants. They also include aquatic species, as in the Hawaiian endemic Hyposmocoma (Schmitz and Rubinoff 2011). The Coleophoridae (case‐bearers, ~1386 species) are concentrated in the Holarctic. Adult coleophorids are typically recognized by their visibly fringed wing margins; their larvae, as the name suggests, feed from the safety of silken cases following their early instars as internal feeders. Behaviors associated with case‐building and the morphology and architecture of the cases have been the focus of phylogenetic research (Bucheli et  al. 2002), paralleling analogous studies of cocoon‐ and case‐building in caddisflies (Weaver and Morse 1986, Wiggins and Wichard 1989, Stuart and Currie 2001). The Lecithoceridae (long‐horned moths, ~1200 species) are concentrated in the Australian and Oriental regions, and can be recognized from other gelechioid families by their long antennae and reduced or absent gnathos in the male genitalia (Park 2011). 13.5.3.2 Pterophoroidea

Of the remaining four most diverse pre‐ Obtectomeran Apoditrysia, the Pterophoroidea or plume moths are the smallest, containing a single cosmopolitan family, the Pterophoridae (~1318 species), noteworthy for their highly modified, characteristically divided wings, extremely long legs, and unique appearance at rest. Pterophorids include several important pests of ornamental plants and numerous species used in biocontrol of invasive plant species. 13.5.3.3 Tortricoidea

Notwithstanding the enigmatic genus Heliocosma (placed its own family, the Heliocosmidae, by Regier et  al. 2013), this superfamily comprises a single highly diverse and widespread family, the Tortricidae, with more than 10,300 described species grouped in three subfamilies. The Tortricoidea include more than 700 species of economically important pests, representing the highest concentration in any microlepidopteran family and the

highest taxonomic concentration of fruit and nut pests in the Lepidoptera. The most well‐known of these pests include the codling moth Cydia pomonella, the light brown apple moth Epiphyas postvittana, the European grapevine moth Lobesia botrana, and spruce budworms (Choristoneura spp.). The potential economic impacts of tortricids are as far‐reaching as the diversity of their food plants, threatening markets as varied as avocado, orange juice, and wine production. Adult tortricids are united by characteristic flat ovipositor lobes in the female genitalia (Horak 1999), but can be identified by a combination of characters that include an unscaled proboscis, rough‐scale head, porrect or horizontal three‐segmented labial palpi with a characteristically short apical segment, reduced maxillary palpi, and the presence of ocelli and chaetosemata (Horak 2006). Tortricid larvae are varied in their feeding habits, ranging from leaf rollers, flower‐ and litter‐feeders, and gall‐makers to borers of roots, fruits, and seeds. They are readily identified by the presence of a common pinaculum or saddle on A9 and the characteristic configurations of the secondary dorsal pinacula in each of the two major subfamilies, Tortricinae and Olethreutinae. These taxa overlap in their areas of concentration: the Australasian, Neotropical, and Palearctic regions for the Tortricinae versus the Nearctic, Palearctic, and Oriental regions for the Olethreutinae (Heppner 1991). 13.5.3.4 Cossoidea

The carpenter moths (Cossidae, ~971 species), clear‐winged moths (Sesiidae, ~1397 species; formerly recognized as its own superfamily Sesioidea), and giant butterfly moths (Castniidae, 113 species) include the most massive of the ­ditrysian ‘microlepidoptera’; they are stem‐ and wood borers with many of the features commonly associated with such habits, including grub‐like coloration and motile pupae that facilitate adult eclosion. Sesiids are almost all diurnal and rarely collected, except through rearing or pheromone‐ trapping efforts. The Castniidae, or giant butterfly‐moths, are likewise diurnal and are implicated in mimetic complexes involving a range of butterflies and other moths.

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13.5.3.5 Zygaenoidea

The 12 currently recognized zygaenoid families are perhaps more diverse behaviorally and morphologically than their taxonomy suggests. They include the only two lepidopteran families (Epipyropidae and Cyclotornidae) with ectoparasitic larvae, their hosts being fulgoroid planthoppers, leafhoppers, and scale insects. Many zygaenoids are chemically defended as larvae (e.g., Dalceridae, Megalopygidae, and Limacodidae), and the most diverse zygaenoid family, the Limacodidae (slug caterpillars, ~1672 species), are as fascinating for their unique larval locomotory mechanism (Epstein 1995) and striking appearance as for their urticating spines. As in the related Cossoidea, at least one major diurnal lineage within the Zygaenidae (~1036 species) has been accompanied by chemical sequestration of pyrrolizidine alkaloids, aposematism, and mimicry. The phyletic breadth of butterflies and moths associated with the Zygaenidae via Müllerian mimicry rings in Asia alone is perhaps greater than that associated with any other lepidopteran family. 13.5.4 Obtectomera

Although supported by recent molecular work, this grouping rests on weakly corroborated morphological grounds. It includes all Apoditrysia with the first four pupal abdominal segments immobile and the pulvillus in the adult pretarsus modified with a dorsal lobe (Minet 1991). Historically, these included the “pyraloid grade” of six superfamilies and the much larger Macrolepidoptera (Kristensen and Skalski 1999), but these loose groups have largely dissolved, as will be summarized following individual superfamily treatments. The phylogenetic position of the most conspicuous diurnal Lepidoptera, the butterflies and skippers (Papilionoidea), is among the more controversial. Several of the component papilionoid families have been recognized as superfamilies. It has been suggested that butterflies represent derived geometroid‐like moths, with the enigmatic Hedylidae at the center of this discussion

(Scoble 1986, Weintraub and Miller 1987). The link with hedylids was controversial when introduced, as it seemed to imply potential derivation of butterflies from Geometroidea, which would in that case have been rendered paraphyletic. The monophyly of the “Hesperioidea” was not in question; the discussion was primarily one of placement and thereby rank. Here the simplified higher classification of Nieukerken et al. (2011) is followed, in which both the skippers (Hesperiidae) and the “moth‐butterflies” (Hedylidae) accompany the five true butterfly families within the Papilionoidea instead of forming their own eponymous superfamilies. This arrangement is consistent with the phylogenetic analysis of Heikkila et al. (2012), who combined morphological characters with sequence data from eight gene regions to recover [Papilionidae + [[Hedylidae + Hesperi idae] + [Pieridae + [Nymphalidae + [Riodinidae  +  Lycaenidae]]]]. Their results suggested an early Cretaceous origin for the butterflies sensu lato, with diversification accelerating post‐ Cretaceous–Paleogene. The exclusively Neotropical Hedylidae, with fewer than 40 described species, is the smallest of these, united in part by the reduced foreleg and characteristic adult resting posture with midlegs raised (cf. Thyrididae). The diverse and cosmopolitan Hesperiidae, with more than 4000 described species, is most diverse in the tropics and includes one of the largest assemblages of lepidopterous insects associated with grasses and other commelinids, the subfamily Hesperiinae, or grass skippers. Skippers are strong flyers and, with exceptions, typically drab in coloration. They form an unambiguously supported monophyletic group, united by the wide separation of antennal bases, characteristically hooked antennae, and a narrow hind wing cell formed by the union of the R and Sc veins, among other features. Skipper caterpillars are usually characterized by tapering at either end, enhancing the appearance of the enlarged head capsules common among grass‐feeding Lepidoptera. The true butterflies include, in order of decreasing size, brush‐footed butterflies (Nymphalidae, > 6150 species described); the blues, coppers, and

13  Diversity and Significance of Lepidoptera

hairstreaks (Lycaenidae, >  5200 species); the metalmarks (Riodinidae, > 1530 species); sulphurs (Pieridae, ~1164 species); and the swallowtails (Papilionidae, 570 species). Swallowtails, so named for the modified hind wings of many species, are perhaps most conspicuous of all the butterflies. Their caterpillars are almost as well known and recognized, in part, by the presence of the post‐cephalic repugnatorial gland, the osmeterium. Swallowtails include the largest of the butterflies, the birdwings (Troidini) native to the Indian subcontinent, Southeast Asia, and Australasia, which are now listed by CITES (the Convention on International Trade in Endangered Species of Wild Fauna and Flora) and thereby heavily restricted or banned from international trade. Many papilionids feed as larvae on chemically defended hosts, for example, in the Aristolochiaceae and Apiaceae. Having evolved the ability to sequester and coopt defensive compounds such as aristolochic acid from their larval host plants, birdwings and their relatives represent a textbook example of coevolution (literally, as they feature on the cover of Futuyma’s 1986 edition of Evolutionary Biology). Other butterflies have evolved analogous strategies for exploiting allelochemicals of their host plants: glucosinolates from Brassicales in the case of Pieridae (Edger et  al. 2015); cardiac glycosides from milkweeds (Asclepiadaceae) in the case of monarchs and other Danainae (Nymphalidae) (Parsons 1965); and cyanogenic glycosides from Passiflora in the case of Heliconius (Nymphalidae) (Gilbert 1972). Whites and sulphurs (Pieridae) are worldwide in distribution excepting New Zealand; their synapomorphies include fully developed forelegs in both sexes (cf. Nymphalidae) and bifid tarsal claws, distinguishing them from papilionids. Pierid pupae are suspended with the aid of a silken girdle secured abdominally rather than thoracically as in the Papilionidae. The Riodinidae and Lycaenidae form a closely related pair of families that are worldwide in their distribution, with much of their species richness (especially that of the Riodinidae) concentrated in the Neotropics. Adult males in both families have reduced forelegs; hindwings

of riodinids exhibit a uniquely configured costa. Larvae of both families tend to be dorsolaterally compressed and have evolved unique, commonly mutualistic associations with ants, which they supply with nutrient‐rich secretions in return for defense against parasitoids (reviewed by Pierce et al. 2002). Some myrmecophilic riodinid larvae, the singing caterpillars of DeVries (1990, 1991), produce substrate‐borne sounds to communicate with ants for protection. The Nymphalidae include some of the most popular butterflies. Several nymphalids, most obviously the monarch Danaus plexippus (Danainae), but also species of the Nymphalinae, such as the red admiral Vanessa atalanta, are well‐known seasonal migrants. Nymphalids comprise the most diverse assemblage of butterflies, both in terms of species richness and in that many of its at least 12 component subfamilies were, until relatively recently, considered to be families. Now included under the umbrella name of brush‐ footed butterflies are the admirals, fritillaries, longwings, monarchs, morphos, owls, and satyrs – a cosmopolitan cluster reaching its greatest richness in the Neotropics. Nymphalids are united by a variety of wing venational characters, grooves on the antennal undersides, and with exceptions reduced or atrophied forelegs in both sexes. Larvae in the Nymphalinae tend to be spined. The primary lineages are the snout butterflies (Libytheinae); the milkweed butterflies (Danainae), including the clearwing butterflies and their relatives (Ithomiini), many of which are involved in Müllerian mimicry rings by virtue of larval sequestration of pyrrolizidine alkaloids; the longwings (Heliconiinae), including Heliconius ­ spp., which form the nexus of innumerable studies of mimicry and coevolution; the related, often mimetic Limenitidinae; the Nymphalinae and related subfamilies, an assemblage with broad host associations; and the Satyrinae and their relatives, including the owl butterflies, morphos, and satyrs, which collectively form the largest radiation of grass‐, sedge‐, and other monocot‐ feeding Lepidoptera. Relationships among the major nymphalid lineages have been studied intensively over the past decade.

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Primary among the traditional pyraloid‐grade superfamilies are the Thyridoidea, Hyblaeoidea, and Calliduloidea. Until the recent assignment of Prodidactidae to the Hyblaeoidea, each of these superfamilies included a single family of brightly colored, diurnal species. The Thyrididae are primarily pantropical with a few species in the Nearctic or Palearctic; they are readily differentiated by their characteristic wing shape and resting posture (with midlegs raised, as in the Hedylidae) (Dugdale 1999b). Like the Thyrididae, the less diverse, primarily Old World Hyblaeidae or teak moths, the primary host plants of which are within the Lamiales, can be differentiated on the basis of characters in the adult legs. Each of these families also has been included within the Pyraloidea, but as recent molecular evidence suggests, these placements are poorly supported and superfamily status is warranted. Although the Hyblaeoidea and Thyridoidea share unique modifications of the larval spinneret, Kaila et al. (2013) declined to propose a sister group relationship of the two superfamilies in recognition of apparently conflicting molecular data. The Callidulidae or butterfly‐moths are found in the Old World, primarily in the Oriental region, with an endemic species in Madagascar (Minet 1999). They are united by several features of the male and female genitalia and the adult foreleg. From a phenomenological perspective, it is among the obtectomerans where we begin to see repeated origins of bright, aposematic coloration in association with adult diurnal activity, the callidulids representing a signature example. The precise placements of the Immoidea and Carposinoidea (Carposinidae and Copromorphidae; formerly Copromorphoidea) remain uncertain. Depending on the final phylogenetic residence of the Papilionoidea, the Pyraloidea probably represent the most diverse of the obtectomeran superfamilies outside the Macroheterocera, including more than 16,000 described species, with possibly as many awaiting discovery. Pyraloids include the second largest cohort of pests (~750 species) of any lepidopteran superfamily, including rice borers, flour and meal

moths (e.g., Ephestia elutella and Plodia interpunctella), wax moths (e.g., Galleria melonella), and the European corn borer Ostrinia nubilalis. Considered neither a traditional microlepidopteran nor a true macroheteroceran superfamily, pyraloid larvae are similar to macroheterocera by virtue of having two prespiracular setae instead of the microlepidopteran three. Adult pyraloids have conspicuous maxillary palpi and, as in the two large macroheteroceran moth superfamilies, bilateral ultrasound detection organs. As in the Geometroidea, these organs are abdominal but are thought to have evolved independently, and although neither is considered homologous with the thoracic tympana characteristic of the Noctuoidea, Regier et  al. (2013) suggested the possibility that ultrasound detection in these groups might be attributable to a single evolutionary origin near the base of the Macroheterocera. The two component pyraloid families, the Pyralidae and Crambidae, the latter referred to as grass moths, are differentiated as adults by the configuration of the tympanic organ (Munroe and Solis 1999). In the Crambidae, these organs bear a praecinctorium, and the tympanum and conjunctiva are set at an oblique angle, whereas the Pyralidae have no praecinctorium and exhibit a co‐planar arrangement. The Crambidae are the more diverse in terms of species richness (roughly 9655 versus 5921 in Pyralidae; Nieukerken et al. 2011) and number of subfamilies (13 versus five; Regier et  al. 2012). The Phycitinae (~3450 species) represent the largest pyralid subfamily, and include roughly two‐thirds of the described pyralids. Taxonomically, the Crambidae are dominated by the Spilomelinae (~3767 species), Crambinae (~1987 species), and Pyraustinae (~1450 species) (Regier et al. 2012). Pyraloids are noteworthy not only for their diversity of economically important pests of graminaceous crops such as rice, corn, and sugarcane, but also for their numerous grass‐feeding and wetland‐associated species. The Crambinae make up one of the more diverse assemblages of graminivores within the Lepidoptera and include some of the few aquatic and semi‐aquatic lepidopteran larvae, as well as a number of important biocontrol

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agents that are used against invasive wetland plants. Pyralids, although less diverse, affect a broader range of resources as pests of legumes, stored grains, flours, cereals, dried fruits, and managed bee hives, and as defoliators of cultivated pines. They, too, include important biocontrol agents, for example, of prickly pear (Opuntia; Clausen 1978). 13.5.5 Macroheterocera

The remaining superfamilies have demonstrated varying degrees of compositional as well as phylogenetic instability. Neither the pyraloid grade nor the Macroheterocera seems to be stable in its arrangement; different analyses have placed the Carposinoidea and/or the Immoidea basal within the Apoditrysia (Regier et  al. 2009; Mutanen et al. 2010), and more recently the Carposinoidea firmly within the Obtectomera (Regier et  al. 2013). The uncertain placement of the Papilionoidea highlights the instability of superfamilial relationships, as does the unstable composition of the Bombycoidea/Lasiocampoidea and placement of the Drepanoidea and Mimallonoidea relative to the Geometroidea (i.e., straddling the base of the Macroheterocera). Following the treatments of Regier et al. (2009), which circumscribed Macrolepidoptera to the exclusion of butterflies (Papilionoidea), and Mutanen et al. (2010), who obtained an expanded Macrolepidoptera that included the butterflies and the Pyraloidea as well as related Thyridoidea, Hyblaeoidea, and Calliduloidea, Nieukerken et al. (2011) adopted Macroheterocera to the exclusion of the butterflies (Papilionoidea) and the sack‐ bearers (Mimallonoidea). Subsequent empirical work has retained the Mimallonoidea within the Macroheterocera (Regier et al. 2013). Both Regier et al. (2013) and Kawahara and Breinholdt (2014) retained the circumscription of the Papilionoidea by Nieukerken et  al. (2011) to include the skippers  (Hesperiidae) and the moth‐butterflies (Hedylidae), each of which had been recognized  as superfamilies. Both Regier et  al. (2009, 2013) and Kawahara and Breinholdt (2014) disassociated the butterflies from the Pyraloid grade

altogether: first as sister to a Cossoidea/Sesioidea  +  Zygaenoidea, rendering Macrolepidoptera, Apoditrysia, and Obtectomera all polyphyletic (Regier et al. 2009); next, as embedded within an assemblage of pyraloid‐grade superfamilies (Calliduloidea, Hyblaeoidea, and Thyridoidea) and pre‐obtectomeran Apoditrysian superfamilies (Pterophoroidea, Alucitoidea, and Eper­ menioidea), collectively forming a sister group to the [Pyraloidea +Macroheterocera], all within a monophyletic Obtectomera with the Gelechioidea as the sister taxon (Regier et al. 2013); and most recently as basal within a re‐composed Obtectomera that includes the Gelechioidea as follows: [[Papilionoidea + [[Gelechioidea + [Calli duloidea + Thyridoidea]] + [Pyraloidea +  [Mimallonoidea + Macroheterocera]]]] (Kawahara and Breinholdt 2014). Mutanen et al. (2010) had presented similar results, with the Papilionoidea more or less embedded within traditional microlepidopteran groups. The Bombycoidea include 10 families of large moths. The smallest families include the monotypic Carthaeidae as well as the Phiditiidae (23 species, Old World), Endromidae (59 species, Palearctic), Brahmaeidae (65 species, Old World), and Anthelidae (94 species, Australian). The remaining five range from the moderately sized Apatelodidae (145 species, New World, primarily Neotropical), Bombycidae (185 species, Old World, primarily Oriental), and Eupterotidae (339 species, Old World) to the large, diverse and cosmopolitan Sphingidae (1463 species) and Saturniidae (2349 species), the latter with its greatest diversity in the Neotropics. Except for the worldwide Saturniinae, eight of nine recognized saturniid subfamilies are continentally restricted. Perhaps with the exception of the silk moth Bombyx mori, the Saturniidae and the Sphingidae include the most well‐known and popular bombycoids, and are among the most intensively studied. Their respective life histories have been contrasted by Janzen (1984) and Bernays and Janzen (1988). Saturniids tend to be associated as larvae with the foliage of woody plants and do not feed as adults, bearing reduced

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or vestigial mouthparts and exhibiting little tendency towards long‐distance dispersal. The Hemileucinae are especially well known for their variety of defensive strategies, including urticating spines on the larvae, false eyespots on the wings, and aposematic coloration and behaviors in adults of diurnal species, possibly associated with allelochemicals synthesized de novo. Sphingids, by contrast, tend to specialize on various forbs and vines that bear either defensive allelochemicals or volatile compounds exploited by female moths as oviposition cues. Sphingids as a group are highly vagile and many are seasonal migrants; their presumably high energetic needs as adults may be met, in part, by means of highly efficient mouthparts. The existence and pollination activity of Xanthopan morgani Walker, bearing a proboscis more than 30 cm long, was predicted by Darwin and Wallace following examination of the Malagasy orchid Angraecum sesquipedale Thouars, which has an unusually long nectar‐bearing spur unreachable by other insects. Bombycoids are of economic importance in various ways. The mopane worm Gonimbrasia belina constitutes an important source of protein for indigenous southern Africans, and a significant industry surrounds its cultivation. The cultivation of the silk moth Bombyx mori (Bombycidae) is responsible for sericulture, established in China for more than 5000 years. Silk played a role in international commerce long before being smuggled from China to the Byzantine Empire during the 6th century ad. Bombyx mori is the only known truly ­domesticated insect, unable to reproduce in the wild. Although saturniids are rarely considered pests, outbreaks of the orange‐striped oakworm Anisota senatoria (Ceratocampinae) in northeastern North America and the buck moth Hemileuca maia (Hemileucinae) in southeastern North America have resulted in the localized defoliation of wild and ornamental oaks, respectively. Several sphingid species, most notably the closely related tobacco hornworm Manduca sexta and tomato hornworm Manduca quinquemaculata, are significant

farm and garden pests. Because of its size, availability, and ease in rearing, M. sexta has been used extensively as a model organism in insect physiology and neurobiology laboratories. The Lasciocampoidea, the lappet moths and tent caterpillars, include a single family of nearly 2000 species worldwide in their distribution. Lasiocampids bear similarities to bombycoids in their overall appearance, reduced mouthparts, and in many cases their size. Because of their conspicuous aggregations and tent‐forming behavior, tent caterpillars (Malacosoma spp.) are well‐known pests, especially of ornamental trees, but generally do not kill the plants on which they feed. Although many lepidopterans are gregarious as larvae, Malacosoma caterpillars were the first presocial larvae shown to use chemical recruitment trails (Fitzgerald and Peterson 1983) and have figured more prominently in the sociobiology literature than any other lepidopterans not associated with ants (Costa 2006; Fitzgerald 1995). Geometroidea and its five component families – Epicopeiidae (20 species), Sematuridae (40 species), Uraniidae (686 species), the recently described monobasic Pseudobistonidae, and the overwhelming Geometridae (>  23,000 species) – make up the second most diverse lepidopteran superfamily. The Geometroidea combined with the Noctuoidea make up more than 40% of described Lepidoptera species. In addition to the loss of abdominal prolegs, a reliable synapomorphy for geometroids is the shape of the larval labium, in which the spinneret is shorter than the prementum along its midline (Minet and Scoble 1999). Like the Pyraloidea, adult geometroids bear tympana on the first abdominal segment, but are readily distinguished from pyraloids by the unscaled proboscis and usually broad wing shape. Although diverse, the internal classification of the Geometridae is not excessively complicated relative to other comparably sized groups. The most recent work (Sihvonen et al. 2011) essentially supported the monophyly of the four major subfamilies (Ennominae, Larentiinae, Sterrhinnae, and  Geometrinae); the remaining four (Oenochrominae, Archiearinae, Desmobathrinae,

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and Orthostixinae) have not been as robustly tested, and three appear to be polyphyletic (Oenochrominae and Desmobathrinae) or, in the case of the Orthostixinae, nested within the Ennominae. Representing the second largest lepidopteran family next to the Erebidae, the Geometridae are perhaps most familiar as inchworms, so named for the loss of larval prolegs on abdominal segments 3–5 (retaining those on A6 and A10), which produces their characteristic looping gait (enabling rapid movement) and hence the appearance of measuring or meting out distance. They can be differentiated from superficially similar loopers in the Noctuidae, which have lost or vestigial prolegs on A3–4, retaining those on both A5 and A6. Adult geometroids can appear butterfly like at rest, and include many diurnal butterfly mimics. The Geometridae include few major agricultural pests but several forest pests, including the invasive winter moth Operophtera brumata L. Several geometrid groups display trends toward female aptery (winglessness), dispersing primarily through larval ballooning (Edland 1971). The geometrid genus Nemoria provided the first known example of a tannin‐induced seasonal polyphenism, in which larval mimicry of its host‐plant (oak) catkins is suppressed in late‐ season generations when the catkins are no longer in flower to aid crypsis (Greene 1989). Each of the remaining families, other than the recently described monobasic Pseudobistonidae, is made up of primarily diurnal species variously associated with swallowtail butterflies (Papilionidae) in Müllerian mimicry rings. With more than 40,000 described species and possibly as many undescribed, the Noctuoidea, currently arranged into six families, represent the most species‐rich lepidopteran superfamily, with more than 25% of described Lepidoptera. They account for the largest family cohort of pest species (>  1000), including the bollworms (Helicoverpa), the most economically important insect pests worldwide. Noctuoids are characterized by larval crochets arranged in uniordinal mesoseries and by adult thoracic tympanal

organs whose orientation varies by group. They include the prominent moths (Notodontidae, 3800 species), the owlets (Noctuidae, ~12,000 species), the tiger moths Arctiinae (~11,000 species, cosmopolitan with a Neotropical center of distribution), and the tussock moths Lymantriinae (~2800 species, nearly cosmopolitan but primarily Old World), the latter two formerly recognized as families but now grouped along with the underwings (Catocala) and other former noctuid subfamilies in the Erebidae (~25,000 species). The remaining recognized noctuoid families are the Oenosandridae (eight species, endemic to Australia), Euteliidae (520 species, cosmopolitan but primarily Afrotropical), and Nolidae (1738 species, cosmopolitan but primarily Old World tropics), the latter two of which formerly were treated as subfamilies of Noctuidae. Noctuoids are characterized by the presence of metathoracic tympanal organs and their associated structures. In the past 15 years, the Noctuoidea has undergone perhaps the most controversial taxonomic rearrangement of any superfamily, precipitated by increasing recognition that a large cohort of the Noctuidae bore significant phylogenetic affinities to the then‐recognized Arctiidae (tiger moths) and the Lymantriidae (tussock moths) (Mitchell et al. 2000, 2006; Fibiger and Lafontaine 2005; Lafontaine and Fibiger 2006). Traditionally, noctuoid families were demarcated along differences in fore‐ and hindwing venation and the configuration of tympanal organs, with the Oenosandridae and Notodontidae considered basal with respect to the remaining families on the basis of the trifid state of the forewing medial veins and the horizontally oriented thoracic tympana without counter‐tympanal hoods (Miller 1991). The remaining noctuoids exhibit a quadrifid condition in the forewing and obliquely oriented tympana with counter‐tympanal hoods. Although the noctuoids had undergone numerous rearrangements, Arctiidae and Lymantriidae remained intact as separate families while the so‐ called deltoid subfamilies (underwings and their relatives) were retained within the Noctuidae proper. These latter groups were differentiated

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from so‐called trifine noctuids in part by a quadrifine condition in the hindwing analogous to that in the forewing, and it became increasingly clear that they bore more in common with each other than with typical Noctuidae. Following an analysis of molecular data that supported earlier findings of Mitchell et al. (2006) and Weller et al. (1994), Zahiri et al. (2011) faced the alternatives of either uniting the lymantriids and arctiids within the Noctuidae to retain its monophyly, or cleaving the Noctuidae into multiple monophyletic families. Either alternative, inevitably, would render the Arctiinae and Lymantriinae as subfamilies. Rather than create a vastly expanded Noctuidae, the decision, therefore, was made to circumscribe a monophyletic Erebidae to include deltoid subfamilies as well as Arctiinae and Lymantriinae (Zahiri et al. 2011), and elevate the noctuid subfamilies Nolinae and Euteliinae to family rank. This arrangement restricts the still‐ enormous Noctuidae to a core of subfamilies bearing trifine venation, although exceptions ultimately might destabilize this classification. Recent analyses of relationships among the quadrifid noctuoid families have varied (cf. Zahiri et al. 2011, 2012, 2013a, 2013b; Yang et al. 2015). In their coverage of the Nolidae, Zahiri et al. (2013b) recovered support for the arrangement [Oenosandridae + [Notodontidae + [Eute liidae + [Erebidae + [Noctuidae + Nolidae]]]]]. Because of the widespread familiarity of noctuids sensu lato, these rearrangements have been accepted slowly. In terms of species richness, the result is that the Noctuidae have been reduced by more than 50%, from roughly 25,000 to 12,000 species, the remainder combined with Arctiinae and Lymantriinae to form the Erebidae of nearly 25,000 species or distributed within the elevated Euteliidae and Nolidae. Significant strides have been made in resolving relationships within Erebidae (Zahiri et  al. 2012) and Nolidae (Zahiri et al. 2013b). The tribal and subfamilial classification of the trifines, the Noctuidae sensu stricto, is a highly unstable taxonomic morass, but one likely to congeal in the upcoming years.

13.6 ­Needs and Challenges for Advancing Lepidopteran Studies Developing phylogenetic information is crucial to exploring an extensive range of questions. Still largely unexplored are the roles of climate shifts in the evolution of diapause, diet breadth, and life‐history timing. Broad patterns in the evolutionary lability of host associations and what mediates diet breadth have not been explored in detail. Likewise, major questions remain regarding timing of evolutionary events involving the origins of echolocation, the coevolutionary chemical arms race, the mechanics of mimicry, and the relationships between major climatic shifts and the appearance and disappearance of major moth and butterfly groups. These endeavors require insight from a wide variety of fields, including those external to entomology. Regier et  al. (2013) mention three trends: increasing body size, the transition from endophytophagy to concealed external feeding and thence to exposed external feeding, and sound detection. A fourth is a proliferation in the number of origins of diurnality and aposematism (visual and acoustic) in association with the allelochemicals synthesized de novo or coopted from chemically defended host plants. The ways in which Müllerian mimicry rings are amplified over macroevolutionary time have not been explored adequately, nor have higher‐level phylogenetic trends of co‐mimetics. But the repeated origins of similar patterns among moth and butterfly groups with widely disparate origins is noteworthy, including the ­convergence toward butterfly patterns within groups both ancestrally derived (e.g., Zygaenidae: Chalcosiinae) and more recently derived (e.g., Epicopeiidae) with respect to the butterflies themselves. At a time when advances in bioinformatics, data mining, and especially genomic research coincide with unparalleled loss of habitat, a pressing need exists for deep phylogenetic research, basic alpha taxonomy, and faunal inventory alike.

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Genomic data will be crucial for elucidating relationships among lepidopteran groups, but will need to be coupled with careful comparative work to better understand the origins of insect‐life histories and how they reflect the history of the planet. Such efforts also will be crucial for stabilizing nomenclature across continents where closely related species have been isolated in monobasic genera (Mikkola et al. 1991). And so, although it will be critical to accelerate the pace of evolutionary research, systematics requires greater use of and more rigorous analyses of even rudimentary molecular genetic data, such as DNA barcodes, not simply for purposes of raw description but for formal diagnostic purposes. For Lepidoptera, and insects in general, the age of discovery is far from over. Major groups of small and large moths alike might have fewer than 50% of their species described. Even with the integration of molecular data for purposes of discovery and description (Goldstein and DeSalle 2011), the documentation of life‐history information required to answer evolutionary and ecological questions is both daunting and even more time sensitive than the collection of specimen material. Unfortunately, dwindling resources might not be adequate to maintain existing natural history collections that make phylogenetic and evolutionary research possible. As the pace of scholarship enables empirical and analytical shortcuts, it will be important to ensure that the novelty of genomic data does not fuel the confusion of phylogenetic systematics with simple nomenclature (Costello et  al. 2013; cf. de Carvalho et  al. 2013). Although a growing number of tools have been developed and are being brought to bear on entomological research generally and systematic and taxonomic work in particular, systematic entomology is struggling with an increasingly rarefied professional climate and dwindling funding resources at a time when biological diversity is threatened more directly than ever before. If we are to be realistic, we must acknowledge that the current extinction crisis is not likely to abate,

and that many groups of organisms will one day be known only from preserved specimens and tissues. We do not suggest that systematists will assume the roles of biological morticians. Short of proposing major infrastructural overhauls to the way resources are allocated to biological research, we might at least redouble our exploratory and expeditionary efforts in the more diverse and threatened regions, adopt techniques for collecting and indefinitely preserving genomic‐grade tissues of as many taxa as possible, and mount efforts to identify diverse and under‐sampled groups and generate baseline faunistic data as efficiently as possible.

­Acknowledgments John Brown and Gary Miller reviewed drafts of this manuscript and made numerous constructive suggestions. Don Davis, Maria Heikkila, and John Brown made especially helpful suggestions on treating microlepidopteran classification.

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Butterflies. Volume 1. Evolution, Systematics, and Biogeography. Walter de Gruyter, Berlin. Dugdale, J. S., N. P. Kristensen, G. S. Robinson, and M. J. Scoble. 1999b [1998]. The smaller microlepidopterous grade superfamilies. Pp. 216–232. In N. P. Kristensen (ed). Handbuch der Zoologie/Handbook of Zoology Volume IV – Arthropoda: Insecta. Part 35: Lepidoptera, Moths and Butterflies. Volume 1. Evolution, Systematics, and Biogeography. Walter de Gruyter, Berlin. Eberhard W. G. 1985. Sexual Selection and Animal Genitalia. Harvard University Press. Cambridge, MA. 244 pp. Edger, P. P., H. M. Heidel‐Fischer, M. Bekaert, J. Rota, G. Glockner, A. E. Platts, D. G. Heckel, J. P. Der, E. K. Wafula, M. Tang, J. A. Hofberger, A. Smithson, J. C. Hall, M. Blanchette, T. E. Bureau, S. I. Wright, C. W. dePamphilis, M. E. Schranz, M. S. Barker, G. C. Conant, N. Wahlberg, H. Vogel, J. C. Pires and C. W. Wheat. 2015. The butterfly plant arms‐race escalated by gene and genome duplications. Proceedings of the National Academy of Sciences USA 112: 8362–8366. Edland, T. 1971. Wind dispersal of the winter moth larvae Operophtera brumata L. (Lep., Geometridae) and its relevance to control measures. Norsk Entomologisk Tidsskrift 18: 103–105. Ehrlich A. H. and P. R. Ehrlich. 1978. Reproductive strategies in butterflies. I. Mating frequency, plugging and egg number. Journal of the Kansas Entomological Society 51: 666–697. Epstein, M. E. 1995 [1997]. Locomotion and its evolution in caterpillars with a slug‐like ventrum (The Limacodid Group: Zygaenoidea). Journal of Research on the Lepidoptera 34: 14–20. Fibiger, M. and J. D. Lafontaine. 2005. A review of the higher classification of the Noctuoidea (Lepidoptera)—with special reference to the Holarctic fauna. Esperiana 11: 6–85. Fitzgerald, T. D. 1995. The Tent Caterpillars. Cornell University Press, Ithaca, NY. 338 pp. Fitzgerald, T. D. and S. C. Peterson. 1983. Effective recruitment by the eastern tent

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Pellmyr, O. 2003. Yuccas, yucca moths, and coevolution: a review. Annals of the Missouri Botanical Garden 90: 35–55. Pierce, N. E., M. F. Braby, A. Heath, D. J. Lohman, J. Matthew, D. B. Rand and M. A. Travassos. 2002. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annual Review of Entomology 47: 733–771. Powell, J. A., C. Mitter and B. Farrell. 1999 [1998]. Evolution of larval food preferences in Lepidoptera. Pp. 403–422. In N. P. Kristensen (ed). Handbuch der Zoologie/Handbook of Zoology Volume IV – Arthropoda: Insecta. Part 35: Lepidoptera, Moths and Butterflies. Volume 1. Evolution, Systematics, and Biogeography. Walter de Gruyter, Berlin. Rainds, M., D. R. Davis and P. W. Price. 2009. Bionomics of bagworms (Lepidoptera: Psychidae). Annual Review of Entomology 54: 209–226. Rajaei, H., C. Greve, H. Letcsh, D. Stuning, N. Wahlberg, J. Minet and B. Misof. 2015. Advances in Geometroidea phylogeny, with characterization of a new family based on Pseudobiston pinratanai (Lepidoptera, Glossata). Zoologica Scripta 44: 418–436. Regier, J. C., A. Zwick, M. P. Cummings, A. Y. Kawahara, S. Cho, S. Weller, A. Roe, J. Baixeras, J. W. Brown, C. Parr, D. R. Davis, M. Epstein, W. Hallwachs, A. Hausmann, D. H. Janzen, I. J. Kitching, M. A. Solis, S.‐H. Yen, A. L. Bazinet and C. Mitter. 2009. Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. BMC Evolutionary Biology 9: 280. Regier, J. C., C. Mitter, M. A. Solis, J. E. Hayden, B. Landry, M. Nuss, T. J. Simonsen, S.‐H. Yen, A. Zwick and M. P. Cummings. 2012. A molecular phylogeny for the pyraloid moths (Lepidoptera: Pyraloidea) and its implications for higher‐level classification. Systematic Entomology 37: 635–656. Regier, J. C., Mitter, A. Zwick, L. Bazinet, M. P. Cummings, A. Y. Kawahara, J.‐C. Sohn, D. J. Zwickl, S. Cho, D. R. Davis, J. Baixeras, J. Brown, C. Parr, S. Weller, D. C. Lees and K. T. Mitter. 2013. A large‐scale, higher‐level,

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14 The Science of Insect Taxonomy: Prospects and Needs Quentin D. Wheeler1 and Kelly B. Miller2 1 2

College of Environmental Science and Forestry, State University of New York, Syracuse, New York, USA Department of Biology, University of New Mexico, Albuquerque, New Mexico, USA

The first step in wisdom is to know the things themselves. (Carl von Linné 1735) If we and the rest of the backboned animals were to disappear overnight, the rest of the world would get on pretty well. But if they were to disappear, the land’s ecosystems would collapse. (Sir David Frederick Attenborough, Life in the Undergrowth 2005) Let us begin by stating what taxonomists under­ stand but few other scientists have yet recog­ nized, that taxonomy is to the life sciences as cosmology is to the physical sciences. Only tax­ onomists have the audacious goal of enumerat­ ing the millions of kinds of extant and extinct animals and plants and understanding the 3.8 billion‐year history of character transforma­ tions by which we may explain why these unique kinds of organisms are as they are. Unlike the Universe, the observable elements of the bio­ sphere  –  species  –  are disappearing rapidly. Unless we explore, describe, preserve in muse­ ums, and set into their rightful place in a phylo­ genetic classification Earth’s species, millions may never be known, leaving great gaps in the story of their evolutionary history and of the function of the biosphere before massive

disruption. At the current rate of extinction, an estimated 70% or more species will be gone within 300 years. If we are to learn about the history of life in significant detail, it is a now or never proposition. Although nearly all taxono­ mists are engaged in this race against time, entomologists are specially challenged along with experts on similarly megadiverse and poorly known taxa. Many mammals remain undescribed, mostly small ones such as rodents and bats, but the numbers of undescribed insects approach three orders of magnitude the number of undescribed mammals. Despite such unprecedented challenges, the prospects for insect taxonomy have never been brighter. The science of taxonomy is in the midst of transformation, undergoing remarkable theo­ retical and technological changes. No taxon spe­ cialty stands to benefit more from these advances than insect taxonomy, for the simple reasons that most living insect species are unknown to science, most “known” insect species are poorly and infrequently tested, and there are so many insect species. The translation of Hennig’s theo­ ries into English (1966) initiated a theoretical revolution, transforming Linnaean classifica­ tions and names into testable reflections of phy­ logenetic history and an improved “general reference system” (Hennig 1966, Eldredge and Cracraft 1980, Nelson and Platnick 1981, Schoch

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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1986, Schuh 2000). Hennig’s theory was built on traditional strengths of the comparative method of taxonomy, with added or enforced explicit­ ness and testability (Nelson and Platnick 1981). Although the influence of Hennig’s Phylogenetic Systematics is evident in most biological subdis­ ciplines today, his revolution is far from com­ plete, cut short by a preoccupation with molecular techniques and a focus on global par­ simony at the expense of individual character analysis (Rieppel 2004, Nelson 2004, Williams 2004, Wägele 2004, Williams and Forey 2004, Williams et  al. 2016). A return to unresolved theoretical and practical challenges associated with complex and evolutionarily interesting characters is inevitable and overdue. Taxonomy was traditionally, and should be today, as much about character analysis as it is about species descriptions, phylogeny, and classification. Molecular methods have added to the sources of data routinely synthesized by taxonomists, such as morphology, paleontology, ontogeny, and ethology (Simpson 1961), thus enriching our understanding of “holomorphology” (Hennig 1966). Molecular data are used to construct cladograms, identify species, and “fingerprint” individual organisms. Perhaps the greatest con­ tributions of molecular data are yet to come in the form of tests of complex morphological characters by unraveling the “black box” of developmental biology and bridging genome and phenotype. Wägele (2004: 116) reminds us that “complex­ ity of characters is the most significant criterion of homology.” Yet our knowledge of complex characters is limited severely. This point is high­ lighted by the recent discovery of a new organ in the mouse (Terszowski et  al. 2006), one of the most intensively anatomically studied species. Only a few insect species have received such a detailed level of study. Even if comparably detailed morphological and anatomical studies were completed for the more than 1 million named insect species, the morphology of 75% of living insect species would remain completely unknown. Morphological characters are testa­ ble because they are potentially falsified by

contradictory evidence. Although one aspect of contradiction arises from the congruence of characters on a cladogram, “contradictory evi­ dence is to be derived from a critical discussion of character hypotheses in themselves, not merely from the reciprocal relationships among all characters” (Rieppel 2004: 89). The hard work of such thoughtful comparative morphol­ ogy demands additional attention to complete the Hennigian revolution. This is so because cladistic analysis, like taxonomy generally, is as much about characters as it is about relations among species.

14.1 ­The What and Why of Taxonomy What is taxonomy? That such a question should seem necessary two and a half centuries after Linnaeus is indicative of the myths and misper­ ceptions that surround taxonomy (Wheeler and Valdecasas 2007). Without getting embroiled in formal definitions of taxonomy and systematics (Wheeler 1995a), it is fair to say that an implicit duality in taxonomy contributes to the confu­ sion. Taxonomy is, on the one hand, an informa­ tion science responsible for erecting formal classifications and maintaining names that make possible the storage, retrieval, organiza­ tion, and communication of facts about millions of species. On the other hand, taxonomy is a hypothesis‐driven science concerned with test­ able predictions about characters, character dis­ tributions, species limits, and phylogenetic relationships among species (Nelson and Platnick 1981, Wiley 1981, Schoch 1986, Schuh 2000). Many users of taxonomic information, from agriculturalists to ecologists, simply want the ability to identify species and refer to them by name. Understandably, therefore, such users are frustrated by name changes and the fact that most insect species on Earth remain unidentifi­ able (the basis of the so‐called “taxonomic impediment”). Name changes, of course, reflect improved hypotheses about species and their relationships that make Linnaean names more,

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not less, useful (Dominguez and Wheeler 1997). At root, perhaps the greatest cause for misun­ derstanding arises from the non‐experimental and historical focus of taxonomy (Nelson and Platnick 1981; Wheeler 1995a, 2004). Although this does not detract from its standing as a rig­ orously testable science (Farris 1979, Gaffney 1979, Nelson and Platnick 1981), it does seem to illuminate a misunderstanding among many experimental biologists about what is or is not science. Anticipated advances in cyberinfrastructure promise a new generation of tools with which to integrate and add efficiency to nearly every aspect of taxonomy (Atkins et  al. 2003; Page et  al. 2005; Wheeler, 2004, 2008b, 2008c). Seizing this historic development, taxonomy has the opportunity to overcome many of the limitations of the present, including constraints used as excuses for the reduction of funding for studies integrating diverse evidence. As a result, the prospects for successfully exploring the spe­ cies and character diversity of megadiverse taxa, such as insects, are better than ever  –  even in the face of imminent threats of mass species extinctions (Wilson 1985, 1992). The goals of taxonomy sound deceptively simple: to discover, describe, and critically test species; to describe and interpret the origin and diversification of their characters; to place them in classifications that reflect phylogenetic hier­ archy; to make them identifiable; to give them unambiguous names; and to make information about them reliable and accessible. Such goals, however, are not easily attained. In the case of insects, these goals seem particularly difficult. Articulating and testing the numerous hypoth­ eses associated with taxonomy (e.g., characters, species, and monophyly) represents an enor­ mous amount of currently time‐consuming work for any taxon. These challenges are magni­ fied by the sheer numbers of insect species. To put this into perspective, Grimaldi and Engel (2005) estimate that about 925,000 species of insects had been described at the time of their writing, to which we can add more than 80,000 in the decade since. Their estimate of about

3  million insect species awaiting discovery is reasonable, but conservative. Other authors suspect the number could be as much as an order of magnitude larger (e.g., Erwin 1982). Given the tempo of the biodiversity crisis and the fact that 250 years were required to describe the first 1 million species of insects, using exist­ ing tools and practices, something has to change if entomologists are going to succeed in explor­ ing insect diversity before a great number of unique species and clades have disappeared. Reasons to learn our world’s species are largely self‐evident, including the fact that sus­ tainable ecosystems and evolutionary history are comprised of species (Wheeler 1999). The ability to accurately identify species that are themselves corroborated hypotheses about homologies and character distribution is a nec­ essary prerequisite for credible research. Stated bluntly, unless species are known to science and recognizable by scientists, limited progress is possible in basic and applied biology. Prudent steps to assure our security from bioterrorism; emerging diseases of humans, plants, and ani­ mals; and the ravages of introduced pestiferous non‐native species similarly depend on reliable taxonomic information. Reasons to document species and clades soon to be extinct are equally compelling and more urgent, even if less evident to non‐taxonomists. Our ability to interpret newly discovered char­ acters (from morphology to genomics) and to continue to test and refine boundaries of species and the accuracy of phylogenies and classifica­ tions depends upon as comprehensive an under­ standing of species and character diversity as possible. Long after species are extinct in the wild, specimen and tissue collections will con­ tinue to permit taxonomists to recognize and fix mistakes and improve and refine classifications, names, and hypotheses of characters. As Hennig (1966) rightly observed, the only thing that the vast diversity of life on Earth shares in common is evolutionary history. The more comprehen­ sive our collections and complete our knowl­ edge of species, the better our classifications. A relatively complete inventory of species and

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their distributions also provides invaluable base­ line data for detecting increases or decreases in biodiversity, as well as failures and successes in conservation. We know that insects are among the most spectacularly successful living organisms. We know, too, that without reliable insect taxon­ omy, the goals of many other fields would be seriously compromised, including those of agri­ culture, vector biology, ecology, ecosystem sci­ ence, conservation biology, and genetics, to name only a few. We know that almost every process and phenomenon in nature can be approached through studies of insects and that, for many purposes, insects provide the best model organisms. Without pursuing the aims of insect taxonomy, no deep understanding of either the evolutionary history of life or ecosys­ tem functions are possible, at least for most ter­ restrial and freshwater systems. Yet, in spite of the crucial importance of advancing insect tax­ onomy, the field does not yet have suitable sup­ port for its research agenda or infrastructure, or an adequate workforce. Beyond the informed guesses of experts such as Grimaldi and Engel (2005), we do not know what or exactly how many species of insects are

living today. Although the majority of insect species are less than 10 mm in length, our igno­ rance is so great that it is not confined to small‐ sized insects. This point is made impressively by a photograph of George Beccaloni of the Natural History Museum, London, holding the largest insect ever seen on Earth, as measured in total body length (Fig. 14.1). At the time of the photograph in 2006, the specimen was of an undescribed species! Imagine the parallel in botany or vertebrate zoology – discovering the equivalent of a redwood tree or blue whale in 2006. We do not yet know enough about insect biodiversity to characterize precisely the mag­ nitude of our ignorance. Although many insects awaiting discovery are closely related to known forms, there remain, without doubt, numerous unique subclades to be brought to light. The magnitude of the challenge facing insect tax­ onomists can be appreciated by comparing the estimated several millions of undescribed insect species to the total number of species in the classes Mammalia (about 5000) and Aves (about 10,000). Theodosius Dobzhansky (1973) famously observed that: “Nothing in biology makes sense except in the light of evolution.” With millions of unknown species, there is no

Figure 14.1  A new species of insect held by George Beccaloni of London’s Natural History Museum is the longest ever recorded. Photo: courtesy of George Beccaloni.

14  The Science of Insect Taxonomy

hope of casting evolution’s light on most of life until many more insect species have been dis­ covered, described, and placed in the context of phylogenetic classifications. Advancing our knowledge of insect biodiversity is a scientific imperative. Biology is wholly dependent on taxonomy for species identifications, information retrieval, precise words with which to communicate about species and clades, and phylogenetic clas­ sifications that predict what characters to expect among species, including those not yet studied. Entomologists can anticipate that any beetle will have elytra, that any true fly will have two developed wings and anteromotorism, and that any species of Holometabola will exhibit complete metamorphosis only because insect classifications reflect phylogeny approximately correctly. Entomologists of the future, interested in the evolution of some protein, social behavior, physiological tolerance, or other feature of insects, will be dependent on the extent to which taxonomy’s agenda is fulfilled in the 21st century. The biodiversity crisis threatens much of the evidence of evolutionary history. As spe­ cies go extinct, so too goes the character evi­ dence of evolutionary history. Although it is true that specimens collected today can and will continue to be studied for hundreds of years to come, it is equally true that a growth in taxo­ nomic knowledge will make that inventory pro­ cess itself far more efficient and successful. Next to comprehensive collections, nothing is more important than non‐stop revisionary studies. Without such incessant testing, the reliability of “known” species gradually decays, and both their names and information content slowly become less reliable. Yet the biological commu­ nity forges ahead in blissful ignorance of the fact that our neglect of descriptive taxonomy is slowly eroding the things that we assume we know and obliterating our chances to explore efficiently the even greater number of species of which we know nothing. Before Hennig, insect taxonomy was some­ times viewed as little more than a service,

providing identifications and names so that other biologists could do and communicate their work. The current emphasis on molecular trees has unwittingly also reduced phylogenet­ ics to a mere service. When cladistic analyses are done as part of taxonomic research, a cen­ tral goal is the interpretation of characters and character transformations. Today, many “trees” are presented without enumerated characters because the consumers are other biologists who have some character or process of their own that they are trying to interpret in a historical context. As a mere service, these trees have become divorced from a rigorous and integra­ tive approach to taxonomy, and users as well as taxonomists are ultimately less well served. The result is that the general reference system is compromised as the results of phylogenetic analyses are no longer routinely used to improve formal classifications (Wheeler 2004, Franz 2005) or our understanding of morphology (Wheeler 2008d). Because of the frightening implications of species loss and rapid environmental change, great emphasis is appropriately placed on ecological and conservation biology studies. However, advances in ecology and conservation depend on access to taxonomic information. Unless species are known to exist and can be identified, they cannot be understood or con­ served. Because of this dependence of environ­ mental sciences on taxonomy, taxonomy is rightfully seen by many as an environmental sci­ ence. Conceptually, however, taxonomy is more evolutionary than environmental. Hypotheses about characters, species, and clades are not limited by ecosystem or epoch, but instead tran­ scend the geographic, ecological, and temporal constraints on most biological subdisciplines. Thus, taxonomists need access to all relevant museum specimens, without regard to the country or time in which those specimens were collected. The trend toward increasingly protective laws that limit the collection of specimens is a short­ sighted one deleterious to the advance of tax­ onomy. Countries that seek to close their

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borders to species explorers only succeed in assuring a greater level of ignorance about their own faunas. That is because no fauna can be understood properly if studied in isolation. Taxonomic knowledge and museum specimens should be seen and treated as intellectual prop­ erty of humanity, because no nation can do tax­ onomy to a high level of excellence without comparative studies of specimens and species found only in other countries. “Protecting” fau­ nas by prohibiting taxonomic inventories only assures the absence of the reliable taxonomic information needed to make informed and appropriate decisions and policies about the conservation and management of biodiversity. Such prohibitions on taxonomic collecting are increasingly justified on the basis of ethics: that it is wrong to kill animals great or small. Most entomologists we know respect and deeply care for the insects they study and take no pleasure in killing specimens for the sake of doing so. Rather, properly prepared specimens are essential for the advance of knowledge, and that means collecting and killing specimens for museum collections. Ironically, collecting insects is becoming difficult in many countries while the pest control industry is booming. Anyone mor­ ally opposed to killing insects has likely never had head lice or shared an urban apartment with a few thousand cockroaches. The simple fact is that a single automobile on many stretches of highway kills more insects in a given year than an insect taxonomist is likely to collect for the purpose of scientific study. So‐called “bug zap­ pers” are used in parks where entomologists are denied collecting permits, simultaneously retarding science and indiscriminately killing insects to a questionable end (Nasci et al. 1983). Unless we are prepared to ban automobile travel, concede a lion’s share of our crops to pests, and open our homes to numerous insect pests, we shall have a difficult time obtaining the moral high ground needed to oppose insect collecting for science on ethical grounds. It is not coincidental that Theodore Roosevelt was both an avid outdoorsman and the presi­ dent who championed the United States’

national park system. Because he knew and enjoyed nature intimately, he cared enough to conserve it for future generations. Similarly, children who are encouraged to make insect collections are far more likely to grow up to be voting citizens who appreciate the beauty and importance of insects and who will care whether they are conserved and represented in muse­ ums. Entomologists face simultaneously the control of the destructive minority of insect species and the conservation of the beneficial majority (Samways 2005). Museums are first and foremost taxonomic research resources. Collections are intended to be comprehensive assemblages of species and the variation within and among them. Rare and unusual species are collected preferentially. There is no pretense that collections reflect either local abundance in ecosystems or the shifting gene frequencies of concern to popula­ tion biologists; both ecology and genetics are approached through field observation and experimentation. Only taxonomy is so heavily tied to collections, as they alone afford the opportunity to compare specimens from many times and places at once. Museums provide cru­ cial historical baseline data for geographic dis­ tributions so that we may detect changes in levels of biodiversity. They are a primary data source for host associations and biogeography for most insect taxa. They are essential refer­ ences for the identification of rare species. They are the best possible documentation of biodi­ versity in general. Increasingly, we find new uses for museum specimens, from detecting heavy metals in fishes collected a century ago to retrieving DNA from rare taxa and uncovering evidence of past species distributions. With these and many other uses of collections, it is important to keep in mind their primary pur­ pose as the basis of taxonomy. The most efficient way to do taxonomy is to work in one of a handful of globally comprehen­ sive collections or to temporarily assemble a complete collection of one taxon by borrowing thousands of specimens from many museums. This will remain the case. However, with the

14  The Science of Insect Taxonomy

advent of remotely operable digital microscopes and high‐resolution digital image libraries, we can now envision a future in which type and rare specimens are potentially instantly availa­ ble for study, regardless of where on Earth they are. The current process of borrowing such fragile specimens or travelling to many cities to see them takes weeks or months. With cyberin­ frastructure, access times for specimens can be compressed to hours or minutes. International consortia of museums can coordinate their col­ lection growth and development in such a way as to be complementary, and assure that collec­ tively their holdings contain as many species and populations as possible, freeing limited time and resources from duplicative efforts. Collection development and invention of new cyberinfrastructure‐enabled tools for taxonomy depend on the recognition of the unique needs of taxonomy. Humanity, one argument goes, has survived to the present day with a fractional knowledge of insect biodiversity. So why is it so important that we document the rest of the world’s insect fauna now? Even many biologists question putting resources into naming species that will soon be extinct, arguing that funds be directed instead at saving natural places and deferring descriptive taxonomy until some future date. Environmental changes that threaten the survival of millions of species should be answer enough. It is perhaps worth observing that humanity also managed to survive for centuries believing the Earth to be flat, the Sun to revolve around the Earth, and flies to spontaneously generate from rotting meat, while being totally ignorant of atoms or molecules. Does this justify denying funding to physics, astronomy, geography, developmental biology, and molecular genetics simply because experience suggests that we could get by with­ out them? Ignorance may be survivable, but in science it is no virtue. Few other sciences are asked to be content with so much ignorance and fewer still have as much direct relevance to human and environmental welfare. No science faces the prospect of a greater loss of evidence in the decades immediately ahead.

Environments are changing so rapidly and so unpredictably around the world that the idea of conserve‐it‐first, study‐it‐later is unrealistic. How can we set conservation priorities, imple­ ment conservation plans, or even know when we have a conservation success unless we know what species exist in a given ecosystem from the outset? We might succeed in conserving a few easily recognized and putatively “key” species, but we cannot know with any certainty just how intact such systems are. Even if unlimited eco­ nomic resources existed for conservation pur­ poses, it is unlikely that we could conserve anything close to all species. The old, implicit conservation goal of maintaining the status quo is simply untenable (Wheeler, 1995b). Literally saving all species is a vacuous slogan; we face much harder decisions about which and how many species to conserve and how to undertake an ambitious inventory of species. Although many branches of biology, including taxonomy, have major parts to play in assuring the contin­ ued existence of sustainable tracts of wild places and agroecosystems, taxonomists alone bear the enormous challenge of exploring all species on a rapidly changing planet, including  –  in some senses, especially – those species soon to become extinct. Species exploration will move us closer to answers for taxonomy’s “big questions” (Cracraft 2002, Page et al. 2005), as well as countless lesser ones. At the same time, benefits will accrue to other sciences and to humanity as a whole. Among the many reasons to support a major taxonomic study of the world’s insect fauna are the following. 14.1.1  Improving Biology’s “General Reference System”

The point of phylogenetic systematic theory was to make classifications and names reflect evolutionary history. As Hennig (1966) cor­ rectly reasoned, patterns of descent with modi­ fication are the only logical organizing framework for such a general reference system. Put simply, the more species and character

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states that we know, the better, more complete, more informative, and more corroborated will be our classifications. 14.1.2  Inter‐Generational Ethics

Because no future generation will have access to as many species and clades as we do, we have a special responsibility to expand and develop collections. There is no question that this is the single most important and noble thing that we can contribute to science and humanity. Because we are aware of the challenge and capable of meeting it, we have an ethical obligation to do so. Our generation is contributing heavily to the decimation of the world’s species. While some mitigation is taking place, including a slowing of deforestation in some developing countries, our descendants will face countless challenges due to environmental change. The cost and effort to support taxonomy’s goals are not particularly great; the ignorance resulting from inaction will ultimately be far more costly in lost opportuni­ ties than any investment in taxonomy and museums. 14.1.3  Fulfilling Our Intellectual Manifest Destiny

In completing an inventory of species, we do more than assure that classifications continue to be refined. We fulfill a human intellectual mani­ fest destiny. We have as a species, from our very earliest days, practiced various levels of taxon­ omy. Initially sorting food from foe and eventu­ ally contemplating the mysteries of the origin of species. Through it all, we have been drawn by a deep intellectual curiosity about biodiversity, the patterns of similarities and differences among species, and our place in that diversity. We stand to lose priceless details about the ori­ gin and diversification of life and condemn all future generations to wonder what else we might have understood had we bothered to doc­ ument species diversity with well‐chosen museum specimens. Astronomers are rapidly providing answers to similar age‐old questions about the heavens. Unlike astronomy, the

subjects of taxonomic curiosity have a “sell‐by date” that is rapidly approaching. Anyone who questions the importance of preserving evi­ dence of species, in the form of specimens, should ask themselves how valuable it is that we know that dinosaurs ever existed. How impov­ erished would our thinking be about the origin and diversification of reptiles, birds, and mam­ mals without such fossils? We can assure that curious humans far into the future have a rea­ sonably complete snapshot of the current diver­ sity of species if we inventory, describe, and classify species today. For most of the insect species facing potential extinction, there is effectively no chance that they will leave fossils behind without our helping hand. 14.1.4  Solving Problems

Time and again we return to nature in search of solutions to problems. Almost without exception we are rewarded. Insects with their adaptations and attributes are a cornucopia of potential solutions; from biological control agents to sources of chemicals, proteins, behaviors, natural products, physiological processes, and cures for diseases, insects hold incomparable clues. The possibilities for economic returns and human welfare are almost without limit, yet we have barely scratched the surface. Why? Before access­ ing possible silks, adhesives, shellacs, and phar­ maceuticals from the insects, we must be able to identify them. To explore the properties of mil­ lions of species, one must have a roadmap; in tax­ onomy, that means a predictive classification. 14.1.5  Model Organisms

Although insects have served and continue to serve as model organisms, such as Drosophila melanogaster in genetics and evolutionary development or Manduca sexta in insect endo­ crinology, biologists have not even begun to exploit the possibilities. Interested in the evolu­ tion of social behavior? The greatest non‐human success stories are found among termites, ants, bees, and wasps. Interested in extreme phy­ siology? Desert darkling beetles can live up to

14  The Science of Insect Taxonomy

20  years in harsh deserts. Want to know more about plasticity in ontogenetic pathways? At various times, populations of Micromalthus debilis are bisexual or parthenogenetic, egg lay­ ing or live birthing, and sexually mature as adults or larvae (Pollock and Normark 2002). Curious about biogeographic history? Insects can tell us about the spatial history of evolution from scales as fine as individual islands and mountaintops to patterns tied to continental drift. Wonder about rates of evolution? Some fossils reveal insect species unchanged over millions of years, while examples exist of insects that have completed speciation since the Wisconsin glacial maxi­ mum about 12,000 years ago. 14.1.6  Molecular Tools of the Trade

Molecular data represent the first major “new” source of evidence for taxonomists. Had DNA been known and accessible to Agassiz, his three‐ part parallelism – the idea that fossils, anatomy, and ontogeny all reveal one and the same sequence of evolutionary change between ancestral and descendant species – would cer­ tainly have been a four‐part one (Bryant 1995). Among the most significant advances in insect taxonomy in recent decades is the devel­ opment of molecular data techniques, specifi­ cally access to DNA‐sequence and genomics data for inferring relationships. Although these data have largely corroborated historical hypotheses about relationships among insect taxa, in many cases they have provided evidence where few morphological synapomorphies had been found and have yielded some surprising relationships, at times overturning previously long‐held ideas (Grimaldi and Engel 2005). These advances have occurred in several ways. First, large volumes of data have become increasingly available since the advent of Sanger sequencing methods in the 1980s and 1990s. DNA sequence data provide several advantages. There is the potential availability of vast amounts of comparative data, the independence of specific molecular data from morphology, and the opportunity to model the evolution of

nucleotide substitutions. Molecular data were discovered to be no panacea, however, with many new problems arising along with their use, including issues with assessment of homol­ ogy (problems of paralogy and orthology, for example, as well as alignment of individual nucleotide positions), incongruence of gene trees and taxon trees, inadequacy of models and difficulties in testing them, and inherent prob­ lems with the data such as saturation and super­ imposed substitutions leading to unreliable results. A major problem is taxon sampling for molecular data. Great numbers of insect species are known only from a few, old museum speci­ mens that have severely degraded DNA. Also, fresh specimens may require extensive interna­ tional collecting efforts that are becoming increasingly challenging, expensive, and even dangerous – and at odds with the urgent need to collect representatives of the millions of species not yet known to science and on the brink of extinction. Sanger sequencing has been replaced by next‐ generation (Next‐Gen) sequencing techniques for larger projects, although Sanger methods continue to be used for smaller or more routine research. High‐throughput or next‐generation parallel sequencing methods have resulted in new opportunities for understanding genomics and epigenomics and promise to revolutionize our knowledge of the interaction between varia­ tion in the genome and phenotype (Pevsner 2009). These laboratory methods can poten­ tially yield vast amounts of data for phylogenetic comparisons. These advances, however, have resulted in a “data deluge” as the amounts of comparative molecular data have, in many ways, outstripped our ability to analyze, interpret, and even practically manage them (Scudellari 2011). Assembly and annotation of the data are signifi­ cant problems partly because of the sheer vol­ ume of information, but also because so little is known about most genomes, especially among megadiverse taxa such as insects. Thus, there has been a significant shift toward emphasizing data management, bioinformatics, and compu­ tation in systematics, sometimes at the expense

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of targeted empirical studies of insect systemat­ ics. These techniques are just beginning to be applied to insect studies, although the vast amounts of new data becoming available to clar­ ify insect species diversity and relationships among them is impressive. A third advance based in molecular data anal­ ysis is in the area of modelling evolutionary his­ tory in space and time, using relationships among taxa and rates of change in sequence data. Phylogenetic modelling approaches have allowed investigation into clade ages and his­ torical biogeography by calibrating nodes with fossil ages and other dating methods. Other phylogenetic modelling methods allow for test­ ing correlations of specific characters, investiga­ tion of diversification patterns and extinctions and their correlations with evolutionary innova­ tions or historical events, and coevolution of hosts and parasites or plants and herbivores, among other things. The techniques for study­ ing insect evolution have been revolutionized by the availability of molecular data and com­ puterized phylogenetic algorithms, but the questions we ask about the origins of the amaz­ ing diversity of insects remain the same. One molecular taxonomic advance is some­ what more controversial, the use of small sequence fragments for species diagnostic pur­ poses, or “DNA barcoding.” The idea is simple: that species can be diagnosed based on variabil­ ity in nucleotides. Although the most effective applications of barcodes depend on sound tax­ onomy and taxonomic expertise, the suggestion is that species identification can be possible without the need for detailed knowledge of a taxon or in the absence of typical diagnostic characters for the group (e.g., a tissue sample or a female or larval specimen when the diagnostic characters are based on adult males). Although superficially appealing, the program has signifi­ cant problems, as currently practiced, including incomplete knowledge of the comparative vari­ ation within and between species. DNA bar­ coding provides utility in certain situations, such as testing samples among taxa with a well‐­ established taxonomy. DNA barcoding in the

absence of a robust, well‐established taxonomy based on many sources of information, how­ ever, is likely to have limited utility. These tech­ niques have been advocated for species discovery (i.e., by identifying terminals of poten­ tial interest in a phylogeny or outlier popula­ tions deserving further study) or to provide links among life‐­history stages. These applica­ tions of barcoding are less controversial and are being used more routinely. 14.1.7 Aesthetics

Even conceding that beauty lies in the eye of the beholder, most people draw great inspira­ tion from the beauty of insects. Few would deny the breathtaking image of a morpho but­ terfly fluttering in the undergrowth of a tropi­ cal forest, a metallic wood‐boring beetle alit on a fallen tree, or the lace‐like wings of an owlfly by camp light. Who among us is so little a poet as to not be moved to compare the ephemeral nature of our own lives with that of a mayfly, whose adult life span is measured in fleeting minutes? As a rule, those insects that people have not appreciated are those they have never seen under the right conditions, sufficiently magnified to reveal their morphological detail, closely enough observed to unmask their remarkable behaviors. Artists, poets, authors, naturalists, hikers, gardeners, and the child in all of us will continue to marvel at the beauty of insect species for as long as they survive and, given adequately preserved collections, for much longer. 14.1.8  Creating the Vocabulary and Syntax of a Language of Biodiversity

Scientific names, the means by which we refer to hypotheses about the kinds of insects, consti­ tute the vocabulary of a taxonomic language that is sufficiently rich to enable clarity and pre­ cision when talking about millions of species. If Linnaean names are the vocabulary of this rich language, then phylogenetic classifications are its syntax, making special sense of these words

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by virtue of phylogenetic relationships among the biological entities to which they refer. This remarkable system of nomenclature, begun by Linnaeus, works so well that we sometimes take its power and necessity for granted. We should instead celebrate its incredible accomplish­ ments and potential, and push for its continued refinement. 14.1.9  Mapping the Biosphere

Imagine exploring the narrow streets of the Latin Quarter in Paris or the vast expanses of the Brazilian Amazon region without a map. Descriptive taxonomy empowers people to explore and enjoy nature on their own, up close and personal. Such experiential access to insect species engenders a visceral appreciation for biodiversity that, in turn, builds a basis for sup­ porting conservation efforts, natural history museums, and taxonomy generally.

14.2 ­Insect Taxonomy: Missions and “Big Questions” Systematics Agenda 2000 (Anonymous 1994) restated clearly the tripartite mission of taxon­ omy: to discover and describe Earth’s species; to  place species in a predictive, phylogenetic classification; and to make species, and all that is known about them, accessible. Discovering and describing species is not, as some have intimated (Janzen 1993), a one‐time process. Rather, it is a continuing, arduous process of hypothesis testing. This testing entails both the search for species new to science as well as the repeated critical testing of “known” species and their characters in light of new specimens, pop­ ulations, species, and evidence. The falsifica­ tionism of Karl Popper (1968; also Gaffney 1979, Nelson and Platnick 1981) seems simplistic for complex experimentalism, but applies far better to elegant scientific hypotheses. Taxonomy uses such elegant hypotheses almost exclusively. All or nothing statements about character distribu­ tions and clade inclusivity are the norm. Such

statements are subject to refutation as new characters and specimens are found. The second mission, predictive classification, involves the realization of Hennig’s (1966) vision of a “general reference system.” To make classifications reflect descent with modifica­ tion, taxonomists undertake cladistic analyses. Although it is technically possible for any biolo­ gist to plug data into phylogenetic software (Godfray 2007), such “analyses” rarely result in as well‐corroborated estimates of cladistic pat­ terns as when such studies are undertaken as objects of interest in and of themselves. Traditionally, the distinction is evident in the extent to which attention is paid to the analysis and interpretation of individual characters. Ontological protestations notwithstanding (de Queiroz 1988), character evidence is what sepa­ rates testable species from Roswellian extrater­ restrial life forms (e.g., Nixon and Wheeler 1990, 1992). Hennig’s (1966) admonition that how data are analyzed is more important than their source, and the tradition of including all relevant sources of data (Simpson 1961) applies still, and the best taxonomy is integrative (Will et al. 2005). I interpret the third mission, making what is known of species accessible, in two ways, both resting on the descriptive and classificatory activities in the first two missions. The first involves the application of Linnaean ranks and names in formal classifications. Such nomencla­ ture is absolutely key to clarity and precision in communication and in information search and recovery (Franz 2005). The second involves the use of the best available information systems. In the past, this meant the synthesis and interpre­ tation of taxonomic information in printed pub­ lications. It is increasingly coming to mean the use of the Web and electronic means to make information accessible. In addition to the many reasons that Linnaean classifications and names remain our best communication tool after two‐ and‐a‐half centuries (Forey 2002, Nixon et  al. 2003), Linnaean names are a superb basis for increasingly sophisticated information search strategies (Patterson et al. 2006).

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14.3 ­Insect Taxonomy’s Grand Challenge Questions The “big questions” in insect taxonomy are the same as those for taxonomy in general (Cracraft 2002, Page et al. 2005). The expansiveness of the taxonomic vision and its grand‐challenge ques­ tions are not widely appreciated. Taxonomy often deals with fine scales, enumerating the elements of ecosystems and making species identifiable at field study sites; but it deals, too, with questions on massive scales. Just as ecosystem scientists must account for global carbon budgets, taxono­ mists must account for the history of billions of characters and millions of species worldwide. Taxonomy is as much a planetary‐scale science as plate tectonics. Taxa, at least large and diverse ones, seldom recognize geopolitical, ecosystem, or continental borders. To understand a taxon is to transcend such geographic and ecological boundaries and to explore taxa across scales of time from the historic to the geologic. New tools and practices, including those on massively larger scales, are needed to gather, analyze, store, retrieve, and disseminate taxonomic information. Cyberinfrastructure, by opening access to museum specimens through images and distance microscopy, makes it possible to envision a virtual “species observatory.” With such an “instrument,” taxonomy’s big questions can be pursued on every appropriate scale. What are these big questions? 14.3.1  What Is a Species?

Insects have had a central role in theories of species and studies of speciation, and will con­ tinue to provide valuable model organisms in the refinement of our understanding of what species are and how they evolve. The compara­ tively few arguments for sympatric speciation models have been based largely on insects, and insects are among the archetypal examples of evolutionary radiations, such as Hawaii’s droso­ philids (Otte and Endler 1989). Entomologists have attempted to apply most species concepts at one time or another and have proposed several of them. The biological

species concept (BSC) was long the most widely cited concept in entomology, but this reflects (in our view) historic inertia rather than con­ vincing theoretical arguments in its favor, and we believe that its prominence has significantly begun to change. The BSC was effectively advo­ cated by architects of the “new systematics,” particularly Ernst Mayr, over a period of six dec­ ades (Mayr 1942, 1963, 2000). The concept is based on arguments about interbreeding that introduce process assumptions that today seem unnecessary to recognize species (Nelson and Platnick 1981). As Rosen (1979) observed, inter­ breeding is a shared ancestral condition that gives little insight into species divergence except through its absence. Botanists never widely accepted the BSC, and since the publication of Hennig (1966), increasing numbers of zoolo­ gists have questioned its general applicability (e.g., Wheeler and Platnick 2000). An improved version of this concept was advocated by Hennig (1966; see also Meier and Willmann 2000), but most of the concerns about the concept remain. The BSC is emblematic of a larger number of concepts, each of which makes some particular assumptions about the underlying processes associated with speciation. Although geneticists have convincingly demonstrated a range of causal factors associated with speciation (e.g., Mayr 1963, Otte and Endler 1989), it remains speculative to ascribe a process to a particular case. Recognizing species based on patterns does provide a logical starting point that is con­ sistent with some processes but inconsistent with others (Cracraft 1989). Many of the argu­ ments in the literature about species could be avoided were we to focus initially on patterns that reveal species, and then undertake studies to attempt to understand the processes that might have been responsible for their diver­ gence. A species concept exists that reliably identifies species prior to cladistic analysis and that is consistent with any speciation process. The phylogenetic species concept (PSC), as articulated by Eldredge and Cracraft (1980), Cracraft (1983), and Nelson and Platnick (1981), and restated by Nixon and Wheeler (1990, 1992)

14  The Science of Insect Taxonomy

and Wheeler and Platnick (2000), is such a concept. It is applicable to any taxon and any combination of evolutionary processes because it merely recognizes patterns of character distri­ bution that are the outcome of evolutionary his­ tory. Two concepts have vied for authority to use the name “phylogenetic species concept.” One is consistent with phylogenetic theory but not dependent on cladistic analysis (Nelson and Platnick 1981, Cracraft 1983, Nixon and Wheeler 1992, Wheeler and Platnick 2000); the other is more appropriately called the autapomorphic species concept (ASC) in that it claims (unneces­ sarily) “monophyly” for species (de Queiroz and Donoghue 1988, Mishler and Theriot 2000). An early version explicitly portrayed species as mini­ mum autapomorphic units (Hill and Crane 1982). The latter point is of some concern in current efforts to use DNA sequence data to diagnose and recognize species. All species are evolution­ arily significant groupings, but not all evolution­ arily significant groupings are species. Efforts to recognize every unusually wide gap in similarity (genetic or otherwise) as a species (e.g., Pons et al. 2006) trivializes species into simplistic for­ mulae divorced from an explicit, testable con­ cept such as the PSC. Many such efforts construct branching diagrams using cladistic methods and claim to recognize “monophyletic” groups of individuals as species. Aside from the fact that monophyly was defined by Hennig (1966) as a relationship among species  – not populations or individual organisms – two sim­ ple examples illustrate why this insistence on monophyly is misguided. First, there is no rea­ son to suppose that ancestral species do not occasionally coexist with one or more of their own daughter species. Such an ancestral species must, by definition, have apomorphies shared also by all of its descendant species. Had autapo­ morphies evolved in such an ancestral species, it would not be recognizable as an ancestor and would be treated methodologically like any other term. Only when no autapomorphies are known would it be a candidate ancestral species. Second, speciation comes about as a result of extinctions that eliminate ancestral polymorphism (Nixon

and Wheeler, 1992). Given two alternative morphs in an ancestral species and the extinc­ tion of alternate morphs in two allopatric daugh­ ter species, in what sense is one of the morphs present in a daughter species more or less apo­ morphic than the other? Additional reasons to prefer the PSC relate to applicability and testability. Because it is based on character‐distribution patterns, it is compat­ ible with all potential underlying processes, including sexual and asexual reproduction (Wheeler and Platnick 2000). The PSC is testa­ ble. Predicted character distributions are tested critically when new specimens or characters are discovered. Because the PSC recognizes the least inclusive or elemental group definable by a unique combination of characters, the PSC is a unit species concept and permits comparisons of taxa shaped by very different causal forces. It is important to evolutionary biology that varied causal factors can be compared. For example, without such a unit concept of species, it is impossible to answer questions such as: “Does asexual evolution result in greater or lesser numbers of descendant species over compara­ ble periods of evolutionary time?” Or, for that matter: “Can numbers of species in different taxa even be compared?” If species of insects mean something evolutionarily different from species of plants or microbes, what possible basis is there to compare the diversity of taxa? Arguments in favor of pluralism (e.g., Mishler and Donoghue 1982) confuse pattern and pro­ cess, supposing that different processes demand different species concepts. A simpler solution is to avoid process assumptions in species con­ cepts. This reasoning is familiar to cladists who reconstruct patterns of relative recency of com­ mon ancestry by avoiding unnecessary process assumptions (Eldredge and Cracraft 1980, Nelson and Platnick 1981). 14.3.2  What (and How Many) Insect Species Are There?

The appropriate question is “What species of insects live or have lived on Earth?” Expressing

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the question instead as “How many insect spe­ cies are there?” suggests that the important thing is some absolute number. Because such an absolute number is obviously unknowable, cyn­ ical observers may suggest that we might as well simply approximate that number by some indi­ rect measure such as overall gene divergence. Although most entomologists would confess a curiosity about that number, they know that the  number itself is not all that important. Discovering and describing as many species as possible, on the other hand, is both achievable and meaningful. To succeed in this question, we must recognize it as “big science.” This is a taxo­ nomic question, and a combination of the strengths of existing taxonomy and innovative tools and practices can solve it. We can learn much from the preliminary successes of the US  National Science Foundation’s Planetary Biodiversity Inventory (PBI) projects (Knapp 2008, Page 2008), which put together large international teams of taxon specialists and museums to accelerate species discovery and description. The result is the description or re‐ description of about 5000 species in 5 years. 14.3.3  What Is the Phylogeny of Insects?

With notable exceptions, comparative morpho­ logical, paleontological, and molecular studies have confirmed a great deal of the higher clas­ sification of insects (Grimaldi and Engel 2005). The relationships among major subdivisions of insects are demonstrably approximately cor­ rect, although some enigmatic relationships remain. For example, the position of Strepsiptera relative to other holometabolous orders has been controversial, as has the exact position of the Hymenoptera and the interrelationships among extant palaeopterous orders, although Misof et al. (2014) offer a counterpoint. Because three‐quarters of living insects are unknown and many exciting fossils continue to be discov­ ered, some surprises no doubt remain. Examples include the new order Mantophasmatodea (Grimaldi and Engel 2005) and a living species of  Lepidotrichidae, a family that was thought

to  have been extinct for millions of years (Wygodzinsky 1961). However, it is remarkable that, with several thousand new species described each year, the higher classification of insects remains largely intact. 14.3.4  What Are the Histories of Character Transformation in Insects?

Among the most intellectually challenging and rewarding aspects of taxonomy is explaining the evolutionary history of complex characters (Cracraft 1981). Insects present intricate and sometimes intuitively improbable characters in astounding abundance, making them incredibly rewarding to study. Even the sexiest questions about character evolution in insects remain controversial. For example, what is the origin of insect wings? Among all animals to have taken to flight, insects are unique in having evolved wings in addition to ancestral ambulatory appendages. The ultimate answer to this ques­ tion is likely to include clues from paleontology, developmental biology, molecular genetics, and more detailed and inclusive comparative anat­ omy and morphology. Other major events in insect evolution that demand similarly exten­ sive additional research include tagmatization, endognathy, wing flexion, male and female geni­ talia, holometaboly, and on and on. Such ques­ tions extend downward through all subclades to the species level, where incredible “leaps” some­ times are seen between closely related species. Examples of the latter include a remarkable array of sexual dimorphisms and contrivances by which insects advertise and perceive chemi­ cal signals, “songs,” and visual displays. Advances in digital technologies will soon revolutionize how morphological character data are gathered, analyzed, visualized, and communicated. 14.3.5  Where Are Insect Species Distributed?

For the vast majority of insect species, what we know of their geographic and ecological distri­ butions are recorded in a few taxonomic publi­ cations and databases and on specimen labels.

14  The Science of Insect Taxonomy

As ecology has appropriately become more quantitative and exacting, what used to be called “natural history” has fallen increasingly to tax­ onomy. It is doubtful that we will ever have the resources to complete serious ecological studies of more than a handful of insect species. Taxonomy is, therefore, complementary to ecol­ ogy, recording broad but shallow insights into insect associations, including simple co‐occur­ rences in ecological and geographic space. Insect geographic distributions matter. Within a year of the first detection of West Nile virus in the United States, it became obvious that it had the potential to spread rapidly (Rappole et  al. 2000). We must establish baseline knowledge of what insect species exist, where, and in what combinations. Otherwise, what hope do we have of efficiently detecting or monitoring pests, vectors, invasive species, instances of bioterror­ ism, or increases or decreases in biodiversity? For insects, well‐annotated voucher speci­ mens must be deposited in collections. As these collections develop and their data are made retrievable electronically, countless new appli­ cations and ways of analyzing those data will emerge. As one example, such data combined with ecological information and remote‐sensing data can support predictive modeling of inva­ sions of pest species (Roura‐Pascual et al. 2006). 14.3.6  How Have Insect Distributions Changed through Time?

Because many insects leave a sparse fossil record, detailed answers to such questions can be difficult to provide even for higher taxa. Among Pleistocene species are subfossils that have provided remarkably detailed pictures of the effect of glacial events on insect populations (e.g., Coope 1979). Chironomid heads from ancient lake sediments have provided another view of changes in insect populations and a novel way to study climate change (Brooks and Birks 2000). What is currently most crucial is establishing baseline knowledge of insect distri­ butions so that changes in the future can be detected.

14.3.7  How Can Insect Classifications and Names Be Most Predictive and Informative?

Hennig (1966) provided the theoretical answer to this question in his Phylogenetic Systematics. That referential framework is, in its most useful form, a Linnaean classification. Such phyloge­ netic classifications are highly informative (Farris 1979), and aid in both information retrieval and prediction (Nelson and Platnick 1981). The chal­ lenges ahead are more practical ones related to work on a larger and more international scale, as well as the need to add efficiency to what taxono­ mists already do well. A renewed emphasis on and support for descriptive taxonomy is imme­ diately and urgently needed.

14.4 ­Transforming Insect Taxonomy The rate at which human knowledge doubles is accelerating at a blinding speed, yet the rate at which our knowledge of Earth’s species doubles is slowing. Taxonomy must undergo a funda­ mental transformation if it is to meet the chal­ lenges of the biodiversity crisis. Put in stark terms, we have a matter of decades to discover, describe, and classify three times more insect species than we have described in the past two‐ and‐a‐half centuries. This is literally a race against time. It is a virtual certainty that many species, some the last vestiges of unique branches of the insect tree of life, will soon go extinct (Wilson 1992). Because we get only one chance to document many parts of insect life, we must get it right; we must preserve those aspects of entomological taxonomic practice that are good while accelerating its pace and adding innovations. Hennig’s revolution in taxonomy was cut short (Williams and Forey 2004). Completing it will involve a returned emphasis on charac­ ter  analysis, including morphology (Wheeler 2008d), the relationship between cladograms and Linnaean ranks and names, the adoption of

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a uniform theory of species, and the integration of all relevant sources of evidence (Will et  al. 2005). Hennig’s revolution had begun to undo the damage of the New Systematics that had attempted to recast taxonomy in the image of modern genetics (Wheeler 1995a, 2008a). A renewed emphasis on Hennig (1966), combined with cyber tools (Atkins et  al. 2003), has the potential to forge a “New Taxonomy” focused on its own agenda and strengths (Wheeler 2008c). The concept of cyber‐enabled, international, taxon‐focused “knowledge communities” is central to the transformation of taxonomy. Such “collaboratories” will build on the success of the PBI model (Knapp 2008, Page 2008) and take advantage of the potential of domain‐specific cyberinfrastructures for efficient collaboration. All science builds on prior work, of course, but the chain of scholarship is more explicitly evi­ dent in taxonomy because of the nomenclatural mandate to consider all relevant names pub­ lished since 1758. Taxon communities have a strong start and can build upon this centuries‐ old chain of scholarship, facilitating the acquisi­ tion, testing, and growth of knowledge. Printed libraries have served as the central repository for growth of taxon knowledge for centuries, but cyber‐enabled taxon “knowledge banks” will provide more up to date, complete, and reli­ able information for users. Challenges associated with building such collaboratories are great. There are technical ­ challenges in fine‐tuning cyberinfrastructures to meet the unique needs of taxonomists (particu­ larly in regard to specimen access and character visualization and communication) and users of taxonomic information. There are sociological challenges in team and collaborative work prac­ tices for a discipline with a long tradition of fierce individualism (Knapp 2008). Although the chal­ lenges are great, there is every reason for opti­ mism. It is entirely realistic to imagine a great taxonomic infrastructure linking the world’s tax­ onomists, research resources, and museums within a decade, utterly transforming the disci­ pline. Foundation stones for this new taxonomy infrastructure are being set in place today.

14.5 ­Insect Taxonomy: Needs and Priorities Many of the needs of insect taxonomy are not unlike those of other sciences, such as educating a new generation of experts and funding research projects. Other needs, however, differ markedly from those of sister biological sciences. For example, there is a special need for a taxonomy‐ specific cyberinfrastructure that networks the resources required for species inventories, col­ lection growth and development, broadly com­ parative studies of specimens, unprecedented international collaboration, and revisionary studies of species by taxon “knowledge commu­ nities.” This “cybertaxonomy” approach repre­ sents a sea change in thinking for insect taxonomists and suggests a number of challenges (e.g., Wheeler and Valdecasas 2005). Let’s exam­ ine some of these needs. 14.5.1 Education

Although cyber tools will allow us to work more efficiently and collaboratively, taxonomy will remain highly dependent on a well‐educated workforce of taxon experts. We need to over­ come the political correctness and fads that skew the workforce away from revisionary taxonomy and toward molecular phylogenetics divorced from descriptive work. Rather than coercing all students to work with molecular data, why not encourage and support students to work at the highest levels of excellence in all aspects of tax­ onomy: morphology, palaeoentomology, ontog­ eny, molecular taxonomy, comparative ethology, and so forth? We talk a lot about “interdiscipli­ narity” and “transdisciplinarity” and then expect utter conformity among students. Forming teams of specialists who each bring a unique set of skills, knowledge, and perspectives to insect taxonomy will greatly enrich the field and ulti­ mately make it useful to a much wider range of communities. Given the massive amount of work to be done in exploring, describing, and classifying our planet’s insect fauna, more than enough work exists for specialists of every kind.

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Taxonomy’s agenda cannot be realized with­ out the support of others. It is equally impera­ tive that we educate biologists in general to understand the epistemic basis of taxonomy and to distinguish good taxonomy from expedient substitutes. Further, we need to share the won­ ders of taxonomy with the public at large. Cyber tools will open many opportunities to do so through both formal and informal (public) edu­ cation activities. Efforts to open access to taxo­ nomic information, such as the Encyclopedia of Life initiative (www.eol.org and Wilson 1993) will greatly expand appreciation for taxonomy. Such portals to species information depend on active taxonomists to supply content. Amateurs have always had a major role in tax­ onomy and should be invited, encouraged, and enabled to continue to do so into the future. There shall never be a taxonomic workforce suf­ ficiently large to deal with the insects and their relatives adequately. Knowledgeable amateurs can contribute specimens, data, and analyses, as well as provide insights into most facets of tax­ onomy. Cybertaxonomy promises to make many of the research resources formerly reserved for professionals openly available to amateurs. This should make insect taxonomy more productive and rewarding to amateurs and enable them to work to higher standards of excellence. Last, but not least, taxonomic education is essential in developing countries with a dispro­ portionate number of undescribed species. The historic north‐south divide, with major collec­ tions and libraries in Europe and North America and most species in the tropics and southern hemisphere, is rapidly evaporating. Soon, all the same resources will be open to students and taxon experts around the globe via Web‐based sources. Building expertise where the bulk of undescribed species live is only common sense and will fuel a much more diverse and interac­ tive world taxonomic workforce.

and many taxonomic studies have been regional in focus. Such fragments of the total picture of species diversity now can be pieced together in cyberspace to enable taxonomists to virtually “see” species and clades across multiple scales of space and time. The implications are profound for the speed and quality of taxonomic work and for the potential to mobilize comprehensive knowledge of large clades for science. Intensive, internationally coordinated megaprojects are needed to tackle large insect taxa. We shall never gain a comprehensive knowledge of major insect taxa unless we mount truly large‐scale scientific efforts to inventory, describe, and classify species; unless the world’s museums work together to assure comprehensive collec­ tions; and unless we pool our collective exper­ tise to speed species exploration. Taxonomy is asking global questions and, therefore, demands large‐scale solutions. In reality, we need the full range of project scopes from the individual researcher to planetary‐scale teams; each has a part to play, and all deserve our support and encouragement. The full potential of virtual “species observatories” is not yet appreciated but will transform taxonomy. 14.5.3  Cybertaxonomy Infrastructure

Generally, what is needed by insect taxonomists is a specialized (taxonomy‐specific) cyberinfra­ structure that opens access to all those things that a specialist working on a particular taxon needs to work smarter, faster, and better. Rather than attempting a detailed description of what such a taxonomic cyberinfrastructure might look like (Page et al. 2005), let’s examine some vignettes that illustrate what taxonomy might be like a decade or less from now. ●●

14.5.2  Planetary‐Scale Projects and Virtual Species Observatories

Taxonomy must be recognized as a planetary‐ scale science. For practical reasons, collections

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Electronic sensors scattered through remote regions of Australia alert a heteropterist that accumulated degree‐days indicate that host plants are about to flower, and she leads a field team to collect poorly known species and document their hosts. A team of collectors in the Congo sit around a campfire after a long day of work. Lek clouds

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of dance flies were sampled that day. A porta­ ble, digital, remotely operable microscope permits the world’s authority on the group to examine a specimen from his office in Paris. He concludes that it is an exciting find, and the team is requested to collect frozen specimens the following day to support DNA studies. A student in Brazil working on her doctoral thesis needs to see a type specimen in London’s Natural History Museum. She checks the museum’s online library of digital images but finds that an important character cannot be seen. On her command, a robotic arm retrieves the specimen with the precision of a watchmaker and places it under a remotely operable digital microscope. Moments later, she is manipulating the specimen and taking detailed digital images. Because she is the first specialist to look at the specimen, she is in the best position to document key features. Her images answer her question and are added to the Natural History Museum’s digital library for future researchers. A specimen is intercepted at a United States port of entry. A shipment worth tens of mil­ lions of dollars is immobilized on the docks, its cargo rapidly approaching spoilage. The specimen is mounted on a similar instrument, and a specialist at the Systematic Entomology Laboratory in Washington examines it and determines it is harmless. Millions of dollars of wastage are avoided, and a problem is solved in minutes that might have taken a day or more by current standards. A couple packs their bags for an eco‐tour of an Amazonian tributary. They have become espe­ cially interested in dragonflies and look for­ ward to seeing as many species as possible. They log onto a website that is the portal to the world’s odonate knowledge community. As they click the “field guide” option on the drag­ onfly website, software seamlessly incorporates a species named days earlier into a pictorial identification guide and distribution map. An ecologist sampling leaf litter in a rainforest in Malaysia needs to identify obscure and numerous species of staphylinid beetles. Bulk

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samples are placed in an insect processor. Specimens are mounted and labeled automat­ ically and sorted into morphotypes. Those matching the target search image are sent to an expert for human inspection. Limited human resources are targeted where judg­ ment is needed. A school child interested in insects makes a collection. She wanders through a garden to the towering sunflowers, where she is amazed at the diversity of wasps and flies. Using a handheld device, she snaps a digital photo­ graphic image of a beautiful fly. With the click of a button that image is transmitted via satel­ lite to a computer that matches it up to three possible species for her GIS position. She compares the images and easily identifies the fly. A fish ecologist wants to know which species of mayflies are being fed on by fish. He takes a fragment of an insect and sequences a DNA “barcode” that is compared against a library of known barcodes representing corroborated species and quickly answers his question.

14.5.4  Web‐Based Revisions, Taxon‐Knowledge Communities and Taxon‐Knowledge Banks

Taxonomic revisions and monographs have long been the gold standard for taxonomic research. Such comprehensively comparative studies are the most efficient way for taxono­ mists to test large numbers of species and char­ acter hypotheses simultaneously, and they are the most authoritative sources of taxonomic information. The new model will involve taxon‐knowledge banks that exist in cyber­ space and that hold the sum total of all we know of a taxon. These banks will be maintained by an international community of taxonomists who severally and jointly test, improve, and expand knowledge. As such, taxon‐knowledge banks will serve the same functions as mono­ graphs, yet be dynamic and up to date. From such banks, users will request on‐demand “publications”, from checklists to field guides,

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distribution maps, monographs, phylogenies, and homology tables.

14.6 ­Accelerating Descriptive Taxonomy

14.5.5  Collection Development and Growth

Every step in the process of doing descriptive taxonomy can benefit from a taxonomy‐specific cyberinfrastructure. Figure 14.2 is an artist’s depiction of a “taxon space” where taxonomists of the future might work. At the core of this space are research resources, such as collections of specimens, digital instruments, visualization and communication tools, robotics, and collec­ tion‐based data. Collectively, these resources and underlying cyberinfrastructure (Atkins et al. 2003) constitute the taxonomy cyberinfra­ structure. The orbiting “electrons” in the dia­ gram represent individual taxonomists around the world who are experts on this particular taxon. Some work singly on particular subtaxa, whereas others align their efforts to make rapid progress in a shared taxon space, much like cur­ rent PBI projects (Knapp 2008, Page 2008). Results are deposited in an openly accessible taxon‐knowledge bank (Fig. 14.3), from which users can extract information as needed. Let’s examine steps involved in doing taxon­ omy. At every junction, impediments to rapid progress have existed. Cyber‐enabled taxon­ omy, or cybertaxonomy, has the potential to overcome each of these obstacles. The numbers for the paragraphs that follow correspond to numbers between steps in Fig. 14.4.

No aspect of taxonomy is more important or deserving of adequate support than the devel­ opment, growth, and care of insect collections. The estimated 3 billion specimens in natural history collections, perhaps half of which are arthropods, are the most extensive documenta­ tion of biological diversity. The most important thing that our generation can bequeath to future generations is a comprehensive collection of species. Collections divorced from active tax­ onomy soon become little more than relics, and the information associated with such collec­ tions rapidly becomes less and less reliable (Meier and Dikow 2004). 14.5.6  Integrative Insect Taxonomy

The relative merits of molecules versus morphol­ ogy continue to be debated, but this misses the point. It is not a matter of whether classifications should be based exclusively on DNA (Tautz et al. 2003) or not (Lipscomb et  al. 2003, Prendini 2005, Wheeler 2005), but rather how the various sources of evidence about insects can best be integrated into taxonomy (Will et al. 2005). This view is not new. Such integration has long been the aim of taxonomy (e.g., Simpson 1961). The fact that most available evidence in the past happened to be morphological has been mis­ construed as a deliberate attempt to make classifications dominantly or wholly morpholog­ ical. Good taxonomic monographs summarize all that is known of the biology of a taxon (e.g., Lent and Wygodzinski 1979), and “holomorphol­ ogy” was central to Hennig’s (1966) arguments. Molecular evidence is held by some to be neces­ sary for phylogeny reconstruction. This position mirrors a similar, and similarly wrong, position once held by paleontologists who thought fossils were the only means to reconstruct phylogeny (Nelson 2004). In reality, all relevant sources of evidence are to be prized and pursued.

14.6.1  (1) Inventories to collections

Comparatively little has been written on improved ways to undertake taxonomic collect­ ing. Taxonomists are concerned with species limits and phylogenetic and biogeographic pat­ terns. As such, they effectively require pres­ ence–absence data. Where taxonomic and ecological questions coincide, it makes sense to gather appropriate quantitative data. However, unless those data meet specified needs of a par­ ticular ecological question, devotion of the resources required for quantitative sampling over long periods of time at one locality does not make sense for taxonomy. Mobilizing existing

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Figure 14.2  A representation of a taxon “knowledge community.”  Taxonomists are represented as orbits around a “nucleus” of taxonomy‐specific cyberinfrastructure. Taxonomists’ “orbits” vary through time. At one point a given taxonomist is working solo on a taxon; at other times, variable numbers of taxonomists converge to focus their collective attention on rapid progress in species description or testing, as in the US National Science Foundation‐ funded Planetary Biodiversity Inventory projects. The nucleus of cyberinfrastructure includes natural history collections (specimens), literature, databases, digital instrumentation, robotics, descriptive software, and so forth. Advances in knowledge are immediately stored and made accessible through various electronic means and databases, collectively known as a taxon “knowledge base.” This is analogous to the traditional return of improved and expanded knowledge through publications, with the exception that it is immediately and openly accessible, up to date, and can be delivered in a user‐defined format. For example, taxonomists can generate traditional monographs; morphologists can make comparisons of homologues in MorphoBank; phylogeneticists can access and edit full character matrices; eco‐tourists can generate field guides; and field researchers can engage a rich toolbox of species‐identification aids, including interactive keys delivered to handheld devices, DNA “barcodes,” and so forth. Graphic by Frances Fawcett, after Wheeler (2008b).

museum data through efforts such as the Global Biodiversity Information Facility (GBIF) helps to identify gaps in collections. There is no reason that remote sensors, automated mass‐collecting traps, and robots cannot vastly speed collecting for certain taxa or that digital transmitting microscopes and communications from the field cannot allow one expert to choreograph several collecting teams at one time.

Processing specimens is often a highly repeti­ tious and labor‐intensive activity that should be amenable to mechanization. With computer image recognition, aspects of sorting and pin­ ning can, in principle, be automated. For large‐ scale inventory efforts, protocols are needed that maximize the number of characters ulti­ mately retrievable. When possible, alternative preservation methods should be designed to

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Taxon Knowledge Bank

Monographs ID Tools Field Guides EOL Pages Checklists Homologies Maps Ecological Assocs. Data/Information

Figure 14.3  Relationship of the taxon “knowledge community” with a proposed taxon‐knowledge bank from which user‐specified “publications” may be generated on demand. Graphic by Frances Fawcett, after Wheeler (2008b).

capture external morphology, internal anatomy, and tissues for molecular sequencing. 14.6.2  (2) Species descriptions

A high‐tech “cockpit” will place all the remote‐ access, analysis, visualization and communica­ tion tools; instruments; data; literature; and colleagues needed immediately in front of the taxonomist of tomorrow. Whether this taxono­ mist is working alone or as part of a distributed, international team, she will draw from and con­ tribute to the knowledge of a taxon. Many details are to be worked out by the community regarding management of such taxon‐knowl­ edge banks, priority for access to specimens or instruments, peer review of online contribu­ tions, and so forth, yet none of these challenges is, in principle, insoluble. Even the peer review process is expedited through automated notifi­ cation of reviewers and online response.

14.6.3  (3) Species tests

Species descriptions are not one‐time proposi­ tions. Instead, species are based on explicitly predicted unique combinations of characters (Wheeler and Platick 2000). From these hypoth­ eses, the same pattern of characters is predicted among newly found characters or specimens. In the past, such tests were completed through comprehensive revisions or monographs. For many insect taxa, revisions were completed once or twice per century. Such tests now can be conducted effectively as fast as new data become available. This approach will more rapidly and efficiently corroborate or falsify “known” spe­ cies as well as detect new ones. What remains crucial overall, and especially in steps 2 and 3, is the need for the deep knowledge of taxono­ mists. There is no substitute for years of prac­ tice and research to develop this knowledge; however, cyberinfrastructure will make that

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Positions

12

Research grants

13

Public education

14

Goals, agenda

15

16

Publications 11 Names

Classifications 9

10 Inventories

Collections 1

5

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7

Species descriptions 2

3

Data bases

Cladistic analysis 6

Species tests 4

Collections-and cyber-infrastructure: Museums and herbaria; digital instruments; software and digital archives (e.g. GBIF); other cyberinfrastructure and tools.

Figure 14.4  Flowchart showing bottlenecks in the process of taxonomic research. See the section on “Accelerating Descriptive Taxonomy” for explanation.

learning process vastly more efficient than in the past. 14.6.4  (4) Species tests to databases

With cyberinfrastructure, the traditional period of time between critical tests of species and the availability of results to users is compressed. Species are corroborated, refuted, and revised as appropriate, and such decisions are instantly available to the user community. The net result is to verify that the best and most current under­ standing of species and their attributes and dis­ tributions are made available to users.

14.6.6  (6) Cladistic analysis

Most users of cladistic information simply want a cladogram with which to interpret some facts or phenomena. As such, most users want rapid access to a corroborated cladogram. Users have access to published cladograms already (e.g., TreeBase: https://treebase.org/). Advanced users should be able to generate cladograms on demand based on the latest data and chosen parameters. Efforts are underway to increase our capacity to deal with ever‐larger data matri­ ces (e.g., CIPRES: www.phylo.org).

14.6.5  (5) Collection data

14.6.7  (7–10) Phylogenetic classifications, names, and identifications

Access to existing specimen‐associated data is important. It allows taxonomists to find and cor­ rect mistakes (Meier and Dikow 2004) and museums to prioritize collection growth. And, of course, it is available to researchers for appli­ cation to countless questions about biodiversity.

Cladograms are the basis for phylogenetic clas­ sifications that are the general reference system (Hennig 1966). Classifications should be dynamic, constantly changing to reflect growth in knowledge. As concepts change, so too do the meanings of names. Approaches are being

14  The Science of Insect Taxonomy

developed (e.g., Franz 2005) to track concepts of species and higher taxa. The language of taxonomy (nomenclature) will become more transparent, more uniformly up to date, and more easily interpreted by users as cybertax­ onomy progresses. The most fundamental example of applied taxonomy is species identification. In the past, identifications frequently required an expert or synoptic collection. Cybertaxonomy will give users a wide array of identification tools. These will include interactive “keys” accessible on handheld computers, computerized image rec­ ognition systems (e.g., MacLeod 2007, 2008), and DNA barcodes (Little and Stevenson 2007). Access to species is also enhanced by the grow­ ing number of electronic catalogs. Registration of names (Polaszek et al. 2005) has the poten­ tial to assure that all available names are easily accessed. 14.6.8  (12–16) Inputs

The inventory and classification of millions of species of insects will require substantial invest­ ments in education, positions, research fund­ ing, and collections. It is urgent that funding for collections and descriptive taxonomy be imme­ diately increased. If the taxonomy and collec­ tions community speaks with one voice and sets clearly stated goals, such funding is realistic and within reach.

14.7 ­Beware Sirens of Expediency Excellent taxonomy is hard work that requires special knowledge. Many who do not under­ stand or appreciate the epistemology of taxon­ omy advocate quick fixes, short cuts, and inferior substitutes. For those who simply want taxonomic information, the appeal of apparent speed and ease are easily understood. Ultimately, however, users of taxonomy are better served by rigorous taxonomic practices. Molecular data are presumed by some to be independent of other data sources and, to a

significant degree, selectively neutral. That said, how data are analyzed is still more important than the kind of data collected (Hennig 1966). Disproportionate funding seems to be driven by a perception that molecular data are superior. That perception seems to be based on modernity, technology, and association with biomedical trends rather than on theoretical arguments. Much is to be learned from the comparative study of molecular, fossil, morphological, and ontoge­ netic data, and much is to be gained from integra­ tive taxonomy (Will et al. 2005). Further, historical (phylogenetic) information is most faithfully stored in the form of complex characters, many the result of multiple genes and epigenetic factors not merely read from nucleic acid sequences. Yet to be seen is whether the current practice of using as much DNA as possible (idealized as whole‐ genome sequencing) and trusting overall phe­ netic similarity to mirror phylogenetic relatedness is ultimately the most successful strategy. It should give us pause that the phenetics program of the 1970s was thoroughly discredited. The fun­ damental concepts of phylogenetic systematics still include special similarity and homology (Hennig 1966). Several current proposals would undermine what continues to make taxonomy excellent. Among these are DNA taxonomy and DNA bar­ coding (Tautz et  al. 2003, Hebert and Gregory 2005; but see Lipscomb et al. 2003, Seberg et al. 2003, Prendini 2005, Wheeler 2005); the PhyloCode (de Queiroz and Gauthier 1990; but see Forey 2002, Carpenter 2003, Nixon et  al. 2003); and Felsenstein’s (2001, 2004) preposter­ ous suggestion that formal classifications are no longer needed (but see Franz 2005). These are dangerous distractions at a time when the full attention of taxonomists is needed to confront the biodiversity crisis, create a legacy of speci­ mens and knowledge for posterity, and trans­ form taxonomy into an efficient, responsive, cyber‐equipped science for the 21st century. It is not an accident that most of these proposals originated from or were promoted by individu­ als who have done little if any descriptive, revi­ sionary, or monographic taxonomy and who

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presume to solve taxonomic problems with little understanding of the theories, epistemology, history, or practices of good taxonomy.

14.8 ­Conclusions The science of insect taxonomy has never had greater prospects for fulfilling its potential. Advances in theory and technology are arming taxonomy with the most powerful tools in its long history, and vastly more powerful tools are within reach. The biodiversity crisis has added a sense of urgency to our purpose and sharply focused the great challenges facing us. Insect taxonomists stand at a crossroads and, given the right decisions and priorities, can make unprec­ edented, timely, and lasting contributions. The time has arrived for insect taxonomists to think big. For the first time in history, we can realistically envisage a generation of tools that enable entomologists to study whole clades effi­ ciently. The fragmented research resources, provincial collections, and individual scholar models of the past can give way to the elevation of taxonomy to an appropriate global scale. A  combination of cyberinfrastructure (Atkins et al. 2003, Wheeler et al. 2004) and the kind of teamwork exhibited in the PBI projects (Knapp 2008, Page 2008), along with a possible alterna­ tive strategy for accelerating species inventories (Wheeler et  al. 2012), point to a clear path to success.

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Novacek and Q. D. Wheeler (eds). Extinction and Phylogeny. Columbia University Press, New York. Otte, D. and J. A. Endler (eds). 1989. Speciation and Its Consequences. Sinauer Associates, Sunderland, Massachusetts. 679 pp. Page, L. M., H. L. Bart, Jr., R. Beaman, L. Bohs, L. T. Deck, V. A. Funk, D. Lipscomb, M. A. Mares, L. A. Prather, J. Stevenson, Q. D. Wheeler, J. B. Woolley and D. W. Stevenson. 2005. LINNE: Legacy Infrastructure Network for Natural Environments. Illinois Natural History Survey, Urbana. 15 pp. Page, L. M. 2008 Planetary biodiversity inventories as models of the new taxonomy. Pp. 55–62. In Q. D. Wheeler (ed). The New Taxonomy. Systematics Association Special Volume Series. CRC Press, Boca Raton, Florida. Patterson, d. J., D. Remsen, W. A. Marino and C. Norton. 2006. Taxonomic indexing – extending the role of taxonomy. Systematic Biology 55: 367–373. Pevsner, J. 2009. Analysis of genomic DNA with the UCSC genome browser. Methods in Molecular Biology 537: 277–301. Polaszek, A., D. Agosti, M. Alonso‐Zarazaga, G. Beccaloni, P. de Place Bjørn, P. Bouchet, D. J. Brothers, the Earl of Cranbrook, N. Evenhuis, H. C. J. Godfray, N. F. Johnson, F. T. Krell, D. Lipscomb, C. H. C. Lyal, G. M. Mace, S. Mawatari, S. E. Miller, A. Minelli, S. Morris, P. K. L. Ng, D. J. Patterson, R. L. Pyle, N. Robinson, L. Rogo, F. C. Thompson, J. van Tol, Q. D. Wheeler and E. O. Wilson. 2005. A universal register for animal names. Nature 437: 477. Pollock, D. A. and B. B. Normark. 2002. The life cycle of Micromalthus debilis LeConte (1878) (Coleoptera: Archostemata: Micromalthidae): historical review and evolutionary perspective. Journal of Zoological Systematics and Evolutionary Research 40: 105–112. Pons, J., T. Barraclough, J. Gomez‐Zurita, A. Cardoso, D. Duran, S. Hazell, S. Kamoun, W. Sumlin and A. Vogler. 2006. Sequence‐based

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A commentary on DNA‐based taxonomy. Trends in Ecology and Evolution 18: 63–65. Simpson, G. G. 1961. Principles of Animal Taxonomy. Columbia University Press, New York. 247 pp. Tautz, D., P. Arctander, A. Minelli, R. H. Thomas and A. P. Vogler. 2003. A plea for DNA taxonomy. Trends in Ecology and Evolution 18: 70–74. Terszowski, G., S. M. Muller, C. C. Bleul, C. Blum, R. Schirmbeck, J. Reimann, L. du Pasquier, T. Amagai, T. Boehm and H. R. Rodewald. 2006. Evidence for a functional second thymus in mice. Science 312: 284–287. Wägele, J.‐W. 2004. Hennig’s phylogenetic systematics brought up to date. Pp. 101–125. In D. M. Williams and P. L. Forey (eds). Milestones in Systematics. Systematics Association Special Volume Series, 67. CRC Press, Boca Raton, Florida. Wheeler, Q. D. 1995a. The “Old Systematics”: classification and evolution. Pp. 31–62. In J. Pakaluk and S. A. Slipinski (eds). Biology, Phylogeny, and Classification of Coleoptera. Papers Celebrating the 80th Birthday of Roy A. Crowson. Muzeum i Instytut Zoologii PAN, Warszawa, Poland. Wheeler, Q. D. 1995b. Systematics and biodiversity policies at higher levels. BioScience 45 (Supplement): 21–28. Wheeler, Q. D. 1999. Why the phylogenetic species concept? Elementary. Journal of Nematology 31: 134–141. Wheeler, Q. D. 2004. Taxonomic triage and the poverty of phylogeny. Philosophical Transactions of the Royal Society B 359: 571–583. Wheeler, Q. D. 2005. Losing the plot: DNA “barcodes” and taxonomy. Cladistics 21: 405–407. Wheeler, Q. D. 2008a. Introductory: Toward the new taxonomy. Pp. 1–17. In Q. D. Wheeler (ed). The New Taxonomy. Systematics Association Special Volume Series. CRC Press, Boca Raton, Florida. Wheeler, Q. D. 2008b. Taxonomic shock and awe. Pp. 211–226. In Q. D. Wheeler (ed). The New

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15 Insect Species – Concepts and Practice Michael F. Claridge School of Biosciences, Cardiff University, Cardiff, Wales, UK

Insect taxonomists face the enormous task of describing, classifying, and providing means for the non‐expert to identify the vast numbers of entirely new or little‐known species that we know to exist, often in extremely endangered environments. Interest in biological diversity has greatly increased over the past 25 years, and at the same time there has been a realization of the urgent need to conserve as much of it as possible. A major problem with this agenda is the ongoing debate and disagreement about species concepts. No topic in evolutionary and systematic biology has been more contentious than the nature and meaning of species. In the words of the late Ernst Mayr (1982), “There is probably no other concept in biology that has remained so consistently controversial as the species concept.” Species are usually the primary practical units of biodiversity and conservation (Wilson 1992), so it is important that, so far as possible, we agree on their nature. One of the aspects of the species problem that has made it on the one hand so intractable but on the other so reward­ ing is that it is not only a practical problem for all taxonomists and biologists, but also a deeply philosophical and theoretical one (Hey 2006). The continuing interest in these problems over the past 25 years has led to the publication of several relevant books and review articles, nota­ bly by Ereshefsky (1992), Paterson (1993),

Wilson (1999), Wheeler and Meier (2000), and Wilkins (2009a, b). However, these publications are mostly concerned with the diversity of theo­ retical and philosophical approaches to the issues, with little reference to real practical problems. Almost 20 years ago, together with my ­colleagues Hassan Dawah and Mike Wilson, I edited and contributed to a multi‐author vol­ ume under the title Species: the Units of Biodiversity (Claridge et  al. 1997a). In this ­volume, we brought together practicing tax­ onomists from across the breadth of organis­ mal diversity, including workers on different groups of animals, plants, fungi, and microor­ ganisms, in an attempt to find common ground. The results showed how difficult it is to have a biologically meaningful and unified species concept across such diverse organ­ isms. However, insects, although they repre­ sent some 60–65% of all living biodiversity (Hammond 1992), are just one subset, one class of one phylum, of all living organisms and thus share many genetic mechanisms and more of a common heritage. Maybe, therefore, we can be more optimistic in attempting to agree on a common species concept for these megadiverse organisms? Here, I review spe­ cies concepts in a historical context and look for a unified concept that may be of practical use for insects.

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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15.1 ­Early Species Concepts – Linnaeus The term species is an old one and derives from the writings of classical Greek philosophers, most notably Aristotle (Cain 1958). It was natu­ ral for scholars and naturalists of the 17th and 18th centuries to adopt the systems of Aristotelian logic in attempting to classify and make sense of the natural world. Technical terms from this system that were used in attempts to classify living organisms included “definition,” “genus,” “differentia,” and “species.” Here, genus referred to the general kind, whereas species referred to the particular kind within the genus, as qualified by the differentia. Carl von Linné, better known as Linnaeus and the founder of the binomial system of nomen­ clature that we still use for living organisms, most clearly documented his principles and practice in producing classifications of both ani­ mals and plants (Cain 1958). The binomial sys­ tem itself is a result of the use of the Aristotelian system. Authors previous to Linnaeus, and indeed Linnaeus himself in his early works, had given multinomial names to organisms  –  the genus being one word, but qualified by a descrip­ tive phrase, the differentia, to describe and delineate the species itself. Linnaeus, from the 10th edition of the Systema Naturae in 1758 and probably because of the pressures to describe such large quantities of new material, reduced the differentia for animal species to a single word – the specific name – and so invented the binomial that has been used for plants and ani­ mals to this day. It has been challenged unsuc­ cessfully at various times in the past and is currently under attack by proponents of the phylocode, but it is likely once again to prevail (Wheeler 2004). To Linnaeus, species were simply the lowest category of particular kinds in his classifica­ tions, although he also often recognized “varie­ ties” within species. Linnaeus not only published classifications and descriptions of many animals and plants, but also wrote books in which he detailed his methods and

­ hilosophy (e.g., Linnaeus 1737). In a study of p these many ­ writings, Ramsbottom (1938) showed that in developing a practical concept of species, Linnaeus recognized three main cri­ teria. Species were (i) distinct and monotypic, (ii) immutable and created as such, and (iii) true breeding. Criteria (i) and (ii) here are to be expected in pre‐evolutionary philosophy; (iii)  may be a little more surprising. The idea that species had a single norm of morphologi­ cal variation and were clearly each distinct from all other species within the same genus was widely accepted. Linnaeus was, of course, working in exciting times when European explorers were travelling widely in regions of the world previously unknown to them and bringing back large collections of plants and animals for study. For obvious reasons, these samples consisted of dead and often poorly pre­ served material. Thus, to describe new species and to classify them, early taxonomists had lit­ tle recourse but to use morphological charac­ ters. The total immutability of species was clearly widely accepted in the 18th and early 19th centuries, but even Linnaeus later in his life developed some complicated theories of speciation by hybridization (Cain 1993). Before the enormous influx of tropical mate­ rial into European museums, most early taxon­ omists, including Linnaeus, were field naturalists themselves and familiar with the organisms on which they worked as living entities. They knew that the species they described from local fau­ nas and floras were biologically distinct and dif­ fered in obvious features of their natural history, as well as their morphology. The swamping of museums by large collections from overseas inevitably led to the almost exclusive use of morphological differences to describe and rec­ ognize species. This situation remains so today for most groups of animals, and particularly for species‐rich groups, such as insects. The mor­ phological species, or “morphospecies,” has evolved from these early classifications, mostly for reasons of convenience. Today, such mor­ phospecies are being developed through the use of molecular characters for recognizing species

15  Insect Species – Concepts and Practice

(Tautz et  al. 2003; Blaxter 2004, Sperling and Roe (2009); Roe et  al., this volume). The mor­ phospecies, however, is not a philosophical con­ cept, but simply a practical category. No doubt Linnaeus would have been unhappy that his philosophy should be reduced to such a purely practical matter. Following Linnaeus, taxono­ mists were forced to use the practical morphos­ pecies for what they largely knew only as dead museum specimens. The amount of difference required to recognize and separate species became inevitably more and more subjective, as illustrated by Regan (1926): “A species is a com­ munity, or a number of related communities, whose distinctive morphological characters are, in the opinion of a competent systematist, suf­ ficiently definite to entitle it or them to a spe­ cific name.” Because taxonomy and systematics, more and more through force of circumstance, were based only on morphological differences among dead museum specimens, the two quite different tra­ ditions of studying the natural world diverged, with what we might call the morphologists on one side and the naturalists on the other. Even in the late 18th century, naturalists were well aware that species had some real biological basis in the field. The British naturalist Gilbert White (1789), for example, first showed that several morphologically similar species of song birds of the genus Phylloscopus, the warblers, in Britain were separated in the field by their distinctive male songs, now known to function as impor­ tant elements of their specific mate‐recognition systems (SMRSs). This interest in breeding bar­ riers and species as reproductive communities was an essential element of the naturalist tradi­ tion. Later in the 19th century, Charles Darwin and Alfred Russel Wallace were notable figures of the naturalist tradition in the English‐speak­ ing world. From this tradition, they indepen­ dently developed the theory of evolution by natural selection and accumulated overwhelm­ ing evidence for descent with modification. After the general acceptance of evolution, spe­ cies were recognized as the end terms of differ­ ent lines of descent. The controversies around

evolution itself meant that the nature of species was not regarded at that time as a high‐priority subject. Darwin himself seems often to have regarded species as more or less arbitrary stages in the process of evolutionary divergence.

15.2 ­Biological Species Concepts In addition to developing the idea of species as morphologically discrete entities, Linnaeus had the idea, admittedly more vague, of species as breeding units that generally breed true (Ramsbottom 1938). These ideas were clarified and became central to species philosophy only in the late 19th and early 20th centuries. Probably the most important contributor to this way of thinking, certainly in the English‐speak­ ing world, was Sir Edward Poulton. First in 1904, in his presidential address to the Entomological Society of London, and later in a volume of essays on various aspects of evolution, Poulton (1908) made the most important advance toward what has since become known as the biological species concept. He emphasized the importance of interbreeding in the field as the most crucial species criterion. This criterion was what Mayr (1942, 1963) later termed cross­ ability and contrasted strongly with interfertility or simple ability to hybridize. Poulton was one of the first authors to make this clear differenti­ ation and thus effectively to develop the modern biological species concept, for which generally he has received insufficient credit (Claridge 1960, Mallet 1995). During the early and mid‐20th century, the revolution in evolutionary thinking, often known as the Evolutionary Synthesis (Mayr and Provine 1980), was developed by means of the attempted unification of systematics, genetics, and evolution, exemplified by the publication of major seminal volumes, including Genetics and the Origin of Species (Dobzhansky 1937) and Systematics and the Origin of Species (Mayr 1942). The so‐called biological species concept was central to these ideas and received many definitions, perhaps the most useful and

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c­ ertainly most widely cited of which is: “species are groups of actually or potentially interbreed­ ing natural populations which are reproduc­ tively isolated from other such groups” (Mayr 1942: 120). Reproductive isolation in nature was the key factor in identifying and maintaining species, as it was for Poulton. Reproductive iso­ lation was maintained by what Dobzhansky (1937) termed “isolating mechanisms,” which were attributes of species populations that reduced the likelihood of interbreeding. Such a category is a wide one, including behavioral and ecological differences that act before mating and the fusion of gametes, post‐mating genetic incompatibilities, and totally extrinsic geo­ graphical barriers. The latter are not properties of organisms and are not now generally classi­ fied with the intrinsic factors. To Dobzhansky, speciation was the origin of reproductive isolat­ ing mechanisms and thus of reproductive isola­ tion. Dobzhansky’s system of classification of isolating mechanisms was followed and modi­ fied by many authors during the 20th century, including particularly Mayr (1942, 1963, 1982) and Cain (1954). A major set of criticisms of the biological spe­ cies concept has been developed over some years by Hugh Paterson (1985, 1993). One of his main concerns is with the concept of species isolating mechanisms and with the implication that they have evolved as adaptations under nat­ ural selection to achieve and maintain repro­ ductive isolation. Paterson must be correct, at least for all so‐called post‐mating mechanisms, which logically cannot be due to such adapta­ tion (Mallet 1995). Avise (2004) and Coyne and Orr (2004) have suggested the more neutral term “isolating barrier” to replace isolating mechanism. This suggestion is useful, but does not deal with Paterson’s further criticisms. Maybe there is no need for a term to include such a diversity of phenomena? Paterson regards species as groups of ­organisms with common fertilization systems. “We can, therefore, regard species as that most inclusive population of individual biparental organisms which share a common fertilization

system” (Paterson 1985: 25). He recognized an important subset of the fertilization system that he termed the specific mate‐recognition system (SMRS), “which is involved in signaling between mating partners and their cells.” Thus, the often complicated reciprocal signals and signaling systems of mating and courtship, classically documented by ethologists (Tinbergen 1951, Eibl‐Eibesfeldt 1970, Brown 1975), have the essential function, among others, of ensuring specific mate recognition. Successive signals release, in turn, successive responses via tuned receptors in the opposite sex. These sequences are usually, but not exclusively, initiated by males. Unless appropriate responses are received at each stage and the signals are recog­ nized as appropriate, exchange will be termi­ nated and ultimate exchange of gametes will not occur. The exchanges of signals between part­ ners may be broken off at any stage. Thus, to Paterson, species are defined by their unique SMRSs and the evolution of new species, speci­ ation, is the origin of new SMRSs. He has argued at length over the years that his concept of spe­ cies is quite distinct from the biological species sensu Mayr. He terms the latter the “isolation concept,” because it is defined by reproductive isolation from other species, and terms his own system the “recognition concept.” Lambert and Spencer (1995) and Vrba (1995) strongly sup­ ported this line of argument, but others have doubted the clear demarcation between isola­ tion and recognition concepts (Claridge 1988, 1995a; Claridge et al. 1997a; Coyne et al. 1988; Mayr in Wheeler and Meier 2000; Coyne and Orr 2004). In practice, a broadened biological species concept would recognize that different species are characterized by distinct SMRSs that result in the levels of reproductive isolation between sympatric species observed in the field. However, species are only rarely recognized by direct studies of the SMRSs, which are them­ selves equally rarely understood with certainty, but which must be the final arbiters for deter­ mining biological species boundaries (Claridge 1988; Claridge et  al. 1997a, b). More usually,

15  Insect Species – Concepts and Practice

biological species are recognized by markers that are thought to indicate the existence of reproductive isolation. Typically, these have been morphological markers, so taxonomists hypothesized that the differences they recog­ nized and used to separate morphospecies were also indicators of biological species boundaries. More recently, morphological markers have been supplemented by a wide range of other markers, including cytological, behavioral, and biochemical ones. In particular, molecular markers involving characters derived from the amino acid sequences of specific sections of DNA are being used more and more (Avise 2004; Sperling and Roe 2009; Roe et al., this vol­ ume). Indeed, it has even been suggested that all species should be diagnosed primarily by such molecular differentiation (e.g., Tautz et al. 2003, Blaxter 2004). In my view, the enormous diversity of markers now available to taxono­ mists, including molecular ones, simply pro­ vide indicators for levels of reproductive isolation, the ultimate criterion for species sta­ tus. However, levels of gene flow between pop­ ulations and, therefore, probable levels of reproductive isolation, are now routinely esti­ mated by molecular divergence (e.g., De Barro et al. 2011), which is an enormous advance for taxonomic science. A particular feature of the biological species concept is that reproductive isolation can occur between species populations without obvious accompanying morphological differentiation. This phenomenon of real biological species existing in nature without, to the human observer, any obvious differences between them has been recognized since early in the 20th cen­ tury and was well discussed by Mayr (1942). Such species are usually known as sibling, or cryptic, species and have been demonstrated in many groups of insects (Thorpe 1940; Mayr 1942; Claridge 1960, 1988; Claridge et al. 1997b; Bertrand et al. 2014). During the heyday of the biological species concept in the middle years of the 20th century, a large body of opinion among museum taxono­ mists was nevertheless opposed to it (e.g., Sokal

and Crovello 1970) and preferred either some overtly morphological species approach or a purely phenetic one. Such views have been held strongly by many botanists on the grounds that interspecific hybridization is so common in plants that reproductive isolation is not a useful criterion (Gornall 1997, Bachmann 1998; but see Mayr 1992). However, entomologists also have often led criticism of the biological species concept. Two important problems in the use of the bio­ logical species concept are acknowledged by all of its proponents. These concern the status of asexual and parthenogenetic forms, and geo­ graphically or spatially isolated (allopatric) populations. 15.2.1 Agamospecies

The biological species concept in its various manifestations can be applied only to bipa­ rental, sexually reproducing organisms in which a distinctive SMRS leads to reproduc­ tive isolation. Neither asexual nor obligate parthenogenetic organisms have a functional mate‐recognition system that leads to the fusion of gametes, so the biological species concept cannot apply to them. These organ­ isms exist as clones that can differ in mor­ phology, biochemistry, cytology, behavior, ecology, and other features (Foottit 1997). Distinctive and diagnosable clones are often described as species, but they cannot be bio­ logical species. They are, thus, practical cate­ gories like the morphological species, which were given the useful term agamospecies by Cain (1954). Many groups of living organisms, including many microorganisms, can only be agamospecies. 15.2.2  Allopatric Forms

A real problem with applying the biological species concept is that reproductive isolation in the field can be determined only for sympa­ tric populations where alone there are possi­ bilities of testing the effectiveness of SMRSs in the field. Geographical variation and the ­status

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of allopatric populations have long been of major interest to taxonomists and evolution­ ary biologists. Degrees of observable differen­ tiation between allopatric populations vary from almost nothing to large differences, at least comparable with those observed between distinct sympatric species of the same taxo­ nomic group, but the criteria of gene flow and reproductive isolation in the field cannot be conclusively tested. Experimental crossings of allopatric forms under laboratory and experi­ mental conditions yield results of only limited value (Claridge et  al. 1985a). The polytypic nature of biological species has long been rec­ ognized, and a series of taxonomic categories, from subspecies to superspecies, has been developed to describe essentially continuous geographical variation (Mayr 1942, Cain 1954). This continuum on the one hand has provided vital data for the development of theories of allopatric, or geographical, specia­ tion (Mayr 1942, Cain 1954), but on the other hand has led many also to regard the species as no more than a rather arbitrary stage in the divergence of local populations. Alfred Russel Wallace (1865: 12), when confronted with the bewildering range of geographical variation and polymorphism in the swallowtail butter­ flies of Southeast Asia, said: “Species are merely those strongly marked races or local forms which, when in contact, do not inter­ mix, and when inhabiting distinct areas are generally believed to … be incapable of pro­ ducing a fertile hybrid offspring … it will be evident that we have no means whatever of distinguishing so‐called ‘true species’ from the several modes of variation … into which they so often pass by an insensible gradation.” Wallace, and Darwin also, was impressed with variation within and between natural popula­ tions as the basic material for evolution by natural selection. Equally today, the allocation of allopatric populations within the subspe­ cies/superspecies range is largely subjective. Drawing a line through any continuum must be arbitrary. This problem is undoubtedly a weakness of the biological species concept,

but I would argue equally that it is a weakness of all discrete species concepts that aim to reflect biological reality. These complications, together with a desire to eliminate the priority given to one set of organismal characters – the SMRS and repro­ ductive isolation  –  over all others, including molecular ones, have persuaded many sys­ tematists to abandon completely the biologi­ cal species concept in favor of what we have termed a general phylogenetic species con­ cept (Claridge et  al. 1997a). But before con­ sidering phylogenetic concepts in more detail, it is appropriate to discuss the ideas of Mallet (1995) on his “genotypic cluster criterion” or concept of species. Mallet is a geneticist, who has worked on widely distributed species and populations of tropical butterflies. He is con­ cerned that the biological species concept is absolute and does not allow for interspecific hybridization and intergrading, which he has extensively reviewed (Mallet 2005). However, because intergradation is the basis of the pol­ ytypic biological species espoused by Mayr, Cain, and others, this criticism cannot be a real problem. Even in sympatric interactions, reproductive isolation does not need to be absolute to maintain species integrity. Indeed, the acceptance of the reality of evolution demands that species cannot always be com­ pletely reproductively isolated. Intermediates and intergradation must be expected. Thus, all realistic species concepts must allow for such intergradation, and the broadly con­ ceived biological species concept certainly does this. Another contribution, along lines similar to those of Mallet (1995), is the “genomic integrity species definition” of Sperling (2003). Here, species are “popula­ tions that maintain their genomic integrity when they contact each other, even if they occasionally exchange genes.” These various attempts to formulate more inclusive and realistic species concepts appear to me to be quite compatible with, and similar to, the broadly based biological species concept advocated here.

15  Insect Species – Concepts and Practice

15.3 ­Phylogenetic Species Concepts A revolution in the philosophy and practice of systematics took place in the English‐speaking world after the publication of Hennig’s Phylogenetic Systematics in translation from the original German in 1966. Almost all systema­ tists today use some variant of the cladistic methodologies pioneered by Hennig. Coincident with this widespread acceptance of cladistic methods for establishing phylogenetic hypoth­ eses and making robust classifications came increased published dissatisfaction with, and rejection of, the biological species concept by many systematists (e.g., most authors in Wheeler and Meier 2000). Hennig, who was a distinguished German entomologist, thought of species as reproductive communities, so his species concept was broadly similar to the bio­ logical species concept of Mayr (1942). Hennig, of course, was interested primarily in extending species back in time as diagnosable clades, for which the biological species is not suited. In this, he was developing what Simpson (1951) had begun as a broader evolutionary species concept, which has since been taken up by many others (e.g., Cain 1954, Wiley 1978, Mayden 1997, Wiley and Mayden in Wheeler and Meier 2000, Hey 2006). Cladists certainly have not spoken with one voice on the nature of species. Hennig (1966) saw species as that unique level in the taxo­ nomic hierarchy at and above which cladistic methods could be applied to determine phy­ logenies and below which they could not. Within species, interbreeding relationships dominate; Hennig differentiated these from phylogenetic relationships, calling them “tokogenetic relationships,” a term that has not been widely adopted. Wheeler and Nixon (1990) supported the idea that species are uniquely different from higher‐level taxa on the grounds that they do not have resolvable internal phylogenetic structure. On the other hand, Nelson (1989), in stating that “A species is only a taxon,” expressed the view that s­ pecies

simply represent one level in the taxonomic hierarchy and are of no more significance than any others, such as genus, family, or order. Similar views have been argued more recently and strongly by Mishler (2010) and criticized by me in the same volume on contemporary debates on the philosophy of biology (Claridge 2010). Wheeler (1999) also supported the idea of the reality of species, stating: “That species exist in nature is one aspect of species about which I can agree with Mayr (1963).” Most tax­ onomists also seem broadly to agree, although Mallet (1995) expressed doubts. However, modern molecular phylogeographic tech­ niques suggest also that the sharp differentia­ tion in terms of phylogenetic pathways above and below species is not as absolute as Hennig, Wheeler, and others have suggested. A full introduction to these methods was given by Avise (2000) and reviewed by Sperling and Roe (2009). Many authors have attempted to formulate an expressly phylogenetic species concept. In a valuable volume devoted to a debate about spe­ cies concepts and phylogenetic theory, propo­ nents of two different such phylogenetic concepts presented their arguments and disa­ greements, not only over the biological species concept and what is termed the Hennigian spe­ cies concept, but also with each other – Mishler and Theriot on the one hand and Wheeler and Platnick on the other (in Wheeler and Meier 2000). Despite these disagreements, there is some practical consensus, and perhaps the most widely cited definition of the phylogenetic con­ cept is that of Cracraft (1983, 1997), who stated that the species is the “smallest diagnosable cluster of individual organisms within which there is a parental pattern of ancestry and descent.” Some critics have suggested that this definition does not apply to populations, a view fiercely refuted by Cracraft (1997). Nixon and Wheeler (1990) emphasized this when they defined phylogenetic species as “the smallest aggregation of populations (sexual) or lineages (asexual) diagnosable by a unique combination of character states in comparable individuals.”

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Thus, it seems to me that the essence of the phylogenetic concept in its various forms ­ involves the recognition of diagnosable clades. The major question then has to be just exactly what is diagnosable? How different do two pop­ ulations or lineages have to be before they are diagnosably and recognizably distinct? These judgments must surely be subjective, particu­ larly because what is distinct to one taxonomist might well not be to another. Leaving aside the latter major difficulty, any of the markers discussed above that are useful for delimiting biological species, including molecu­ lar and behavioral ones, also can be used to characterize phylogenetic species, although in most groups such characters have tended to be exclusively morphological. Claridge et  al. (1997a) concluded that the practical differences between the application of a phylogenetic con­ cept and a broadly biological one were not great, a view which I still broadly hold. To me, the great disadvantage of the phylogenetic concept is the difficulty in agreeing on what precisely is a diagnosable difference. The advantage of the biological concept is that it attempts to identify real, reproductively isolated populations, even though isolation is not always complete. However, the phylogenetic concept can be applied to asexual or parthenogenetic lineages, which are effectively agamospecies (Cain 1954). When applying the phylogenetic species con­ cept, the problems faced when differentiating allopatric populations are no different from those faced when differentiating sympatric ones. Thus, diagnosably distinct allopatric pop­ ulations will be regarded as separate species. The result will almost always be that more allopatric populations will be recognized as dis­ tinct species than would be the case if a poly­ typic biological concept was applied. For example, the well‐known analysis of the birds‐ of‐paradise (Aves: Paradisaeidae) by Cracraft (1992), using his phylogenetic concept, estab­ lished more than twice as many species (90) than had previous applications of the biological species concept to the same data set! However, the judgment will be essentially subjective under

both concepts, although various authors, from Mayr (1942) to Sperling (2003), have attempted to provide more objective criteria for assessing the species status of totally allopatric popula­ tions. Although there are fundamental differ­ ences of philosophy and theory between the biological and phylogenetic concepts, I see little difference generally when they are applied in practice. Despite the apparent advantages of the phylo­ genetic concept in breadth of application, in my view it has one additional and major practical disadvantage when compared with biological concepts, and that is the improbability that its application will reveal the existence of com­ plexes of sibling species. The philosophy of the phylogenetic species gives no incentive or rea­ son to search for further divisions once diagnos­ ably distinct forms have been established. Conversely, the emphasis of the biological spe­ cies concept on reproductive isolation and spe­ cific mate recognition means that sibling species will be revealed by its diligent application. Among insects, and many other organisms, sib­ ling species are now widely known and are often of great biological significance.

15.4 ­Species Concepts and Speciation – a Digression? Although not strictly within the remit of this book, theories of speciation have been closely tied to the development of particular species concepts, so a brief review is appropriate here. Most modern authors will agree that in recog­ nizing and describing species, taxonomists are providing a framework for understanding the diversity of living organisms and their evolu­ tionary relationships. However, the philosophi­ cal interactions between different species concepts and particular theories of speciation are long standing and still not fully resolved. A system for describing observed diversity should be independent of the various possible modes by which that diversity might have evolved (but see Bush 1994, 1995; Claridge 1995b).

15  Insect Species – Concepts and Practice

Probably the most widely accepted mode of animal speciation is that of geographical or allopatric speciation (Mayr 1942, 1963; Cain 1954). The essence of allopatric speciation is that an ancestral population becomes divided into at least two daughter populations that are isolated in space; as a result, they diverge and develop genetic isolation prior to any subse­ quent meeting and sympatry. The most extreme view of this is that the daughter species must have diverged to the extent that they do not interbreed on meeting: that is, they have devel­ oped completely separate SMRSs, in the termi­ nology of Paterson (1985, 1993), who is the strongest current supporter of this view. Contrary to this theory of speciation in com­ plete allopatry, many authors, particularly Wallace (1889) and Dobzhansky (1940), have developed theories of the reinforcement of spe­ cies isolating mechanisms in sympatry after the partial divergence of incipient species popula­ tions in allopatry. This theory is still controver­ sial and has been reviewed by Coyne and Orr (2004). Apparently quite distinct from the various theories of allopatric speciation are those of sympatric speciation, whereby no period of allopatry is necessary for two species to diverge from a previous one, normally by powerful dis­ ruptive selection. Although not strongly sup­ ported in the early years of speciation theory, such ideas have always been advanced by some entomologists and others working with large groups of sympatric specialist feeders, including parasites and herbivores (Walsh 1864; Bush 1975, 1993, 1994). Here, descendant species diverge within the range of the ancestral species and, therefore, all stages of such divergent pop­ ulations can be expected to exist in the field together. These ideas have become more accept­ able in recent years (Coyne and Orr 2004), to the extent that even Ernst Mayr, the strongest opponent of such theories since his 1942 book, accepted in his final work that sympatric specia­ tion is probable at least in some parasites (Mayr 2004). A developing consensus is that there may be a continuum from pure allopatric to pure

sympatric speciation, whereby intense natural selection might outweigh the swamping effects of gene flow by hybridization. A recent example is given by Butlin et al. (2013). Whatever the final consensus on speciation, there is little doubt that the nature of our spe­ cies concept should not depend on the mode of speciation. Thus, in principle, I agree with most cladists on the particular point that we should describe the patterns of diversity that we see in nature independently of the theories concern­ ing the evolution of such patterns, in as far as this is possible (Wheeler and Nixon 1990). However, I cannot agree with these authors that: “the responsibility for species concepts lies solely with systematists.” Aside from the essen­ tial arrogance of such a statement, an evolution­ ary view of species inevitably must involve at least genetics and evolutionary biology, in addi­ tion to systematics. If we accept the generality of evolution and species as the end results of evo­ lutionary divergence, then the species concept itself must be an evolutionary one. Simpson (1951) first attempted to fuse biological species, agamospecies, and paleospecies into a unitary, all‐embracing evolutionary concept. Cain (1954) developed further and clarified these ideas. Later, particularly following the general acceptance of cladistic methodologies, the ideas were further refined by Wiley (1978), Mayden (1997, 1999), and Wiley and Mayden (in Wheeler and Meier 2000). Such theories pro­ vide a reasonably satisfactory philosophical fusion of the variety of species concepts that account for the diversity of living organisms and their relationships over time, but do not help much in the purely practical recognition and identification of species.

15.5 ­Insect Species – Practical Problems About 99% of all insects are estimated to be biparental and to reproduce sexually, a process involving the meeting of males and females and the exchange of gametes by copulation in often

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complicated sequences of courtship behavior. Here, in principle, the criterion of reproductive isolation is applicable and, thus, the biological species concept should provide a basis for rec­ ognizing and establishing species limits for most insect groups. 15.5.1  Parthenogenetic Insects

About 1% of all insects are obligately partheno­ genetic, and an agamospecies concept has to be used in the recognition and description of “spe­ cies” (Foottit 1997). Parthenogenetic organisms exist as clones, which, contrary to some opin­ ion, can incorporate considerable genetic varia­ tion (Loxdale and Lushai 2003). It is essential in such groups to have names for distinctive enti­ ties that may be regarded as species. They often differ in important features of behavior, such as feeding preferences and ecology, from other agamospecies (De Bach 1969). From a practical viewpoint, species in these insects should be treated in essentially the same way as biparental species. They may be discriminated by any of the morphological and molecular characters normally used for biological species. 15.5.2  Species, Host Races, and Biotypes

Terrestrial ecosystems are dominated by the enormous numbers of insect species. Despite this diversity, insects are remarkably conserva­ tive in morphology and, to the non‐entomolo­ gist, most tend to look much the same. The result is that morphological taxonomy has to be based on relatively small differences that are often difficult to appreciate, so species taxon­ omy is generally difficult. Despite their mor­ phological conservatism, however, insects are ecologically diverse and usually species‐specific in their habits. Thus, species often differ most obviously in features of ecology and behavior. About 50% of insects are estimated to be herbi­ vores (Strong et al. 1984), and a high proportion of the remainder are probably parasitoids, largely attacking other insects. Thus, most insects are effectively parasites (Price 1980),

either on plants or other insects (parasitoids), and tend to be narrow ecological specialists. The result is that, in well‐studied groups, spe­ cies are most obviously characterized by differ­ ences in food exploitation and behavior (Claridge et al. 1997b). Perhaps not surprisingly, the idea of sibling, or cryptic, species has been explored widely, particularly by entomologists. After such species have been recognized by appropriate biological studies, markers may then be found that enable simpler identification. In traditional taxonomy, these markers can be small, but consistent, morphological differ­ ences, as for example in the fine structure of the external genitalia (Claridge et  al. 1997b), but today are also likely to be molecular ones (e.g., Tautz et al. 2003, Al‐Barrak et al. 2004, De Barro et  al. 2011, Sperling and Roe 2009). The latter have the enormous advantage that all stages of the life cycle are potentially identifiable. The specialized relations between insect par­ asites, including herbivores, and their hosts often make species delimitation and identifica­ tion difficult. Host‐associated populations can show varying degrees of phenotypic differentia­ tion in terms of the markers, both morphologi­ cal and molecular, used by taxonomists. Difficulties in determining the status of such populations have resulted in the widespread use of such quasi‐taxonomic terms as “host race,” “biological race,” and “biotype” (Walsh 1864, Thorpe 1930, Claridge and den Hollander 1983, Diehl and Bush 1984, Claridge 1988, Claridge et  al. 1997b, Drès and Mallet 2002) for stages intermediate between completely panmictic populations and distinct biological species. The status of such populations is intimately involved in arguments over the role of sympatric specia­ tion in the evolution of insect parasites (Bush 1994). In my view, these hypotheses should not affect directly discussions on the species status of host‐associated populations (Claridge 1995b). Of course, species are the result of split­ ting lineages, so that at some stage during the process of speciation, diverging populations will not be completely reproductively isolated from each other. Nevertheless, many examples of

15  Insect Species – Concepts and Practice

supposed host races and biotypes, when closely analyzed, have been found to represent separate biological species. An important set of tech­ niques widely used in such studies, those of multivariate analysis, have enabled small and variable characters, generally morphological ones, to be evaluated to great effect (Sorensen and Foottit 1992). The phenomenon of complexes of sibling spe­ cies was first recognized by workers on insect vectors of disease organisms of both humans and domesticated animals (Lane 1997). The rea­ sons for this are obvious  –  these insects have been intensively studied because of their impor­ tance to human health. Malarial mosquitoes of the genus Anopheles were the first to be studied in sufficient detail for them to be recognized as complexes of sibling species with differing abili­ ties to transmit various forms of malarial para­ sites (Linton et al. 2003). Experimental breeding and crossing showed that a wide variety of markers might be used to identify genetically distinct populations, including the morphology of all life‐history stages, chromosome banding patterns, allozyme markers, and, particularly now, DNA markers (Linton et al. 2003). A recent detailed macrogenomic and large spatial scale study of another group of blood‐sucking flies, “ black flies” (Simuliidae) of the subgenus Wilhelmia, over the whole Palearctic region has revealed the existence of more cryptic species than previously thought (Adler et  al. 2015). These results were achieved by analyses of giant polytene chromosome banding patterns that provided markers for distinct and largely geo­ graphically replacing species. Related insect herbivores on different host plants can show marked differences between each other. When interpreting such variation, biologists encounter problems similar to those faced when interpreting the variation between allopatric populations. These problems may be even more complicated by the problems of dif­ ferentiating between those characters that are the direct result of induced responses to living and feeding on particular hosts and those that reflect real genetic differences between

­ opulations. Ideally, such differentiation is best p achieved by experimental rearing and transfer between hosts (Claridge and Gillham 1992). For example, Gillham and Claridge (1994) reported the results of multivariate analyses of morpho­ logical characters of the common, polyphagous, tree‐feeding leafhopper Alnetoidia alneti in Europe. Differences in the body size and color of populations from different tree species had ear­ lier suggested that A. alneti is a complex of sib­ ling species. We found that populations from different tree species were statistically separable by these techniques. However, the transfer of first‐instar nymphs from one host to another resulted in adults similar to those normally found on the host plant to which they were transferred. Thus, no evidence suggested that the differences between host‐associated popu­ lations of this insect represent any significant genetic differentiation, and we concluded that A. alneti is a truly polyphagous species, at least in Europe. A further example is provided by the widely distributed and studied Asian brown planthop­ per Nilaparvata lugens, which is a major pest of rice (Oryza spp.) in Asia and Australasia. The main strategy for control of this insect has been the use of host‐plant resistance, which was originally developed, to great effect, mainly at the International Rice Research Institute (IRRI) in the Philippines. Populations of N. lugens evolved rapidly in the field during the 1970s and 1980s in different rice‐growing areas of Asia, and were able to overcome previously resistant rice varieties. Some of these virulent populations were reared in laboratory cages and termed biotypes 1, 2, 3, and so forth, depending on their patterns of virulence to par­ ticular resistant varieties (IRRI 1979). Working at IRRI, Saxena and Rueda (1982) and Saxena et al. (1983) demonstrated significant morpho­ metric differences among these biotypes. They concluded that the biotypes were host races and represented intermediate stages in a pro­ cess of incipient speciation. We confirmed that there were indeed significant differences between these biotype populations, but when

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they were all reared on one susceptible rice variety under the same conditions, the differ­ ences among them disappeared after only one generation (Claridge et  al. 1984). These bio­ types are, thus, simply locally adapted popula­ tions with relatively little genetic differentiation among them, as confirmed also by selection and crossing experiments (Claridge and den Hollander 1980, 1982). They do not merit spe­ cial taxonomic recognition. More refined molecular studies at the IRRI have supported these findings (Chen et al. 2011). Most controversy has surrounded the subject of possible host races and biotypes with respect to theories of sympatric speciation. Drès and Mallet (2002) published a full and critical review of insect host races in the context of sympatric speciation. They concluded that at least some supposed examples of host races represent spe­ cialized, genetically differentiated populations that still interbreed regularly but retain their identities by strong disruptive selection and, therefore, may be regarded as true host races. Other populations represent definite biological species, and yet others, such as the biotypes of N. lugens on cultivated rice crops, show little differentiation and are effectively parts of a pan­ mictic species. 15.5.3  Specific Mate Recognition and Sibling Species

A helpful method of approaching the problems of interpreting different degrees of host‐ or habitat‐ associated variation is to use the biological spe­ cies concept, with its emphasis on reproductive isolation in the field achieved by distinct SMRSs. Mate finding and courtship in insects is usually complex, with a sequential exchange of signals and responses in tuned receptors in the two sexes. Any complete sequence is likely to involve various types of signals and receptors, including chemi­ cal, visual, mechanical, and auditory senses. However, few complete SMRS sequences have been described and analyzed for any insect. Because of the predominance of chemical senses in insects generally, specific chemical

signals – pheromones – are usually important. These are well known among the Lepidoptera, but also occur in many orders, including the large orders Coleoptera, Diptera, and Hymenoptera. Few detailed studies on phero­ mone systems in groups of related specialist‐ feeding insects have been made, but some of the most instructive have been on small ermine moths (Yponomeuta spp.). The larvae of these insects feed on the foliage of their host plants, mostly broad‐leaved trees, where they often cause extensive defoliation. Thorpe (1929), in a classic study, showed how populations from Crataegus and Malus hybridized freely in the laboratory, but the same populations showed both feeding and oviposition preferences for the plant on which they had been reared. He con­ cluded that they were biological or host races. Subsequent study conclusively showed that these two forms do not interbreed in the field and, therefore, are separate biological species (Menken 1980). Nine species now are recog­ nized in northern Europe (Menken et al. 1992). Like many moths, virgin females of these insects “call” by liberating a specific pheromone. Responsive males are attracted maximally to the pheromone of their own species (Hendrikse 1979, 1986). When in close proximity to a call­ ing female, males produce their own specific sex pheromone, which may elicit mating behavior (Hendrikse et  al. 1984). The sequence of exchanges of signals and responses means that interspecific matings are rare. Chemical inter­ actions are thus central to the SMRS of these insects. Chemical signals are generally difficult to study. Most work has been done on single important pest species in which pheromones may be used to manipulate the behavior of the pest and, thus, can be used in control strategies. Visual and acoustic systems of communication seem to be relatively rarer in insects, but are generally easier for the human observer to study. Acoustic systems have received considerable attention in recent years and are more wide­ spread than previously thought (Drosopoulos and Claridge 2006).

15  Insect Species – Concepts and Practice

Auchenorrhyncha (Hemiptera) is a large, spe­ cies‐rich group made up exclusively of herbi­ vores. All species, so far as known, use acoustic signals (including substrate‐transmitted vibra­ tions) in mate finding and courtship (Claridge 1985). The larger cicadas (Cicadidae) are well known for their often loud male songs, which are usually species specific and attractive to vir­ gin females. The classic studies of Alexander and Moore (1962) on the well‐known and abun­ dant 13‐year and 17‐year periodical cicadas of North America showed that each group con­ sisted of three widely sympatric sibling species with distinct, loud male calls. Through ingen­ ious field experiments, they were able to show that the calls functioned in species recognition. Subsequently, many other examples of sibling species in the Cicadidae have been demon­ strated by their distinct male calls. Recently, Gogala (2013) brought together the results of his studies on the mountain cicadas of Europe, which were previously thought to be one spe­ cies, Cicadetta montana (Scopoli); instead, he showed there to be at least 13 biological species across southern and central Europe. The much more abundant and generally smaller species of other families of Auchenor­ rhyncha, such as the Cicadellidae, Delphacidae, and Membracidae, signal between males and females by low‐intensity vibrational calls that are transmitted through their substrate  –  nor­ mally the host plant on which they live. These signals usually function as important elements of their SMRSs (Claridge 1985). One of the best studies on a group of closely related insect her­ bivores was done by the late Tom Wood (1993). He studied the treehopper Enchenopa binotata (Membracidae) in North America with the hypothesis that the eight or nine host‐associ­ ated populations were host races, albeit mor­ phologically almost identical. A series of elegant electrophoretic and field experimental studies on these insects demonstrated that E. binotata consists of at least nine reproductively isolated biological species. Follow‐up studies have shown that these insects communicate by ­substrate‐transmitted acoustic signals that are

central to specific mate recognition and ­maintaining reproductive isolation (Hunt 1994, Rodríguez et al. 2004, Cocroft and McNett 2006). A further example of extreme sibling species is provided by the planthopper, Nilaparvata lugens, the rice‐feeding “biotypes” of which were shown to be populations locally adapted to particular cultivars of rice that incorporate dis­ tinctive genes for resistance. However, popula­ tions morphologically attributable to N. lugens also have been found widely feeding on the wild grass Leersia hexandra, a relative of rice, both of which frequently grow in close proximity. These populations were at first described as “non‐vir­ ulent biotypes” of N. lugens in the Philippines (Saxena et  al. 1983). Rice‐ and Leersia‐associ­ ated populations of N. lugens occur regularly in close proximity in the field throughout much of Asia and northern Australia (Claridge et  al. 1985b, 1988). Like other planthoppers, these insects exchange substrate‐transmitted acoustic signals during mating and courtship. The sig­ nals of sympatric males and females differ con­ sistently in call characteristics (Claridge et  al. 1985a, b, 1988), which act as barriers to inter­ breeding and are important parts of the SMRSs. Mate choice and call playback experiments con­ firm that call differences are responsible for the lack of detected field hybridization between these forms when in sympatry and, thus, show that they should be regarded as different bio­ logical species. In the laboratory, mate‐choice experiments showed high levels of isolation between the two host‐associated populations. However, forced hybridization between the two is easily achieved in the absence of a choice of mates, and results in viable F1 and F2 genera­ tions, with little indication of hybrid inviability. Preliminary molecular studies on these popula­ tions confirmed that they are closely related, with little obvious genetic divergence, but cast doubt on our suggestion that they represented different biological species (Jones et  al. 1996, Sezer and Butlin 1998). We argued (Claridge et al. 1985b) that the small, but consistent, dif­ ferences between calling songs of both males and females of the two host plant‐associated

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populations, together with results of mate‐ choice experiments, suggest that they should be regarded as closely related biological species of the N. lugens complex. The call differences were then the only real markers, other than host‐ plant preference, by which they could be recog­ nized. However, fuller molecular analyses on populations from the two host plants in differ­ ent regions of Malaysia support our original conclusions (Latif et al. 2008). These host‐asso­ ciated populations are, thus, extreme examples of sibling species. Allopatric populations of each of the host‐plant associated species also vary in song characters, such that many do not easily interbreed in the laboratory (Claridge et  al. 1985a, b, 1988). Thus, some might be regarded as additional separate species of the complex. A final example of the problems of closely related populations associated with different host plants is provided by the widely distributed and economically important whiteflies (Hemiptera: Aleyrodidae) known as Bemisia tabaci. These insects are major pests of many tropical crops and have invaded glasshouses across the world (Powell and Cuthbertson 2012). An enormous number of so‐called bio­ types have been recognized on the basis of dif­ ferences among whiteflies associated with different host plants. The most recent compre­ hensive review, based on refined molecular and phylogenetic analyses, rejects the biotype nomenclature and suggests that the group con­ sists of at least 24 well‐supported and geneti­ cally distinct biological species (De Barro et al. 2011). Whiteflies, although not part of Auchenorrhyncha, also use vibratory signals during courtship, but no detailed studies have been made on the B. tabaci species complex. Tantalizingly, Kanmiya (2006) described dis­ tinctive calls of two Bemisia species in Japan. Maybe there is a similar story here on a bigger scale than that described for N. lugens?

biological species concept, as advocated here, will lead to the recognition of more biological diversity than will a purely morphological and phylogenetic approach. Sibling species are important ecological entities about which sig­ nificant generalizations can be made. In prac­ tice, the application of a phylogenetic species concept by taxonomists who are sensitive to the diversity of markers available will often produce results similar to those achieved when applying the biological species concept. The main prob­ lem is that the phylogenetic approach gives little incentive to expose the existence of sibling spe­ cies within an already diagnosably distinct spe­ cies. Thus, the extent of the real biodiversity of insects, enormous as it is, may be dramatically underestimated. If the real diversity of insects in the field is to be recognized by our system of taxonomy, then the biological species concept, despite the difficulties outlined here, will incor­ porate more useful information than will other concepts available to us. Whichever approach is favored by any par­ ticular taxonomist, the enormity of the task we face in attempting to document insect diversity is clear. The lack of support for taxonomy over recent years has been based on the misconcep­ tion that it is in some way not real science. Although we will disagree about species con­ cepts, I conclude by agreeing wholeheartedly with the sentiments of Quentin Wheeler (2004) on this: “Taxonomists synthesise and interpret billions of facts about millions of species, make those species identifiable, provide the vocabu­ lary to talk about them, critically test the evolu­ tionary units of biological diversity, and make accessible and predictable all that we know of life on Earth. It has a rich and proven epistemic basis that makes its hypotheses testable and its results as rigorously scientific as any.”

15.6 ­Conclusions

Adler, P. H., A. Inci, A. Yildirim, O. Duzlu, J. W. McCreadie, M. Kúdela, A. Khazeni, T. Brúderová, G. Seitz, H. Takaoka, Y. Otsuka and J. Bass. 2015. Are black flies of the

Most insects are biparental, sexually reproduc­ ing organisms, so application of the broad‐based

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15  Insect Species – Concepts and Practice

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Ramsbottom, J. 1938. Linnaeus and the species concept. Proceedings of the Linnean Society of London 150: 192–219. Regan, C. T. 1926. Organic evolution. Report of the British Association for the Advancement of Science 1925: 75–86. Rodríguez, R. L., L. E. Sullivan and R. B. Cocroft. 2004. Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Evolution 58: 571–578. Saxena, R. C. and L. M. Rueda. 1982. Morphological variations among three biotypes of the brown planthopper Nilaparvata lugens in the Philippines. Insect Science and its Application 6: 193–210. Saxena, R. C., M. V. Velasco and A. A. Barrion. 1983. Morphological variations between brown planthopper biotypes on Leersia hexandra and rice in the Philippines. International Rice Research Newsletter 18: 3. Sezer, M. and R. K. Butlin. 1998. The genetic basis of host plant adaptation in the brown planthopper (Nilaparvata lugens). Heredity 80: 499–508. Simpson, G. G. 1951. The species concept. Evolution 5: 285–298. Sokal, R. R. and T. J. Crovello. 1970. The biological species concept: a critical evaluation. American Naturalist 104: 127–153. Sorensen, J. T. and R. G. Foottit (eds). 1992. Ordination in the Study of Morphology, Evolution and Systematics of Insects. Applications and Quantitative Genetic Rationales. Elsevier, Amsterdam. 418 pp. Sperling, F. 2003. Butterfly molecular systematics: from species definitions to higher‐level phylogenies. Pp. 431–458. In C. L. Boggs, W. B. Watt and P. R. Ehrlich (eds). Butterflies, Ecology and Evolution Taking Flight. University of Chicago Press, Chicago, Illinois. Sperling, F. A. H. and A. D. Roe. 2009. Molecular dimensions of insect taxonomy. Pp. 397–417. In: Insect Biodiversity: Science and Society. R. G. Foottit and P. H. Adler (eds). Wiley‐ Blackwell, Chichester, UK.

Strong, D. R., J. H. Lawton and R. Southwood. 1984. Insects on Plants: Community Patterns and Mechanisms. Blackwell, Oxford. 313 pp. Tautz, D., P. Arctander, A. Minelli, R. H. Thomas and A. P. Vogler. 2003. A plea for DNA taxonomy. Trends in Ecology and Evolution 18: 70–74. Tinbergen, N. 1951. The Study of Instinct. Oxford University Press, Oxford. 228 pp. Thorpe, W. H. 1929. Biological races in Hyponomeuta padella L. Zoological Journal of the Linnean Society 36: 621–634. Thorpe, W. H. 1930. Biological races in insects and allied groups. Biological Reviews 5: 177–212. Thorpe, W. H. 1940. Ecology and the future of systematics. Pp. 341–364. In J. Huxley (ed). The New Systematics. The Oxford University Press, London. Vrba, E. 1995. Species as habitat specific, complex systems. Pp. 3–44. In D. M. Lambert and H. G. Spencer (eds). Speciation and the Recognition Concept. Johns Hopkins University Press, Baltimore, Maryland. Wallace, A. R. 1865. On the phenomena of variation and geographical distribution as illustrated by the Papilionidae of the Malayan region. Transactions of the Linnean Society 25: 1–71. Wallace, A. R. 1889. Darwinism: An Exposition of the Theory of Natural Selection. MacMillan, London. 494 pp. Walsh, B. J. 1864. On phytophagic varieties and phytophagic species. Proceedings of the Entomological Society of Philadelphia 3: 403–430. Wheeler, Q. 1999. Why the phylogenetic species concept? ‐ Elementary. Journal of Nematology 31: 134–141. Wheeler, Q. D. 2004. Taxonomic triage and the poverty of phylogeny. Philosophical Transactions of the Royal Society B 359: 571–583. Wheeler, Q. D. and R. Meier (eds). 2000. Species Concepts and Phylogenetic Theory, a Debate. Columbia University, New York. 256 pp. Wheeler, Q. D. and K. C. Nixon. 1990. Another way of looking at the species problem: a reply

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Wilson, E. O. 1992. The Diversity of Life. Harvard University Press, Cambridge, Massachusetts. 424 pp. Wilson, R. A. (ed). 1999. Species, New Interdisciplinary Essays. MIT Press, Cambridge, Massachusetts. 325 pp. Wood, T. K. 1993. Speciation of the Enchenopa binotata complex (Insecta: Homoptera: Membracidae). Pp. 289–317. In D. R. Lees and D. Edwards (eds). Evolutionary Patterns and Processes. Academic Press, London.

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16 Molecular Dimensions of Insect Taxonomy in the Genomics Era Amanda Roe1,*, Julian Dupuis2 and Felix Sperling2 1 2

Natural Resources Canada, Canadian Forest Service, Great Lakes Forestry Centre, Sault Ste. Marie, Ontario, Canada Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada

Insect biodiversity is so bountiful that we need to use every means at our disposal to document and organize our taxonomic knowledge about it. Molecular methods, now aided by genomic technologies that are sweeping through ecology and evolutionary biology, have become increas­ ingly important in accomplishing the basic tasks of taxonomy (Harrison and Kidner 2011). As with any subset of the tools of taxonomy, the value of molecular methods is measured by how accurately and conveniently such methods can be used to identify and characterize the species and clades that represent insect biodiversity. In this chapter, we update our earlier review of the molecular dimensions of insect taxonomy (Sperling and Roe 2009) by focusing on high‐ throughput sequencing and other genomic advances. Most of the molecular methods that were in common use in 2009 remain rele­ vant today. We now find ourselves in a genomics era in which our capacity for molecular characteriza­ tion is nearly boundless and is poised to affect all aspects of insect taxonomy (Harrison and Kidner 2011). Complete genomes are now avail­ able for numerous arthropod species, and entire mitochondrial genomes have been sequenced for nearly 500 insect species (Cameron 2014). The cost of obtaining these data has dramati­ cally decreased and will continue to do so in the

foreseeable future (Lemmon and Lemmon 2013). This unprecedented access to data has opened doors to previously intractable ques­ tions, but has also introduced new issues that practicing taxonomists must confront. We focus on three facets of the emerging rela­ tionship among taxonomy, systematics, and genomic methodology. We begin by addressing taxonomy conceptually, considering the four fundamental problems in taxonomic science. Then, we briefly summarize the main types of genomic platforms and technologies that are currently widely available, and identify how var­ ious approaches are tailored for different taxo­ nomic questions. Finally, we address the interaction between taxonomy and genomics from the viewpoint of a practicing taxonomist who is just beginning to delve into the genomic revolution; this latter section will have a phylo­ genetic focus that has broad application to all themes in taxonomy.

16.1 ­Opportunities in Insect Taxonomy Molecular taxonomy is not a parallel approach to insect taxonomy. Rather, molecular methods are an important part of a more holistic, inte­ grative taxonomy, and provide diverse additional

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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character sets for addressing classical taxo­ nomic problems (Sperling and Roe 2009). Taxonomy is a venerable discipline that remains both vibrant and fundamental to the rest of biology (Sluys 2013); the use of molecules of all kinds adds depth and new dimensions to this field of study. Practicing taxonomists encounter an array of logical puzzles, the complexity of which is matched only by the profound satisfaction of resolving them. Despite their endless variety, the details of these puzzles can be reduced to varia­ tions on four basic themes: (i) determination of the identity of specimens of known species, (ii) discovery of new species, (iii) delimitation of species boundaries, and (iv) phylogenetic recon­ struction. Molecular methods are helpful, to varying degrees, in resolving each of these four kinds of problem (the first letters of which com­ prise a euphonious acronym  –  D3P). Here we explore how next‐generation sequencing (NGS) techniques are used to answer taxonomic ques­ tions within the D3P framework (Sperling and Roe 2009). Then we ask what new opportunities NGS methods provide and what challenges an insect taxonomist faces when applying these techniques to a taxonomic problem. 16.1.1 Determination

The process of identifying specimens as members of previously demarcated species has benefited greatly from the use of molecular characters, par­ ticularly in cases in which morphological charac­ ters are insufficient. This is a logically simple problem in which the integrity of the boxes (spe­ cies) is fully resolved, but we have too few useable characters to place a specimen into the correct box. Molecular methods provide an immense array of new characters that may assist identifica­ tion, as long as their utility has been thoroughly tested beforehand. Any source of information, such as a single nucleotide, an enzyme allele, or a hydrocarbon variant, may serve to identify a pre­ viously characterized species. Large‐scale biodiversity assessments generally seek to place sampled organisms into previously

determined bins, rather than identifying new species or lineages. Using morphology‐based or traditional DNA barcode identification for these projects can be costly and time consuming (Gibson et  al. 2014), particularly when dealing with thousands of individuals, different life stages, isolated body parts, or specimens bereft of morphologically diagnostic information. NGS has emerged as a partial solution for streamlining taxonomic determinations in large‐scale biodiversity studies, and costs may be equal to or less than that of a morphology‐ based diagnostic system (Stein et al. 2014). One approach, termed DNA metabarcoding (Hajibabaei et  al. 2011, Taberlet et  al. 2012, Cristescu 2014), uses the massively parallel nature of NGS to automatically identify organ­ isms within a bulk or environmental sample. Heralded as a boon to biodiversity studies, metabarcoding has the potential to streamline and speed up the characterization of organisms in large‐scale surveys, eliminating the need to sort and isolate target organisms within each sample (Hajibabaei et al. 2011, Cristescu 2014). The application extends beyond biodiversity studies, and can be used to gain insights into trophic ecology (Clare 2014), endosymbiont diversity (Andrew et al. 2013, Gibson et al. 2014, Paula et al. 2015), food webs (Clare 2014), and diet ecology (Gariepy et  al. 2012, Pompanon et al. 2012). An important complication arises, however, from reliance on any single standardized genomic region, such as 16S ribosomal RNA or cytochrome c oxidase subunit I (COI), even with an NGS approach. Often, a single genomic region is not sufficient to resolve closely related species (Roe and Sperling 2007a, 2007b; Roe et al. 2010; Dupuis et al. 2012), and many groups of organisms require at least two regions to ensure accurate species identifications (CBOL Plant Working Group 2009, Carew et al. 2013). Any molecular marker must be effectively vali­ dated and verified prior to use as a standard reference region (Taberlet et  al. 2012), and researchers should be aware of the potential for biased amplification that can skew or mislead

16  Molecular Dimensions of Insect Taxonomy

biodiversity assessments (Clarke et  al. 2014, Piñol et al. 2014). As NGS technology continues to advance, the field probably will move away from any single or small set of markers, instead focusing on limited shotgun sequencing to pro­ vide suitable coverage of nuclear DNA, as well as organellar DNA, reducing the need for short standardized regions (Taberlet et al. 2012). The foundation of any determination system is the clear demarcation of “boxes” that repre­ sent individual species. DNA metabarcoding requires comprehensive taxonomic reference libraries to accurately identify the organisms in samples (Shokralla et al. 2014). When tied to a robust reference database, the use of diagnostic molecular markers for specimen determination can be quite effective (Hendrich et  al. 2015, Zahiri et al. 2014), although the reference data­ base must be based on a validated and vouchered reference collection (Carew et  al. 2013), a resource that might not yet exist for some groups or might be limited in its geographic focus (Shokralla et al. 2014). To validate effective identification, the natural range of character variation must be well docu­ mented so that we can be confident in the iden­ tification of a single specimen, regardless of where the specimen came from (Bergsten et al. 2012). But how well should the range of charac­ ter variation be known? For cases that really matter, one benchmark is whether the identifi­ cation would hold up in a court of law. Such a standard is not frivolous; insect identifications often support holding up large, perishable ­shipments at ports, expensive eradications of invasive species, or forensic evidence in murder convictions. A 95% probability of correct identi­ fication will not convince a judge who is ­weighing the human cost of a mistake, nor is it likely to deter a sharp corporate lawyer defend­ ing a shipping company. Furthermore, estima­ tion of the probability of correct identification relies on certain assumptions that are difficult to quantify. For example, have all relevant spe­ cies been discovered? Have these units been accurately delimited? Are their frequencies of occurrence known?

16.1.2 Discovery

One of the most obvious applications of molec­ ular methods in taxonomy is to provide new sets of characters that show clear discontinui­ ties in assemblages that were previously seen as more or less continuous. Molecular characters are not fundamentally different from any other kind of characters, although some molecular markers, such as fast‐evolving genes, may be more likely to allow the detection of new spe­ cies. In the past, the presence of a new species was almost always first suspected on the basis of ecological, behavioral, or morphological varia­ tion. With the introduction of large‐scale molecular surveys, cryptic diversity is increas­ ingly being discovered with genetic surveys prior to knowledge of morphological or ecologi­ cal differentiation (Webb et al. 2012, Smith et al. 2013, Bertrand et al. 2014). The discovery of new taxonomic units comes with some inherent risks. As the efficiency of NGS‐powered molecular processing catches up to basic visual methods, there will be a strong temptation to rely on only those molecular markers that are easily assayed. Single‐marker taxonomic systems risk creating an operational dilemma whereby the new units that are discov­ ered are self‐referentially consistent but might have limited relevance to genomic or morpho­ logical diversity (Schmidt and Sperling 2008, Kodandaramaiah et  al. 2013). Thus, it may be better for the stability of communication in tax­ onomy to leave the discovery of a divergent gene lineage (as is increasingly common for mito­ chondrial DNA) for further evaluation using other characters (Taylor and Harris 2012, Kodandaramaiah et  al. 2013, Bertrand et  al. 2014), rather than drawing immediate and potentially disruptive taxonomic conclusions that are still vulnerable to falsification. One problematic outcome of broad‐scale molecular surveys is the creation of “dark taxa” (Page 2011). These are molecular lineages that lack proper Linnaean binomial nomenclature and are vouchered as such within a data repository such as GenBank. In the case of dark taxa, this

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molecular information has become disconnected from other taxonomic or biological information owing to the lack of a proper scientific name. It is impossible to know whether these individuals represent a new species or are already known to science. This issue ties back to the importance of a robust reference library and vouchered collec­ tion to confidently identify novel species. As the accumulation of data from NGS increases, efforts must be made to ensure that molecular data are properly tied to the Linnaean hierarchy, as well as to additional metadata, such as morphology and ecology. Furthermore, some protocols used for conducting large‐scale biodiversity surveys lead to the destruction or absence of voucher speci­ mens (i.e., Hajibabaei et al. 2011). If a novel line­ age is discovered and represents a new species, linking the genetic lineage to a holotype specimen could be difficult or even impossible. Refinement of sample techniques, such as the extraction of DNA from the preservation fluid rather than the entire tissue sample, may help to minimize the  destruction of valuable voucher material (Hajibabaei et al. 2012). However, linking individ­ uals within a bulk sample to individual NGS sequences remains difficult unless the survey is  laboriously repeated by sampling single individuals. 16.1.3 Delimitation

Any reference to species delimitation raises the question “what is a species?” This question seems usually to invite an endless cycle of dis­ cussion and disagreement. An overview of vari­ ous species concepts is given in this volume by Claridge. We focus here on species delimitation as an exercise in determining the degree to which populations maintain their genomic integrity (Sperling 2003a) or, in alternative phrasing, the permeability of genetic bounda­ ries between population lineages (Mullen and Shaw 2014). The enormous number of markers that can be genotyped using NGS makes this technology a powerful tool for visualizing genomic permeability and understanding the process of speciation (Seehausen et  al. 2014).

Patterns of genomic divergence among popula­ tions or closely related species can be surveyed through various methods that we discuss in greater detail below, such as genome scans with single‐nucleotide polymorphism (SNP) arrays (Nosil et  al. 2012, Lumley and Cusson 2013, Leaché et  al. 2014), reduced representation libraries (Nadeau et al. 2013, Wagner et al. 2013, Mastretta‐Yanes et  al. 2014), or transcriptome sequencing (Comeault et al. 2012, De Wit et al. 2012). These data can help to identify regions of genomic divergence (Nosil et al. 2009, Lawniczak et  al. 2010, Nadeau et  al. 2012) that may be linked to functional genes (Dalziel and Schulte 2012, Diz et  al. 2012), proteins (Andrés et  al. 2013), adaptive loci (Nadeau and Jiggins 2010, Pardo‐Diaz et  al. 2015), or hybridization (Gompert et  al. 2014, Nadeau et  al. 2014). By examining patterns of genomic variation in a range of taxa along the speciation continuum, it should be possible to identify signatures of extrinsic and intrinsic events that lead to repro­ ductive isolation and ultimately to biological diversity (Seehausen et al. 2014). Regardless of the nuances of the particular species definition that may be employed by a working taxonomist, or the mode by which spe­ cies boundaries arose, it is important to view each species as a testable hypothesis (Ebach et  al. 2011, Sluys 2013). Such a hypothesis should be tested against multiple data types, preferably with disparate analytical properties, using a range of analytical methods to ensure that biological diversity is accurately delimited (Carstens et  al. 2013). Here again, molecular data have proven to be highly useful. An inte­ grated approach (i.e., Schlick‐Steiner et al. 2010) to species delimitation remains essential to resolving taxonomic problems in recently diverged species groups (Dombroskie and Sperling 2013, Lumley and Cusson 2013, Satler et al. 2013, Pante et al. 2014). The copious and repeated nature of nucleotide sequences makes DNA particularly suited to quantitative analysis for delimiting taxa. One such quantified measure is the degree of diver­ gence (e.g., genetic distances calculated as

16  Molecular Dimensions of Insect Taxonomy

percentage similarity) between populations or between taxonomic groups at the level of species and above. Simple methods include defining species as terminal clusters on neighbor‐joining trees (Hebert et al. 2003), using a standard inter­ specific “barcode gap” of 1–3% (Hebert et  al. 2003a, 2003b; Smith et al. 2009; Tang et al. 2012; Stahlhut et al. 2013), or an interspecific distance of 10 times the intraspecific distance (Hebert et al. 2004). However, even though uniform dis­ tance‐based clustering methods are informative in a preliminary assessment, this approach has serious limitations due to the large amount of overlap in divergences between different taxo­ nomic ranks (Cognato 2006, Nazari et al. 2007, Hendrich et  al. 2010). More‐sophisticated approaches to delimiting species on the basis of barcode gaps include Automatic Barcode Gap Discovery (ABGD: Puillandre et al. 2012). Other programs may take into account evolutionary processes, such as the Generalized Mixed Yule Coalescent (GMYC) model, which estimates the point at which there is a transition between dif­ ferent kinds of branching patterns (Pons et  al. 2006, Fontaneto et  al. 2007). Mutanen et  al. (2014) provide an excellent comparison of these different methods and the potential pitfalls of these techniques when clarifying taxonomic boundaries. Character‐based approaches also can be used with molecular data to delimit species and other taxa, making them conceptually compatible with classical taxonomic practice (DeSalle et al. 2005, Rach et  al. 2008). For example, the sec­ ondary structure of the internal transcribed spacer 2 (ITS2) region can provide a molecular character‐based approach to identify species limits; compensatory base changes (CBCs) alter the secondary structure in ITS and have been proposed as markers to delimit biological spe­ cies (Müller et al. 2007). Intragenomic variation within individuals can complicate the inference of species limits (Song et  al. 2012, Wolf et  al. 2013, Bertrand et  al. 2014), but with NGS sequencing, intragenomic variability can be assessed independently to determine species limits (Wolf et al. 2013, Bertrand et al. 2014).

Single molecular markers have provided enormous benefit to taxonomy when combined with other characters and the biology of the whole organism. For many insects, particularly in temperate zones, a good first draft of regional species assemblages is available based on stand­ ard morphological methods (Zahiri et al. 2015). The undescribed remainder is a combination of rare species, species groups with poor morpho­ logical distinctions, or legitimately messy spe­ cies boundaries where delimitation based on single genes can be highly error‐prone (Funk and Omland 2003, Meier et al. 2006, Monaghan et  al. 2006, Linnen and Farrell 2007, Trewick 2008, Dupuis et  al. 2012). These difficult‐to‐ delimit species often have substantially different economic consequences, and yet such species complexes are also the very ones that are most likely to be resistant to effective characteriza­ tion using single‐gene systems of any kind (Sperling 2003b). Their messy boundaries reflect the fact that genomes of recently diverged species represent a mosaic of molecular ances­ try (Ting et  al. 2000), as influenced by both adaptive and neutral processes (Andrew et  al. 2013). Divergence may be limited to small regions of the genome (i.e., genomic islands, Nadeau et al. 2012), and reproductive isolation might have existed too briefly for divergence to accumulate in other genomic regions. Some genomic regions are more likely than others to show divergence. Speciation genes (Nosil and Schluter 2011, Nosil and Feder 2012, Fontaine et  al. 2014), sex chromosomes (Garrigan et  al. 2014, Lima 2014), and sex‐linked genes (Sperling 1993, Roe and Sperling 2007a, Corl and Ellegren 2013, Martin et al. 2013) have shown promise in clarifying species boundaries that could not be resolved using genes undergoing neutral selection. Ultimately, NGS presents opportunities to obtain a genic view of speciation and to reveal the genomic mosaic that characterizes recently diverged species. NGS illuminates genomic properties of species along the species contin­ uum and can help to detect the tipping point at which reproductive isolation ceases to be a

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property of a few select genes and becomes a property of the genome (Feder et al. 2014). Key advances will be made when NGS data are inte­ grated across multiple disciplines, such as ecol­ ogy, behavior, and developmental biology, particularly when examined across a range of non‐model organisms (Ekblom and Galindo 2011). As genome‐wide data are gathered for more species, comparisons of the genetic signa­ tures of varied modes of reproductive isolation might be possible, allowing a more general understanding of speciation, as well as practical applications, through more accurate species delimitation. 16.1.4 Phylogeny

Phylogenetic reconstruction is a key component of taxonomy, and is pivotal to the implementa­ tion of the three Ds of D3P. Although molecular data have had mixed utility in reconstructing phylogenies above the level of species (Sperling and Roe 2009), NGS is propelling phylogenetics to new levels. Before the emergence of NGS, phylogenetic data were limited by the number of loci and taxa that could be sequenced. NGS technologies have now given rise to the field of phylogenomics, which infers evolutionary rela­ tionships using hundreds, if not thousands, of loci spread throughout the genome for hun­ dreds of taxa (Misof et al. 2014). Genes differ in their divergence rates, and some are best suited for shallow phylogenetic reconstruction (i.e., mitochondrial DNA; Nazari et  al. 2007), whereas others retain traces of their cladistic pattern of nested subsets of mutations from deeper historical relationships. Shallow evolutionary relationships can be dif­ ficult to resolve because differentiation may be limited to a few parts of the genome, and such regions of rapid divergence may be challenging to identify (Hare 2001). NGS methods allow thousands of characters to be surveyed through­ out the genome, increasing the chance of identi­ fying informative loci (Lemmon et  al. 2012, Cruaud et al. 2014). Deep phylogenies can also be challenging to reconstruct with molecular

data because of the overlay of multiple character substitutions over time (i.e., saturation) and the short time period represented by internodal dis­ tances relative to total branch length (Whitfield and Kjer 2008). The challenge is to find and con­ sistently sequence genes that are informative at a particular taxonomic level and homologous across a group, and to employ the most appro­ priate analytical methods. Methodological approaches, discussed below, are emerging to mediate this challenge. NGS has presented opportunities to assay novel, non‐nucleotide‐based, molecular charac­ ters. Large‐scale genomic features, such as gene content, gene order, introns, unique gene struc­ tures, retrotransposons, copy number variation, and microRNAs (Telford and Copley 2011, Bernt et  al. 2013, Tarver et  al. 2013, Cameron 2014, Duvaux et al. 2014, Thomson et al. 2014), can provide novel features that can be used to infer deep phylogenetic relationships or to cor­ roborate relationships inferred using primary sequence information (Delsuc et al. 2005). These novel characters also can help to resolve evolu­ tionary relationships that defy resolution with more commonly used traits (Tarver et al. 2013). Rota‐Stabelli et al. (2011), for example, demon­ strated that microRNAs support pancrustacean relationships resolved from sequence‐based analyses (Regier et al. 2010) and traditional mor­ phology‐based classification (Edgecombe and Legg 2014), refuting previous phylogenomic reconstructions that conflicted with traditional classification schemes (Janssen and Budd 2010). It is important to scrutinize how novel molecu­ lar characters are collected and analyzed to min­ imize potential sampling error and analytical biases that can dramatically change phyloge­ netic relationships (Thomson et al. 2014). With the increased availability of NGS, inter­ esting phylogenetic questions can be explored without the need to generate new data. For example, publicly available data have been used to reassess phylogenetic relationships among beetles (Bocak et al. 2014) and hymenopterans (Peters et  al. 2011), and to address interesting evolutionary questions, such as the timing of

16  Molecular Dimensions of Insect Taxonomy

the Cambrian explosion and the evolution of flight within the Arthropoda (Wheat and Wahlberg 2013). These data also can be used to augment a particular study, thereby reducing the cost of generating new sequence data.

16.2 ­Genomic Methods 16.2.1  Sequencing Technologies

In the past decade, there has been an unprece­ dented development of new molecular tech­ niques (Lemmon and Lemmon 2013). Previously, an immense amount of resources was needed to obtain more than 100 markers for a small group of taxa; now, thousands of markers for hundreds of individuals can be obtained routinely. Such developments have meant that taxonomists and systematists have access to vast quantities of data for a wide range of species, including non‐model organisms. Access to molecular data has led a conceptual shift in approaches to dealing with these data within a taxonomic or systematic framework. We focus our discussion on emerging molecu­ lar technologies. More‐established molecular techniques have been discussed elsewhere (Sperling and Roe 2009). Targeted nucleotide sequencing has been the dominant molecular method in insect taxonomy for nearly three dec­ ades. The first widespread manifestations of this technique are referred to as Sanger sequencing (Sanger et al. 1977) or first‐generation sequenc­ ing. This technique amplifies single regions of DNA, using conserved primer regions, which are individually sequenced on a first‐generation sequencing platform, such as the ABI DNA Analyzer (Life Technologies, Carlsbad, CA, USA). Initial data collection is time and labor intensive, as each organism is independently processed and each genomic region is amplified and sequenced individually. The costs of obtain­ ing these data generally limited studies to less than 100 loci for a moderately sized taxonomic group (Harrison and Kidner 2011, Faircloth et  al. 2012). However, data analysis following data collection is relatively straightforward

owing to the manageable size of the data sets and a priori assessments of gene region orthol­ ogy (McCormack et al. 2013). Over the past five years, there has been a wide­ spread shift from reliance on traditional Sanger sequencing to NGS, also known as massively parallel sequencing or high‐throughput sequenc­ ing. The general workflow for an NGS project proceeds as follows: platform selection, marker development, NGS generation, assembly, identi­ fication of orthologs, gene alignment, and analy­ sis. NGS simultaneously reads libraries of labeled DNA templates, producing millions of base pairs of data in a single sequencing run, which are then processed for quality control, assembled, and analyzed based on the question of interest. The time investment and cost per fragment of obtaining data have been dramatically reduced relative to Sanger sequencing (Buerkle and Gompert 2012, Carstens et  al. 2012), giving access to vast quantities of genomic data spread throughout the genome, even for non‐model organisms (Ekblom and Galindo 2011). Although up‐front time investment is reduced, the signifi­ cant resources required to process these large volumes of data have become the primary bot­ tleneck in current NGS approaches, which we will discuss in the third section. A number of NGS platforms are currently available, which vary in the chemistry and base incorporation‐detection technologies used to obtain sequence data, as well as in their inherent biases and limitations (Glenn 2011, Lemmon and Lemmon 2013). This field is constantly evolving and may change dramatically in the span of a few months. We, therefore, provide a broad overview of the currently available tech­ nologies, rather than focusing on detailed differ­ ences between platforms. NGS platforms can be classified as based on either PCR or single‐mol­ ecule sequencing (Shokralla et  al. 2012). PCR‐ based technologies include 454 pyrosequencing (Roche 454 Life Sciences, Branford, CT, USA), Illumina sequencing (Illumina Inc., San Diego, CA, USA), AB SOLiD™ System (Life Technologies Corp., Carlsbad, CA, USA), and Ion Torrent Sequencing (Life Technologies, Carlsbad, CA,

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USA). PCR‐based systems are considered to be short‐read platforms, with read length (i.e., sequence length) ranging from 300 base pairs (bp) to 700 bp, and many platforms produce only 100 bp reads (Shokralla et al. 2014). These platforms all use pre‐sequencing PCR amplifica­ tion and, therefore, they bias template amplifica­ tion, leading to base‐pair composition bias that results in poor sequencing coverage for some genomic regions (Zhou and Rokas 2014). The resulting gaps in coverage can then impede downstream assembly and post‐processing. Paired‐end sequencing of DNA fragments of particular sizes, such as 2 kb, can help to over­ come some of the limitations of sequencing short fragments (Zhou and Rokas 2014). The alternative to PCR‐based NGS is the sin­ gle‐molecule, real‐time sequencing platform (SMRT), and this technology is currently only available through the PacBio RS SMRT system (Pacific Biosciences, Menlo Park, CA, USA). Helicos BioSciences Corp. previously supported an alternative SMRT platform, HeliScope, but declared bankruptcy in early 2014. SMRT tech­ nology offers longer read lengths than provided by PCR‐based technologies (>14,000bp, with the longest reads greater than 40,000 bp; www. pacificbioscience.com), which is particularly useful when assembling scaffolds for whole genomes or organellar genomes (Ferrarini et al. 2013). The disadvantages of an SMRT platform are higher error rates, higher costs relative to PCR‐based platforms, and a need for greater starting quantities of DNA (Liu et  al. 2012, Quail et al. 2012). 16.2.2  Genomic Sampling Strategies

In addition to the choice of platforms, research­ ers can choose from a range of genomic sam­ pling approaches that will determine what sequence data are obtained from an NGS run. The phylogenetic focus of taxonomy has led to three main approaches: whole‐genome sequenc­ ing (WGS), mitochondrial genome sequencing, and genomic partitioning. WGS, as the name implies, results in the complete sequencing of

an organism’s genome. Initiatives such as the i5K Initiative seek to facilitate the production and dissemination of 5000 complete arthropod genomes (i5K Consortium 2013), which will provide a wealth of information to the research community. Even with our current technologi­ cal advances, high‐quality WGS is still non‐triv­ ial, costly, and time‐consuming (Ekblom and Wolf 2014, Xia et  al. 2014). Whole‐mitochon­ dria sequencing has advanced further than WGS in insects and has become an important source of data for phylogenomic analyses (Cameron 2014). The PCR‐based and SMRT platforms can be used to generate whole genomes or mitogenomes from target taxa (Timmermans et  al. 2010, Chen et  al. 2014). Based on trade‐offs among costs, read length, error rates, post processing, and DNA quantity, combining NGS runs from a PCR‐based plat­ form and an SMRT platform shows promise in delivering high‐quality finished genomes (Ferrarini et al. 2013). The remaining approaches use genomic parti­ tioning, whereby a subset of the entire genome is sampled, and are implemented on PCR‐based NGS platforms (Lemmon and Lemmon 2013). Five main partitioning strategies can be used: (i) targeted amplicon sequencing, (ii) reduced rep­ resentation libraries, (iii) hybrid enrichment, (iv) transcriptome sequencing, and (v) prot­ eomics. Lemmon and Lemmon (2013) provide an excellent evaluation of the platforms and approaches encompassed by NGS in the context of systematics and taxonomy. Targeted amplicon sequencing (TAS) (Bybee et  al. 2011) and an associated method, mas­ sively parallel uniplex PCR (Tewhey et al. 2009), pool PCR products obtained using individual primer sets to create a multiplexed library that is sequenced on an NGS platform. Multiplexing in an NGS context refers to the tagging or bar­ coding of DNA fragments so that multiple sam­ ples can be combined into a single lane within an NGS platform. Samples are then separated bioinformatically during post‐processing. TAS requires high initial investment in primer development, and PCR must be performed for

16  Molecular Dimensions of Insect Taxonomy

each individual at each locus, as in Sanger sequencing, but this approach permits longer read lengths and saves on bioinformatics post‐­ processing (Lemmon and Lemmon 2013, McCormack et al. 2013). Reduced representation library sequencing (RRL) includes a range of methods that rely on restriction enzyme digestion of the genomic DNA, followed by size fractioning, library prep­ aration, and sequencing. Different variations of this method include restriction‐site‐associated DNA sequencing (RAD‐seq; Miller et  al. 2007, Baird et  al. 2008), genotyping‐by‐sequencing (GBS; Elshire et al. 2011), complexity reduction of polymorphic species (CRoPS; van Orsouw et  al. 2007), and multiplex shotgun genotyping (MGS; Andolfatto et  al. 2011). Multiplexing of potentially hundreds of specimens into single sequencing lanes makes these approaches cost effective, although they suffer from PCR ampli­ fication bias (Davey et  al. 2012, Arnold et  al. 2013, DaCosta and Sorenson 2014) and from an increasing proportion of missing data as phylo­ genetic divergence increases (Cariou et al. 2013, Cruaud et al. 2014). These approaches originally were designed to generate large data sets of SNPs (Baird et al. 2008), and the most commonly used methods still focus on the generation of thousands of SNPs. Consequently, the use of these data sets for phylogenetic analyses, par­ ticularly in the absence of a good genomic refer­ ence, is generally limited to sequence lengths of ≤ 100 bp. This property imparts unique meth­ odological considerations for phylogenetics. Despite short reads, RAD‐seq data sets have been empirically used to reconstruct phyloge­ nies from shallow (10,000–20,000 years ago; Emerson et  al. 2010, Merz et  al. 2013) to mid‐ levels (˜2–20 mya; Nadeau et  al. 2013, Cruaud et  al. 2014) of divergence in insects; in silico experiments show utility up to 60 million years of divergence in Drosophila (Rubin et al. 2012). Apart from phylogenetics, RRL approaches also can be used to investigate species bounda­ ries and intraspecific diversity (Wagner et  al. 2013, Lozier 2014, O’Loughlin et al. 2014), and provide a high‐density approach to assessing

ranges of character variation. Another approach for such determination questions is the use of SNP genotyping arrays (“SNP‐chips”; e.g., Shen et al. 2005), which genotype thousands of SNPs for species with well‐known genomes. The cost of these technologies and the required genomic knowledge generally limit the use of SNP‐chips to model organisms, although they have been used for insect pest species (Neafsey et al. 2010). Hybrid enrichment (also called sequence cap­ ture or target enrichment) uses probes to cap­ ture specific regions of the genome to create a large, enriched library of homologous genomic regions that will amplify across a chosen range of taxa (Mamanova et  al. 2010, Faircloth et  al. 2012, Lemmon et  al. 2012, Lemmon and Lemmon 2013, Li et  al. 2013). This approach differs from RRL in that genome reduction is non‐random, and the use of tiled (overlapping) probes facilitates longer sequences after bioin­ formatic processing. Disadvantages are the need for prior genomic or transcriptomic knowledge and up‐front costs of designing the enrichment probes (McCormack et al. 2013). Ultraconserved elements (UCEs), which are conserved regions of the genome flanked by variable regions (Glazov et al. 2005, Faircloth et al. 2012), show great promise for resolving deep‐ and shallow‐ level phylogenies (Faircloth et  al. 2015, Smith et  al. 2014). The main developers of UCEs for phylogenetics have set an excellent precedent by making their probe designs “open‐source” (http://ultraconserved.org), thus reducing some of the bioinformatic costs in designing probes. Transcriptome sequencing (RNA‐seq) tar­ gets the messenger RNA (mRNA) fraction from an organism or tissue, generates complemen­ tary DNA (cDNA) with reverse transcriptase, and uses the cDNA to build a library of cDNA fragments, which are then sequenced on an NGS platform. Unlike the previous techniques, mRNA represents the fraction of the genome that is currently being expressed within an organism, and can link the phenotype of an organism to its underlying genotype (Ferreira et al. 2013), as well as provide genomic resources suitable for a range of taxonomic questions

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(Breinholt and Kawahara 2013, Cutter 2013, Kawahara and Breinholt 2014, Misof et al. 2014, Schultheis et  al. 2014). Disadvantages of this technique are the high up‐front costs and the requirement of large quantities of high‐quality RNA (Gayral et al. 2011, Lemmon and Lemmon 2013, McCormack et  al. 2013), which will be challenging, if not impossible, to obtain for field‐caught specimens or museum material. Transcriptomic sequencing can provide valua­ ble resources with which to develop probes for hybrid enrichment, and to improve gene anno­ tation in draft genome assemblies (Denton et al. 2014). Proteomics is a further extension of transcriptomics, whereby variation in expressed proteins is detected, which can identify genes involved in local adaptation, providing impor­ tant insights into the process of adaptation and speciation. Proteins also can reflect a pheno­ type better than can the RNA fraction of the genome and show a clearer link between selec­ tion and observed phenotype (Dalziel et  al. 2009, Dalziel and Schulte 2012), although this technique is not commonly used in insect tax­ onomy at present. The choice of NGS platform and sampling strategy is a trade‐off among read lengths, error rates, post‐processing methods, costs, and queue time (Glenn 2011, Harrison and Kidner 2011, Buerkle and Gompert 2012, Lemmon and Lemmon 2013, Willette et  al. 2014). The approach that is used ultimately will depend on  the hypothesis, target organism, available genomic and bioinformatic resources, and costs. It is imperative to identify the hypothesis of greatest interest and select the most appro­ priate molecular tool to answer that question. The most advanced NGS methodology is not always the most appropriate.

16.3 ­General Challenges and Considerations The greatest benefit of NGS approaches also can be its greatest challenge  –  data quantity. The phrase “drinking from a fire hose” is

particularly apt when faced with data from even a single NGS run, which can generate from 1 million to more than 1 billion sequences (also referred to as reads). As NGS becomes incorpo­ rated into the taxonomist’s tool kit, a paradigm shift will be necessary because only a fraction of the available data may be needed to resolve a particular taxonomic question. Consequently, each taxonomic question should be approached with thoughtful experimental planning, a pro­ cess well described by Godden et al. (2012). For example, is the taxonomic problem phylogenet­ ically shallow or deep? Is the interest in genomic, transcriptomic, or proteomic information? How many taxa or individuals will be needed to resolve the hypothesis? Are the bioinformatic infrastructure and personnel in place to manage the NGS data when they are available? Are addi­ tional genomic resources (a reference genome) available to facilitate post‐processing, and are they of high quality? Thoughtful experiment design will do much to ease the bioinformatic burden downstream and ensure that the ques­ tion of interest is addressed in the most eco­ nomical way possible (McCormack et al. 2013). 16.3.1  Data Quantity Versus Quality

To resolve any taxonomic problem, taxonomists are faced with two sources of error: stochastic error (a lack of precision) and systematic error (a lack of accuracy). NGS can help to alleviate the stochastic error by increasing the amount of data available for inferring phylogenetic rela­ tionships or species limits. Systematic error, on the other hand, can increase as the amount of data increases (Philippe et al. 2005, 2011), and as NGS data sets dramatically increase in size, sys­ tematic error becomes more pronounced (Delsuc et al. 2005). Researchers ultimately must seek to balance the ratio of phylogenetic signal to noise to reliably estimate species boundaries and phylogenetic relationships (Lemmon and Lemmon 2013). Systematists have been trained to use all ­available data to reconstruct phylogenetic rela­ tionships or determine limits between putative

16  Molecular Dimensions of Insect Taxonomy

species, given the substantial effort needed to extract molecular or morphological data from a set of taxa. With NGS, the effort needed to obtain data has been substantially reduced, and now data subsampling and quality control (QC) is a crucial step in the NGS analytical workflow (Paszkiewicz et  al. 2014, Trivedi et  al. 2014). With Sanger sequencing, chromatograms were obtained for every fragment and checked indi­ vidually. Because chromatograms show the sig­ nal strength of each nucleotide, a sense of data quality could be gained. With raw NGS data, it is not feasible to check the quality of even a frac­ tion of the reads that are generated; researchers must instead rely on alternative methods for QC. These methods depend on the methodo­ logical approach and sequencing platform. Zhou and Rokas (2014) provide a thorough treatment of QC for NGS data and programs to assist the process. One of the largest hurdles for taxono­ mists who are accustomed to a Sanger sequenc­ ing approach may be to become comfortable with throwing away millions of sequencing reads and gigabytes of data. The insightful assessment by Lemmon and Lemmon (2013) cautions that researchers need to escape the dogma “that a large amount of phylogenetic information will overcome any phylogenetic error.” 16.3.2  Phylogenetic Considerations

Most, if not all, taxonomic questions are con­ cerned with phylogenetic reconstruction. Whether the objective is determination, delimi­ tation, or discovery, a thorough understanding of the phylogenetic landscape surrounding the taxon of interest facilitates accurate taxonomic conclusions. The voluminous (and potentially phylogenetically informative) data created by NGS bring many considerations that stand in the way of accurate phylogenetic reconstruc­ tion; some of these are new methodological issues, whereas others are old conceptual acquaintances of practicing systematists. 16.3.2.1  Locus Selection

The number of loci needed to answer a particu­ lar question will depend on the time scale of the

phylogenetic question, population size, and locus properties. Some questions might need only sev­ eral informative loci, whereas others might take several hundred or thousand. Taken to an extreme, if all that is needed to determine the identity of an invasive insect is a single informa­ tive SNP, then obtaining large volumes of NGS data would be overkill. That said, outside a pure determination context where robust validation exists, multiple markers or sources of evidence probably will be needed to confidently address taxonomic or systematic questions in the D3P framework. In the Sanger sequencing days, locus selection was a fundamental step in experimen­ tal planning. Although some approaches still require the selection of loci a priori (e.g., TAS and, in part, hybrid enrichment), many NGS approaches use random genomic subsampling and perform locus selection after the data have been obtained. Even approaches with a priori locus selection, such as hybrid enrichment, fur­ ther subsample loci post‐sequencing to deal with missing data and systematic error (Lemmon and Lemmon 2013). Loci can be selected based on a number of criteria, such as orthology, allele sequences, alignment accuracy, and informative­ ness (Townsend et al. 2012, Boussau et al. 2013, Chan and Ragan 2013). Regardless of sequencing platform and locus selections, almost all approaches will have to grapple with orthology in NGS data sets. Loci traditionally used for molecular taxonomic pur­ poses have generally undergone extensive scru­ tiny to ensure that single‐copy orthologous gene regions are being amplified (e.g., Regier et  al. 2010), although some commonly used genes are notorious for issues of intragenomic variability (e.g., ITS2; Wolf et al. 2013). With NGS, there is less control over which regions of the genome are sequenced, making it more difficult to ensure that orthologous gene regions are being ampli­ fied. Additionally, the sheer amount of sequence data returned from NGS approaches increases the chances that researchers are encountering problematic, paralogous regions of the genome. Often indirect, automated measures of orthol­ ogy are used to assess the single‐copy nature of a

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locus or to select a set of data that represents a single ortholog, such as number of alleles or excessive heterozygosity (Kristensen et al. 2011, Boussau et  al. 2013). In any case, the methods used to identify orthologous gene regions must be based on explicit and reproducible criteria (Giribet and Edgecombe 2012). 16.3.2.2  Missing Data

Phylogenomic data sets are frequently plagued by missing data (Roure et  al. 2013), sometimes up to 80% (Hejnol et  al. 2009). Even data sets developed from single‐locus PCR and tradi­ tional Sanger sequencing are by no means com­ plete (e.g., 18% missing in Regier et  al. 2010). Sequence gaps in NGS data sets may result from technical issues, such as PCR failure or low sequence coverage, or may be due to gene loss, horizontal gene transfer, or paralogy (Roure et al. 2013). Often these data are not randomly distributed and may be concentrated within spe­ cific clades owing to ascertainment bias from locus selection (Faircloth et al. 2015), which can have significant impacts on the resulting analy­ ses. Dell’Ampio et  al. (2014) showed that une­ venly distributed missing data from NGS data sets created well‐supported yet conflicting phy­ logenetic relationships for wingless hexapods (Diplura, Protura, and Collembola) (Meusemann et  al. 2010, von Reumont et  al. 2012). Incongruence due to missing data results from model misspecification, decreased resolving power, and a reduced ability to detect multiple substitutions (Roure et  al. 2013). Creating smaller “decisive data sets” (Dell’Ampio et  al. 2014) that include complete data blocks contain­ ing all focal taxa can minimize the impact of missing data, although if the relationship in question represents a short internal branch, then a large, complete data set might still be needed to ensure that enough phylogenetic signal is obtained to accurately resolve the relationship (Roure et al. 2013). Approaches that use random genomic parti­ tioning generally suffer less from ascertainment bias than do other methods, as all individuals are used to simultaneously identify and genotype

markers. However, missing data resulting from overall lower coverage sequencing is much greater due to less targeted locus selection (Davey et al. 2011). The effect of missing data on phylogeny reconstruction from RRL‐generated data sets has been examined, but for most analy­ ses the inclusion of more data, even with higher proportions of missing data, has no effect on overall topology, or even increases traditional support values (bootstrap support) across the tree (Wagner et al. 2013, Cruaud et al. 2014). In most cases, this likely results from the inclusion of unique characters on terminal branches, and supports the findings of Sanger sequencing‐ based studies (Wiens 2006). In the context of non‐phylogenetic analyses, however, missing data in RRL data sets can have large effects and should be considered along with other limita­ tions of the approach (Davey et al. 2012, Huang et al. 2014). It is advisable to test for an effect of locus selection and missing data, using subsets of loci and taxa to determine the robustness of the evolutionary relationships (Kawahara and Breinholt 2014, Misof et al. 2014). 16.3.2.3  Gene Tree/Species Tree Incongruence

Gene tree/species tree discordance is not a new issue (Fitch 1970, Goodman et  al. 1979, Maddison 1997). However, NGS approaches have amplified this potential incongruence to an unprecedented level, and in some fortunate cases, to its zenith (i.e., when all genes are known; Dasmahapatra et al. 2012, Nadeau et al. 2013). In these cases, the question of whether to concatenate genes into a single analysis or sum­ marize trees inferred from individual genes (Gadagkar et  al. 2005, Kubatko and Degnan 2007, Weisrock et al. 2012) becomes important but difficult to test in an exploratory fashion. Concatenation of large genomic data sets can result in highly supported but biologically mis­ leading phylogenies, particularly when assessed with traditional methods of tree support (e.g., bootstrapping; Kubatko and Degnan 2007, Weisrock et  al. 2012, Wielstra et  al. 2014). Additionally, allele choice at heterozygous sites

16  Molecular Dimensions of Insect Taxonomy

can exacerbate these calculations of support (Weisrock et al. 2012, Lischer et al. 2014). The appeal of “genome‐wide” data for phylogenetics has seemingly distracted many researchers from considering this issue, particularly with meth­ ods such as RAD‐seq, whereby phylogenies are being created from unpartitioned concatena­ tions of entire genomic data sets. However, new statistical approaches and software are being developed to address gene concatenation (Edwards et al. 2007, Kubatko et al. 2009, Heled and Drummond 2010, Larget et al. 2010, Zamani et al. 2013), and we believe that further develop­ ment of these methods is important for the development of phylogenomics. 16.3.3 Computational/Logistical/ Bioinformatic Bottlenecks

For those systematists lucky enough to have gathered “large” data sets during the Sanger sequencing era (e.g., dozens to hundreds of loci for hundreds to thousands of specimens), logisti­ cal data management and computational limi­ tations are not a new issue. These previous con­siderations, however, pale in comparison to the logistical challenges of NGS. Familiarity with NGS data repositories, bioinformatic skills, and new approaches to data storage and computa­ tional approaches are some of the keys to success for a taxonomist venturing into the world of NGS. Before initiating an NGS project, it is impor­ tant to mine molecular data repositories, such as GenBank, for genomic resources that can assist in locus selection and probe development. These resources can include earlier NGS pro­ jects, whole genomes, transcriptomes, or mitogen­ omes. They also can assist with post‐processing NGS data and dramatically reduce computa­ tional time (Miller et al. 2010). Even this initial step can be daunting, given the vast amount of publicly available data. Identifying orthologous gene regions (Peters et al. 2011) and even previ­ ously sequenced taxa (Chesters and Vogler 2013) can be problematic, although data pipe­ lines exist to assist in accessing these data (Chesters and Vogler 2013).

Once an NGS project is initiated, copious quantities of sequence data will be generated and the challenges faced in molecular taxonomy shift to post‐processing bottlenecks. Here, issues of managing and analyzing larger and larger molecular data sets will be faced, includ­ ing substantial post‐processing and access to both bioinformatic infrastructure and person­ nel (Carstens et al. 2012, El‐Metwally et al. 2013, Lampa et  al. 2013). The cost of these post‐ sequencing resources may put NGS approaches out of reach for some researchers (Nekrutenko and Taylor 2012, Smith 2014), although open‐ source and free‐to‐download alternatives abound for most methods. Even data storage can be problematic, exceeding the capacity of most desktop computers (McCormack et  al. 2013). Long‐term archiving of massive NGS data sets for publication has yet to be resolved (Kodama et al. 2012), but is essential to ensure long‐term transparency and reproducibility of NGS results (Nekrutenko and Taylor 2012). Substantive computing power is required for the preparation of NGS data sets (Lampa et al. 2013), as well as subsequent analyses. Many tra­ ditional algorithms used within a taxonomic or systematic framework can become computa­ tionally infeasible, given the size of NGS data sets (Stamatakis et al. 2012). Further complica­ tions come from sequencing errors, contami­ nated DNA, regions of low variability, and intragenomic variability (Chan and Ragan 2013). For example, multiple sequence alignments are the standard within a traditional molecular phy­ logenetic study and provide our best estimation of homology among gene regions. With data sets containing hundreds of loci, all with variable inheritance patterns, substitution rates, alterna­ tive splicing, inversions, and recombination pat­ terns, it may become computationally intractable to approach alignments using the currently available methods (Delsuc et al. 2005, Liu et al. 2012, Chan and Ragan 2013, Song et  al. 2014). Even NGS data itself may be incompatible or less than ideal for traditional phylogenetic analysis because gene trees are best resolved with large, informative loci (i.e., a series of linked SNPs

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within a non‐recombining locus), and many NGS data are comprised of individual, unlinked SNPs (McCormack et al. 2013). Accurate model selection in large, variable data sets also will become increasingly difficult. Failure to appro­ priately partition the data, over‐ or under‐ parameterization, and an improper model of sequence evolution can contribute to systematic error and inaccurate phylogenetic estimation (Felsenstein 2004, Lemmon and Lemmon 2013). Alignment, model selection, and phylogenetic tree reconstruction will all require new approaches, increased computational power, and personnel with bioinformatic experience. 16.3.4  The Role of Morphology in a Post-genomic Era

As NGS techniques and the availability of molec­ ular data continue to grow exponentially, what part will morphology play in this post‐genomic era (Beutel et  al. 2011, Beutel and Kristensen 2012)? Morphological data substantially affect the resolution of deeper phylogenetic nodes, compared with molecular data alone (Wahlberg et al. 2005, Wortley et al. 2006, Beutel et al. 2011), and serve as an independent character partition that can be used to evaluate phylogenetic hypotheses, using the process of reciprocal illu­ mination, as advocated by Hennig (1966). The distribution of presumed homologous morpho­ logical characters also can help to identify sys­ tematic error in genomic data sets (e.g., myriapod relationships; Janssen and Budd 2010, Telford et  al. 2011). Furthermore, only morphological treatments can place fossil taxa into a phyloge­ netic framework and provide insights into the evolutionary transformations experienced by a lineage over time, knowledge that would be unattainable from molecular data alone (Beutel and Kristensen 2012). Consequently, thorough morphological treatments are required to revise or create an effective taxonomic classification (Yassin et al. 2013). Finally, from an evolutionary perspective, NGS can facilitate our understand­ ing of the underlying genetic basis of complex morphological adaptations. Using quantitative

trait locus (QTL) approaches or genome‐wide association studies provides the advantage of having associated gene‐function information for each molecular marker (e.g., Anderson et  al. 2006, Turner et al. 2013). Morphological techniques also have their own trajectory. New technologies, such as micro­ computed tomography, confocal scanning laser microscopy, and transmission electron micros­ copy, are providing access to suites of novel characters (e.g., internal morphology; Deans et  al. 2012) and developmental changes in an organism over time (Lowe et al. 2013), as well as the ability to perform virtual dissections on val­ uable type specimens (Simonsen and Kitching 2014). Effective communication about morpho­ logical traits and character states, particularly among large taxonomic groups, requires further standardization to lower barriers to complete integration across a wide variety of studies (Deans et al. 2012). We believe the key to over­ coming this challenge is to foster an understand­ ing of the appropriateness of Bayesian rather than frequentist approaches to assessing the confidence in broader taxonomic hypotheses (Dombroskie and Sperling 2013). Ultimately, despite the challenges faced with morphological data and their integration with vast quantities of available molecular data, morphology will con­ tinue to have a prominent and essential role in insect taxonomy and systematics.

16.4 ­Conclusions Since the review by Sperling and Roe (2009), insect taxonomy has embarked on a journey into a brave new world of NGS. NGS approaches have the ability to provide a vast wealth of knowledge. We soon may see some stability and resolution of insect relationships that were pre­ viously considered intractable (Misof et  al. 2014) and begin to see new patterns in the genomic mosaic that has given rise to the astounding array of insect diversity. We will truly begin to realize the strength of NGS data when they are tied to morphological, ecological,

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and behavioral data. To quote Paterson and Piertney (2011: 870): “The challenge will be ensuring that the onslaught of data that accom­ panies approaches such as NGS, genome scans and microarray technologies can be coupled to appropriate ecological and phenotypic meta­ data to allow meaningful analysis to be undertaken.” With these exciting new strategies, it is essen­ tial that genomic data are not reserved for a few well‐funded research laboratories. As Nekrutenko and Taylor (2012) point out, there is a need to democratize the computational infrastructure required to analyze NGS data, a need that has been recognized by some coun­ tries, leading to the development of national NGS computational infrastructure (Lampa et al. 2013). Standardized pipelines within established computational networks would greatly assist many taxonomists in entering the daunting field of genomics. A standardized framework of best practices is also needed to ensure that projects are repeatable, particularly the numerous steps needed for NGS post‐processing (Nekrutenko and Taylor 2012). Standardization, however, can be a double‐edged sword; blindly following “black‐box” protocols and analyses without a thorough understanding of the underlying the­ ory can lead to erroneous conclusions (Andrews and Luikart 2014). This point will only become exacerbated with the development of new genomic tools, so taxonomists themselves must take care to understand the fine points of genomics and genomic analyses before embark­ ing into the world of NGS. The field of taxonomy is now in need of com­ putational innovation to match the technologi­ cal advancements in NGS. We need algorithms and approaches that allow us to accommodate the true complexity of genomic structure, find­ ing ways to deal with non‐independence of genomic regions and patterns of recombination within a phylogenetic framework. We are confi­ dent the research community will continue to innovate and advance so that the field of taxo­ nomic science will fully realize the potential of NGS data.

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17 DNA Barcodes and Insect Biodiversity John-James Wilson1,2, Kong-Wah Sing2,3, Robin M. Floyd 4,5 and Paul D. N. Hebert5 1

International College Beijing, China Agricultural University, Beijing, P. R. China Institute of Biological Sciences, University of Malaya, Kuala Lumpur, Malaysia 3 State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, P. R. China 4 Wellcome Trust/MRC Stem Cell Institute, University of Cambridge, Cambridge, UK 5 Centre for Biodiversity Genomics, Biodiversity Institute of Ontario, University of Guelph, Guelph Ontario, Canada 2

About 3500 species of mosquitoes (Diptera: Culicidae) have been described worldwide. In 1897, Ronald Ross, a Scottish physician working  in India, discovered that only members of one  mosquito genus, Anopheles, carry the Plasmodium parasite, the single-celled organism that causes malaria in humans. This revelation reflected painstaking efforts, involving the dissection of stomachs from vast numbers of mosquitoes. It was a key breakthrough that paved the way for Ross to demonstrate the life cycle of the parasite in the laboratory, work rewarded by the 1902 Nobel Prize in Medicine. Sadly, Ross’s hope that this knowledge would quickly lead to malaria control proved too optimistic; the disease still causes more than 1 million deaths per year, mainly in tropical Africa and Asia, despite continuous eradication efforts (Murray et  al. 2012). This situation persists, in part, because the evolutionary dynamics of both Plasmodium and its insect vectors are far more complicated than initially realized. It remains true that only a few species of Anopheles transmit human malaria. However, Anopheles gambiae, the most important vector of the Plasmodium parasite in humans, belongs to a complex of morphologically indistinguishable sibling species

that nevertheless differ markedly in their habitat preferences, behaviors, and ability to transmit human malaria (Lawniczak et al. 2010). Although these species are morphologically indistinguishable, they can be discriminated readily on the basis of DNA sequences (Lawniczak et al. 2010). The message from this story is clear: cryptic biological diversity matters. Anopheles serves as a pertinent example of the challenges faced by those concerned with biodiversity. Life exists in an immense number of forms, which are often tiny, difficult to study, and even more difficult to discriminate. Yet, this subtle variation can be crucially important; paraphrasing one article on the subject, what we don’t know can hurt us (Besansky et al. 2003). With more than 1 million described species and millions more either awaiting description or simply undiscovered (Sheffers et al. 2012), insects are the most diverse group of animals on the planet. They affect human society in myriad ways, both harmful (e.g., disease vectors and agricultural pests) and beneficial (e.g., pollinators and biological control agents). Research with insects has added immensely to our understanding of evolution, ecology, and the genetic control of development. Yet, a fundamental requirement

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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in gaining useful knowledge about any taxonomic group is the ability to recognize – describe, classify, and identify – its members. Groups, such as insects, present a great challenge to the taxonomic enterprise simply because of their diversity. The recognition of species by traditional morphological methods is complex and usually requires specialist knowledge; yet, the number of undescribed insect species far outweighs the number of taxonomic specialists, a workforce in decline (Godfray 2002). Concerns about a lack of species recognition capability are not purely academic, but have significant practical implications. Annual economic losses due to insects for Brazilian agriculture alone have been estimated at US$17.7 billion (Oliveira et al. 2014), making rapid recognition of destructive species vital before invasions become uncontrollable. There is also a basic scientific need to describe biological diversity before the destruction of natural habitats causes the loss of species on a massive scale. We need a rapid way of assembling species catalogs, so that conservation programs can protect those areas of greatest importance before they are lost forever (Sheffers et al. 2012).

17.1 ­Species Concepts and Recognition Although species have long been considered the basic “units of biodiversity” and are considered by some as the only “real” grouping in the taxonomic hierarchy, the issue of how to recognize species remains controversial. Mayden (1997) listed 22 species concepts that had appeared in the literature (although some are essentially synonyms). Each used varied criteria for species recognition, including ecological niches, mate recognition, genetic cohesion, and evolutionary history. This diversity of concepts and recognition criteria necessarily leads to ambiguity, which can have important implications for studies of biodiversity and conservation, as differing species concepts can produce widely varying estimates of species richness (Agapow et  al. 2004).

Although reproductive isolation is often considered to be the most important indicator of species status, it is seldom directly testable and fails to address asexual organisms. In practice, most species continue to be recognized by the presence of one or more diagnostic morphological differences (Davis and Nixon 1992). For most insect groups, detailed examination of genitalic morphology has represented the gold standard for species recognition for nearly a century, reflecting the rapid and pronounced divergence in genitalic structures between even closely related species of insects (Eberhard 1985). The practical application of this criterion, however, is hampered by lack of an appropriate methodology to quantify shape variation and by questionable homology assessments. All these factors collectively make species identification an extremely specialized and time-consuming task, and even expert taxonomists can have difficulty reaching consensus. Moreover, reliance on diagnostic characters that are present only in the adult life stage constrains recognition, as many specimens lack these characters. For example, the life stages most commonly intercepted at ports of entry are those of the larva and pupa (Scheffer et  al. 2006), which rarely can be identified beyond the ­family level. Another option exists – species can be recognized by the genetic changes that arise between reproductively isolated lineages as a result of genetic drift or selection. The earliest use of DNA sequences to gain information about the taxonomic affinities of an unknown specimen was in morphologically intractable groups such as viruses and bacteria (Theron and Cloete 2000). More recently, DNA sequencing has been applied to plants (Chase et al. 2005), small metazoan animals, and even charismatic megafauna such as birds, fish, and mammals (Waugh 2007). An important advantage of a DNA sequence-based approach to species recognition is the digital nature of a DNA sequence, which allows it to be gathered and interpreted objectively. This approach relies on the use of algorithms enabling DNA-sequence comparisons, such as BLAST (Basic Local Alignment Search Tool) (Altschul

17  DNA Barcodes and Insect Biodiversity

et al. 1990), in conjunction with DNA-sequence repositories, such as GenBank or BOLD (Barcode of Life Data Systems), a specialized database that was developed to support both a stronger audit trail between reference sequences and voucher specimens (Ratnasingham and Hebert 2007). DNA extracts from any life stage of an organism – egg, larva, pupa, or adult – or from tissue fragments will generate a similar identification, whereas traditional identification keys (especially for insects that undergo complete metamorphosis) often depend on adult features. Social insects, such as ants and termites, can exhibit highly divergent caste morphologies that, in some cases, have been diagnosed incorrectly as distinct species; DNA sequencing can remove such ambiguities (Smith et al. 2005). Sexual dimorphism, too, has long been a source of complications for taxonomists. Janzen et al. (2005) described a case in which each sex of the butterfly Saliana severus was recorded as a separate species in an i­ nventory until DNA sequencing revealed that males  and females had the same cytochrome c ­oxidase subunit I (COI) sequences, leading to the ­recognition of a single, highly sexually dimorphic species.

17.2 ­DNA Barcoding Methodology DNA barcoding, in a broad sense, is simply the use of short, standardized genomic segments as markers for species recognition. Just as species differ in morphology, ecology, and behavior, they also differ in their DNA sequences. Hence, at least in principle, a particular gene or gene fragment can be used to recognize a given species in much the same way that retail barcodes can be used to uniquely recognize each consumer product. In practice we would not expect DNA barcoding to work in such a simple manner; real DNA sequences are subject to all of the natural complexities of molecular evolution and can show considerable variation within species (Mallet and Willmott 2003). They are not categorically assigned to entities one by one as retail barcodes are. Nevertheless, DNA barcoding

promises the ability to automate the identification of specimens by determining the DNA sequence of the DNA-barcode region, avoiding the complexities inherent in morphological identifications. The particular genomic region used as a DNA barcode represents an important choice. It must be homologous between the organisms compared and have a rate of evolution fast enough to show variation between closely related species, but it also must have sufficient regions of sequence conservation to allow a limited set of PCR primers to amplify the target gene region from broad sections of the tree of life. The resultant sequence information also must generate a robust alignment so that sequences can be compared. In the animal kingdom, attention has focused on an approximately 650-base-pair region near the 5′ end of the mitochondrial COI gene (Hebert et al. 2003). COI provides an ideal species marker in insects owing to its infrequent possession of introns, simple alignment, limited exposure to recombination, and the availability of robust primer sites. Sequence variation in this region generally shows large interspecific, but small intraspecific, divergences, meaning that species frequently form clearly distinguishable clusters on a distance-based or phylogenetic tree. The homogenization of mitochondrial DNA sequences within a species, regardless of population size, is an intriguing phenomenon that has prompted study and speculation as to its evolutionary origin and significance (Stoeckle and Thaler 2014). Boundaries signaled by this molecular marker are strongly concordant with species units recognized through past studies of morphological and behavioral characters in the vast majority of cases where they have been examined (Ratnasingham and Hebert 2013). The Barcode Index Number (BIN) system represents a formalization of this approach and assigns COI sequences to clusters known as BINs (Ratnasingham and Hebert 2013) using single linkage clustering and a graph analytical approach. Extraction and amplification of DNA from insects, including eggs and larvae, presents no

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technical challenge (Wilson 2012). Recent advances in high-throughput DNA-sequencing technology and reductions in costs have made the generation of large volumes of DNA data straightforward (Shokralla et  al. 2014). Sequences can be produced in the laboratory from a sample within a few hours in a largely automated fashion. Although the “Star Trek” vision of a handheld instant species-identification device awaits development, promising advances have been made in reducing the costs and the size of the equipment needed to gather barcode data. Full exploitation of DNA barcodes for species recognition will be possible only after assembling a comprehensive database linking organisms (and Linnaean taxonomy) with their DNA sequences. Although coverage is now rising by more than 1 million records a year, DNAsequence coverage varies considerably among the insect orders (Table 17.1). These gaps raise the possibility of a poor match between a DNA sequence derived from a newly encountered species and an incomplete reference library, meaning that no identification would be possible (Baker et  al. 1996, Ekrem et  al. 2007). Although “best BLAST hit,” the simplest method of taxonomic assignment, may be essentially useless when no relatives have appropriate sequences in GenBank (Tringe and Rubin 2005), tree-based methods can improve assignment accuracy and limit false positives (Wilson et al. 2011). Tautz et  al. (2003) suggested that an attempt be made to provide a DNA sequence as a component of all future species descriptions. Although this is not yet standard practice, the concept of type sequences with voucher specimens authenticated by experts for the taxa and with associated Linnaean taxonomy is becoming reality. In 2004, the US National Center for Biotechnology Information (NCBI), GenBank’s home organization, reserved the keyword “BARCODE” for “barcode standard” DNA sequences archived with the International Nucleotide Sequence Database Collaborative, with relevant supporting data including the name of the identifier and collection location.

The concept of DNA barcoding was initially controversial in the taxonomic community (Smith 2005). Criticisms of the approach included questioning whether a single genetic marker has sufficient resolution to discriminate species reliably (Will et al. 2005) and potential problems caused by differing patterns of inheritance between nuclear and mitochondrial genes, which could confound the association between sequence and species (Rubinoff 2006). The volume of DNA barcodes collected over the past decade indicates that such cases are infrequent. The DNA-barcoding movement began to gather real momentum with its application to insects. Under the umbrella of various global and regional initiatives (e.g., the International Barcode of Life Project and German Barcode of Life Network), there has been an effort to build a comprehensive database of DNA barcodes linked to biodiversity data (geographic, temporal, taxonomic) for the taxa they represent. We, therefore, move to discuss cases in which DNA barcoding has been applied to the different orders of insects (following the taxonomic scheme of Trautwein et al. 2012), and examine how they have advanced our knowledge of biodiversity. The numbers of DNA barcodes reported in Table 17.1 summarize coverage on BOLD (Ratnasingham and Hebert 2007) in early 2015. As such, they provide a benchmark of the past scope of DNA barcoding for each order. All hexapod orders have barcode coverage, but the number of records per order varies from one to 810,000. Much of the variation in barcode coverage is linked to the number of species in each order (eight to 400,000), but coverage per described species varies from a low of 2% for Dermaptera and Zoraptera to a high of 56% for Lepidoptera. The need for much more effort in DNA-barcode library construction is reinforced by the fact that the known species count for each order is just a small fraction of its total diversity.

17.3 ­Basal Hexapod Orders Collembola (springtails), Protura, and Diplura are basal taxa of the superclass Hexapoda. These

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Table 17.1  DNA barcodes and insect biodiversity. No. of public DNA barcode records

No. of public DNA barcode BINs

Basal hexapods

41,412

3,581

0.37

Collembola

41,272

3,547

0.44

Diplura

34

14

0.02

Protura

106

20

0.03

Insecta

2,191,694

243,881

0.24

Archaeognatha

338

64

0.14

Blattodea

1,317

368

0.08

Coleoptera

135,376

23,834

0.06

Dermaptera

412

41

0.02

Diptera

717,433

51,306

0.34

Embioptera

137

62

0.16

Ephemeroptera

14,870

1,364

0.45

Grylloblattodea

3

2

0.08

Hemiptera

97,975

10,259

0.12

Hymenoptera

316,747

47,816

0.38

Isoptera

1585

453

0.15

Lepidoptera

810,000

97,123

0.56

Mantodea

741

294

0.12

Mantophasmatodea

2

1

0.13

Mecoptera

201

42

0.08

Megaloptera

1,383

98

0.33

Neuroptera

4,865

741

0.13

Odonata

8,819

973

0.15

Orthoptera

12,149

1,732

0.07

Phasmatodea

572

108

0.04

Phthiraptera

1,746

100

0.03

Plecoptera

7,019

871

0.38

Psocoptera

10,217

408

0.07

Raphidioptera

110

22

0.1

Siphonaptera

240

38

0.02

Strepsiptera

212

59

0.1

Thysanoptera

9,145

628

0.1

Trichoptera

38,054

5,059

0.4

Zoraptera

1

1

0.02

Zygentoma

26

15

0.04

Group

*For the number of described species in each order, see Chapter 1.

No. of BINs as a proportion of the estimated No. of described species*

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groups are among the most diverse and abundant of all soil arthropods, with about 8000 known species of springtails, 1600 known species of proturans and diplurans, and undoubtedly many more species undiscovered. Springtails have the widest distribution of any hexapod group, with a global distribution including Antarctica. In particular, the polar regions seem to have a considerable uncataloged diversity, a pattern supported by early DNA-barcoding studies (Hogg and Hebert 2004). As is typical for such groups, the large number of species coupled with difficulties in identification and a lack of taxonomic specialists create a severe impediment to understanding their diversity. DNA barcoding has uncovered cryptic species among a number of cosmopolitan springtails (Stevens and Hogg 2003, Porco et al. 2012) and cryptic species of proturans at local scales (Resch et  al. 2014). The concept of type sequences has been realized in a number of new species descriptions from these hexapod groups (e.g., Bai and Bu 2013), which is logical given the widely acknowledged difficulties with species identification.

17.4 ­Archaeognatha (Bristletails) and Zygentoma (Silverfish) Given the phylogenetic position of bristletails and silverfish as wingless entognaths, a number of DNA-barcode sequences have been generated for phylogenetic studies (e.g., Nardi et al. 2003), contributing to 338 public barcodes (64 BINs) for Archaeognatha and 26 public barcodes (15 BINs) for Zygentoma.

17.5 ­Odonata (Dragonflies) Although odonatologists have been reluctant to shift away from the 16S ribosomal RNA gene region employed for phylogenetic studies on dragonflies and damselflies (Ballare and Ware 2011), a number of public DNA barcodes (8819 from 973 BINs) are available for this medium-rich

order. Odonata also have provided a focus for those advocating a “character-based” approach to DNA-barcode analysis (e.g., Rach et al. 2008).

17.6 ­Ephemeroptera (Mayflies) The larval stages of mayflies develop in freshwater habitats and consequently are widely used as biomonitors for water-quality assessment. The species diversity of mayfly and other insect larvae (usually of stoneflies, caddisflies, and some dipterans) is a useful indicator of disturbance in rivers (Webb et  al. 2012), and a standardized and efficient approach to species recognition is needed for this ecological application. A DNAbarcode library for the mayflies of North America, including about 40% of the known species, has been assembled for this purpose (Webb et  al. 2012). The library construction process revealed that DNA barcodes could successfully identify all species, with the exception of three taxonomically complex cases, and that nearly 20% of species examined contained multiple lineages that might deserve recognition as independent species. This library contributed about one-quarter of all DNA-barcode records for mayflies on BOLD (14,870 public barcodes, 1364 BINs).

17.7 ­Orthoptera (Grasshoppers) After early studies revealed that grasshoppers have an especially large number of nuclear mitochondrial pseudogenes (Numts) (Song et al. 2008), the order has become a focus for DNA-barcoding studies related to this phenomenon. If Numts are mistaken for their mitochondrial paralogues (i.e., the “true” DNA-barcode sequences), the number of species recognized can be affected, particularly when using percentage similarity thresholds (Song et  al. 2008). After screening sequences for stopcodons and frameshifts, an automatic procedure for the 12,149 public barcodes (1732 BINs) from grasshoppers submitted to BOLD (or indeed any submitted sequence), Huang et al. (2013) did not

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report any Numts in their DNA-barcode records from grasshoppers from China.

17.8 ­Phasmatodea (Walking Sticks), Embioptera (Webspinners), Grylloblattodea (Icecrawlers), and Mantophasmatodea (Gladiators) Despite a Phasmatodea DNA-barcoding campaign, and the potential for interesting findings as a result of the many parthenogenetic and hybrid species (Brock 2009), few DNA-barcode records are available for this charismatic order (572 published records, 108 BINs). Embioptera, a small order of fewer than 500 nominal species (Szumik 2008) with a unique silk-spinning ability, have a few public DNA barcodes available, most deriving from phylogenetic studies (137 published barcodes, 62 BINs). Likewise, the three published DNA-barcode records (two BINs) from Grylloblattodea and two published DNA-barcode records (one BIN) from Mantophasmatodea  –  which were once considered a distinct order from Africa (Klass et al. 2002) but are now combined with the Gryllobattodea in the order Notoptera  –  derive from phylogenetic studies.

17.9 ­Plecoptera (Stoneflies) and Dermaptera (Earwigs) Plecoptera together with allies from Ephemeroptera and Trichoptera (collectively known as “EPTs”) formed the focus of an inventory of arctic life at Churchill, Manitoba, Canada, that employed DNA barcoding (Zhou et al. 2009). Although the number of stonefly species in that study was modest (only seven), 7019 public barcodes (871 BINs) are now available for the order. DNA barcodes have suggested the presence of cryptic species within the widely distributed European earwig (Jordaens et al. 2011), adding to the 41 BINs and 412 public barcodes available for earwigs.

17.10 ­Mantodea (Mantids) In Mantodea, DNA barcodes have been applied to associate morphologically disparate members of the same species (males and females, and immatures and adults) (Scherrer 2014). DNA barcoding has been applied to Apteromantis aptera, the only mantid protected under international law (Battiston et al. 2014), contributing to the 741 published barcodes (294 BINs) for this order.

17.11 ­Blattodea (Cockroaches) and Isoptera (Termites) Currently considered as members of the same order, the cockroaches and termites include some of the most economically important and easily recognizable human pests. DNA barcoding has been used to re-evaluate the taxonomy of pest cockroaches in urban South China (Yue et al. 2014), identify pest cockroaches in Tehran (Hashemi-Aghdam and Oshaghi 2015), and confirm the invasion of the Japanese cockroach (Periplaneta japonica) into New York City (Evangelista et al. 2013). Likewise, the utility of DNA barcodes for the identification of termite pests (in the genus Reticulitermes) has been firmly established (Foster et al. 2004). The cockroaches and termites represent a modestly large group (2902 published barcodes available from 415 BINs). Away from human habitations, DNA barcodes have been used to assist species delimitation in biodiversity inventories (e.g., cockroaches in Guyana, Evangalista et  al. 2014; termites in Madagascar, Monaghan et al. 2009).

17.12 ­Psocoptera (Booklice) and Phthiraptera (Lice) A large number of public barcodes (11,956 in 507 BINs), but few published studies, exist for these taxa. Both have now been combined into a single order, which includes medically important and agricultural pests.

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17.13 ­Thysanoptera (Thrips) and Hemiptera (True Bugs) Thrips include many species with beneficial roles (e.g., pollinators) as well as agricultural pests. After comparing its performance with other gene regions, Glover at al. (2010) confirmed that COI was the most suitable DNA barcode for thrips. Although only about 1% of about 5800 described species of thrips have been confirmed as pests (Karimi et al. 2010), most DNA-barcoding studies on this group relate to quarantine procedures, for example, in South Africa (Timm et al. 2008), China (Qiao et al. 2012), and the United Kingdom (Collins et  al. 2010), adding to the 9145 public barcodes (628 BINs). The true bugs also are important economically, as the order contains plant pests. Six large-scale studies (335 species, Foottit et al. 2008; 154 species, Lee et al. 2011; 139 species, Jung et al. 2011; 344 species, Park et al. 2011; 471 species, Foottit et al. 2014; and 457 species, Raupach et al. 2014) have validated the use of DNA barcodes for identification of hemipterans in general (116,761 public barcodes available from 11,637 BINs). A number of studies have validated their use in the specific case of the silverleaf whitefly (Bemisia tabaci). This complex of at least 24 morphologically indistinguishable, yet behaviorally and barcode-distinct species (Ashfaq et al. 2014a, Frewin 2014), is responsible for more than $1 billion in accrued costs for crop and ornamental plant damage in the United States.

17.14 ­Hymenoptera (Wasps) With more than 130,000 described species, the Hymenoptera, containing the bees, wasps, and ants, is the fourth largest insect order after Coleoptera, Lepidoptera, and Diptera. In terms of public DNA barcodes, the order ranks third, after Lepidoptera and Diptera, with 316,747 records in 47,816 BINs. Given the number of cryptic species suspected to exist, especially in parasitic forms, the true species richness of Hymenoptera might even surpass the “big three” (Smith et  al. 2013).

DNA barcoding has been explored for identification of bees and wasps on regional scales (Nova Scotia, Canada, Sheffield et  al. 2009; Chamela– Cuixmala Biosphere Reserve, Mexico, ZaldívarRiverón et al. 2010; Ireland, Magnacca and Brown 2012; and Churchill, Manitoba, Canada, Stahlhut et al. 2013) and in specific taxonomic case studies (Liotrigona, Koch 2010; and Bombus, Carolan et al. 2012). For ants, the focus has been on DNA barcoding as a heuristic guide for classifying unknown and undescribed groups. Although instances of incongruities were revealed between molecular and morphological units, strong correlations generally existed (Smith et  al. 2005, Jansen et al. 2009). The occurrence of heteroplasmy and the bacterial endosymbiont Wolbachia in some hymenopterans has been presented as a challenge to conventional DNA-barcoding analyses (Magnacca and Brown 2010). However, Wolbachia sequences are unlikely to be confused with insect COI, and intra-individual divergences due to heteroplasmy are generally equivalent to intraspecific divergences (Magnacca and Brown 2010; in Lepidoptera, Shokralla et al. 2014). Issues in DNAbarcode generation due to both Wolbachia ­infection and heteroplasy are also being addressed by  next-generation-sequencing technology (Shokralla et al. 2014).

17.15 ­Strepsiptera (Twistedwing Parasites) In Strepsiptera, COI sequences have been used to match members of heterotrophic heteronomous species (Kathirithamby et al. 2010). Due to the enigmatic taxonomic position of the group (Trautwein et  al. 2012), a number of sequences derive from phylogenetic studies, taking the total number of public DNA barcodes to 212 (59 BINs).

17.16 ­Coleoptera (Beetles) When asked what the study of nature revealed about the mind of God, the British geneticist

17  DNA Barcodes and Insect Biodiversity

J. B. S. Haldane apparently quipped: “an inordinate fondness for beetles.” One out of every five animals on the planet is thought to be a beetle. As a consequence, the Coleoptera represent a group for which the taxonomic enterprise has been overwhelmed by diversity. Although about 400,000 species of beetles have been described (including many economically important pest species), as many as 5 million to 8 million beetle species might exist. To date, 135,376 public barcodes have been generated representing 23,834 BINs. Some studies have examined the ability of barcodes to identify a priori (morphological) species units (e.g., Raupach et  al. 2010). One study found that 98.3% of 1872 North European species possessed distinct DNA-barcode arrays and also suggested the presence of 20 cryptic species in this well-known fauna (Pentinsaari et al. 2014). However, with so many unknown species suspected in the order, much barcoding research with beetles has focused on the use of DNA-based methods in species discovery and delineation. Early studies in this area employed existing phylogenetic methods, including statistical parsimony networks (e.g., Monaghan et  al. 2005), until Australian tiger beetles from the genus Rivacindela were used as the test group for the development of a General Mixed Yule Coalescent (GMYC) model (Pons et al. 2006). The GMYC has since been refined through testing on various beetle (and other) groups (e.g., Ahrens et  al. 2007, Papadopoulou et  al. 2008, Monaghan et  al. 2009) and has been used to examine the correlation between genetic diversity and species across time and space in European water beetles (Baselga et al. 2013).

17.17 ­Neuroptera (Lacewings), Megaloptera (Dobsonflies), and Raphidioptera (Snakeflies) Public barcode records (4865 in 741 BINs) have enabled the detection of neuropteran species in the diets of North American bats (Clare et  al. 2011). Currently, 1384 (98 BINs) and 111 (22 BINs)

public barcodes are available for Megaloptera and Raphidioptera, respectively.

17.18 ­Trichoptera (Caddisflies) DNA barcodes from caddisflies (38,054 public barcodes from 5059 BINs) have been generated for application in water-quality monitoring (e.g., Baird and Sweeney 2011).

17.19 ­Lepidoptera (Butterflies and Moths) One might think that DNA barcoding has little to offer an order for which bright wing patterns and extensive taxonomic attention suggest a well-resolved species taxonomy. However, this perspective would be overly optimistic; approximately 175,000 species of Lepidoptera have been described, but another 150,000 to 1,250,000 species are thought to await description. The range of estimates itself indicates the lack of knowledge of butterfly and moth diversity. The Lepidoptera have been the model group for DNA-barcoding studies since Hebert et al. (2004) used North American moths to demonstrate the ability of COI to discriminate individuals of different species and Astraptes fulgerator to demonstrate the potential of COI analyses in species discovery. The conclusions of early studies have been validated by large-scale regional DNA-barcode studies of butterflies (Costa Rica, Janzen et al. 2009; Central Asia, Lukhtanov et al. 2009; Germany, Hausmann et al. 2011b; Romania, Dincă et al. 2011; Pakistan, Ashfaq et  al. 2013; and Malaysia, Wilson et  al. 2013), skippers (Costa Rica, Hajibabei et al. 2006), hawkmoths (Australia, Rougerie et  al. 2014; and Costa Rica, Hajibabei et al. 2006), saturniids (Costa Rica, Janzen et  al. 2012), geometrids (Ecuador, Strutzenberger et al. 2011; and Bavaria, Hausmann et al. 2011a), and Noctuoidea (Canada, Zahiri et al. 2014), among others. The popularity of butterflies and moths means that they have been widely collected, and the available natural history collections have ­facilitated the construction of comprehensive

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DNA-barcode libraries (e.g., in North America, Hebert et al. 2010; Costa Rica, Janzen et al. 2009; and Australia, Hebert et al. 2013), contributing to 810,000 public barcodes (97,123 BINs) for the Lepidoptera.

17.20 ­Diptera (Flies) The flies constitute a hyper-diverse insect order, with more than 150,000 described species, and now with 717,433 public barcodes (51,306 BINs). Among insects, the Diptera have the greatest negative impact on human and livestock health, with groups such as mosquitoes and tsetse acting as vectors of the agents that cause major diseases including malaria, sleeping sickness, and filariasis. Before the publication on DNA barcodes by Hebert et  al. (2003), various molecular tools already had been applied to the identification of mosquito species, including allozyme electrophoresis, DNA hybridization, and restriction fragment length polymorphism (RFLP) and sequencing-based approaches using COI and other markers. One of the earliest applications of a DNA-based approach to species identification involved fly species that lay eggs on corpses shortly after death (Calliphoridae and Sarcophagidae) and can be used to estimate the postmortem interval; DNA barcoding has been established as an appropriate tool in this field of forensic science (Meiklejohn et  al. 2013). DNA-barcode libraries also have been assembled and validated as effective identification tools for medically important dipteran groups, such as black flies (e.g., Pramual and Adler 2013), deer flies and horse flies (Cywinska et  al. 2010), mosquitoes (e.g., Kumar et al. 2007, Wang et al. 2012, Ashfaq et al. 2014b), and sand flies (e.g., Kumar et al. 2012), overruling the suggestion by Meier et  al. (2006) that high intraspecific sequence divergences at COI would lead to low identification success. Their mistaken conclusion was almost certainly because they based their assessment on GenBank records, which are known to include many specimens with incorrect taxonomic assignments.

Dipteran parasitoids provide interesting case studies for DNA barcoding. Parasitoids are not only a major component of global biodiversity, but also comprise a large number of suspected cryptic species that are distinguished by strong host specificity (Godfray 1994). When DNA barcoding was applied to an ongoing inventory of the parasitoid fauna of Lepidoptera in the Area Conservación Guanacaste in Costa Rica (Janzen et  al. 2009), unprecedented specieslevel, host-specific diversity was revealed among presumed generalists in the family Tachinidae (Smith et al. 2006, 2007).

17.21 ­Siphonaptera (Fleas) and Mecoptera (Scorpionflies) DNA barcodes have been used to uncover cryptic diversity in the globally distributed cat flea Ctenocephalides felis (Lawrence et  al. 2014), but otherwise, few public barcodes exist (240 in 38 BINs) for this medically important order. A similar number of public barcodes exist (201 in 42 BINs) for the less species-rich order Mecoptera.

17.22 ­Conclusions DNA barcodes represent stable data points around which to accumulate ecological, geographical, morphological, and other information from specimens. DNA barcodes can be integrated into the traditional Linnaean classification system (Dayrat 2005), while remaining independent from it. Once submitted to public online databases, DNA sequences represent a freely available taxonomic resource that allows taxon recognition to be accomplished in a uniform manner by non-experts. DNA barcoding has the potential to become a universal communication tool in a way that complicated and often incomprehensible morphological descriptions cannot be, especially in developing countries where the majority of biodiversity resides (Sheffers et al. 2012).

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DNA-sequence information is easy to obtain, unambiguous, and enables species recognition without requiring familiarity with the intricacies of morphology. Molecular operational taxonomic units (including BOLD BINs, Ratnasingham and Hebert 2013) – valid species or not, depending on the species concept applied – nevertheless can be a suitable surrogate for partitioning diversity into interoperable units for biodiversity studies. This approach enables users to obtain taxonomic data much faster than with the traditional morphological approach, making surveys scalable across much larger taxonomic groupings and wider geographical regions (Smith et  al. 2005). Yet, the appeal of DNA barcoding stems not only from speed and operationality, it also reflects the increasingly held view that DNA-sequence analysis is as appropriate a mechanism for recognizing evolutionary units as morphological comparison (Miralles and Vences 2013). It does not automatically follow from this premise that an analysis based on single-gene comparisons will always recognize species-level groups in line with those recognized by expert morphological taxonomists, but past studies have convincingly shown that this is often the case. To describe approximately 1 million insect species using morphological approaches has taken more than 200 years. To characterize nearly 400,000 BINs through DNA barcoding has taken just 10 years. DNA-assisted species discovery has the potential to rapidly accelerate the process of cataloging biodiversity, a huge advantage in light of the current biodiversity crisis affecting our planet (Sheffers et al. 2012). By allowing more rapid detection and monitoring of agricultural pests and disease vectors, the pragmatic significance of DNA barcoding can hardly be overemphasized. Considering the rapid technological developments of the 21st century, one can easily envisage a time when a handheld DNA-barcoding device will allow any curious child to scan an insect and gain immediate access to a library of information  –  not only the insect’s name, but also its biology, ecology, conservation status, and more. Human beings preserve those things we value, and we

can only value those things we perceive. For biological diversity to become something valued by all, it must be made visible and understandable in all its complexity – a goal for which DNA barcoding can play a significant role.

­Acknowledgments The first incarnation of this contribution was supported by the Canadian Barcode of Life Network with funding from Genome Canada through the Ontario Genomics Institute, and the Natural Sciences and Engineering Research Council of Canada. The present version was supported by funding from the University of Malaya, Kuala Lumpur. We thank all those who provided constructive comments on the various drafts of this manuscript.

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Timm, A. E., M. Stiller and J. E. Frey. 2008. A molecular identification key for economically important thrips species (Thysanoptera: Thripidae) in southern Africa. African Entomology 16: 68–75. Trautwein, M. D., B. M. Wiegmann, R. Beutel, K. M. Kjer and D. K. Yeates. 2012. Advances in insect phylogeny at the dawn of the postgenomic era. Annual Review of Entomology 57: 449–468. Tringe, S. G. and E. M. Rubin. 2005. Metagenomics: DNA sequencing of environmental samples. Nature Reviews Genetics 6: 805–814. Wang, G., C. X. Li, X. X. Guo, D. Xing, Y. D. Dong, Z. M. Wang, Y. M. Zhang, M. D. Liu, Z. Zheng, H. D. Zhang, X. J. Zhu, Z. M. Wu and T. Y. Zhao. 2012. Identifying the main mosquito species in China based on DNA barcoding. PLoS ONE 7: e47051. Waugh, J. 2007. DNA barcoding in animal species: progress, potential and pitfalls. BioEssays 29: 188–197. Webb, J. M., L. M. Jacobus, D. H. Funk, X. Zhou, B. Kondratieff, C. J. Geraci, R. E. DeWalt, D. J. Baird, B. Richard, I. Phillips, P. D. N. Hebert. 2012. A DNA barcode library for North American Ephemeroptera: progress and prospects. PLoS ONE 7: e38063. Will, K. W., B. D. Mishler and Q. D. Wheeler. 2005. The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology 54: 844–851. Wilson, J. J. 2012. DNA barcodes for insects. Pp. 17–46. In W. J. Kress and D. L. Erikson (eds). Methods in Molecular Biology. Humana Press, New York. Wilson, J. J., R. Rougerie, J. Schonfeld, D. H. Janzen, W. Hallwachs, M. Hajibabaei, I. J. Kitching, J. Haxaire and P. D. N. Hebert. 2011. When species matches are unavailable are DNA barcodes correctly assigned to higher taxa? An assessment using sphingid moths. BMC Ecology 11: 18–18. Wilson, J. J., K. W. Sing and M. S. Azirun. 2013. Building a DNA barcode reference library for the true butterflies (Lepidoptera) of Peninsula

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Malaysia: what about the subspecies? PLoS ONE 8: e79969. Yue, Q. Y., K. L. Wu, D. Y. Qiu, J. Hu, D. X. Liu, X. Y. Wei, J. Chen and C. E. Cook. 2014. A formal re-description of the cockroach Hebardina concinna Anchored on DNA barcodes confirms wing polymorphism and identifies morphological characters for field identification. PLoS ONE 9: e106789. Zahiri, R., J. D. Lafontaine, B. C. Schmidt, E. V. Zakharov and P. D. N. Hebert. 2014. A transcontinental challenge – a test of DNA barcode performance for 1,541 species of Canadian Noctuoidea (Lepidoptera). PLoS ONE 9: e92797.

Zaldívar-Riverón, A., J. J. Martínez, F. S. Ceccarelli, V. S. De Jesús-Bonilla, A. C. Rodríguez-Pérez, A. Reséndiz-Flores and M. A. Smith. 2010. DNA barcoding a highly diverse group of parasitoid wasps (Braconidae: Doryctinae) from a Mexican nature reserve. Mitochondrial DNA 21 (S1): 18–23. Zhou, X., S. J. Adamowicz, L. M. Jacobus, R. E. DeWalt and P. D. N. Hebert. 2009. Towards a comprehensive barcode library for arctic life—Ephemeroptera, Plecoptera, and Trichoptera of Churchill, Manitoba, Canada. Frontiers in Zoology 6: 30.

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18 Insect Biodiversity Informatics Norman F. Johnson Department of Evolution, Ecology and Organismal Biology and Department of Entomology, Ohio State University, Columbus, Ohio, USA

One of the hallmarks of natural science is its empirical nature. Repeatable observation of phenomena in the natural world is an essential element of the scientific process, and these observations, the data, are the foundations upon which our understanding of the world is based. Biodiversity informatics, in the sense that I will use it throughout this chapter, refers to the acquisition, storage, dissemination, and analysis of data, particularly using electronic technolo­ gies (e.g., Soberón and Peterson 2004). Today, we have greater access to data than ever before, and the volume of information is growing rap­ idly at the same time as the tools to integrate and analyze it are proliferating. My objective is to provide a brief overview of the field of biodi­ versity informatics, particularly as it applies to entomology, to provide context within which to understand and integrate future developments. It is all too easy to become immersed and bogged down in the technological details; this arcane knowledge is necessary at one level, but it obscures the bigger and more important picture. Nothing inherently distinguishes biodiversity informatics of insects and sets it apart from that of any other taxon. In practice, however, the nature and small size of insects and the enormity of insect collections impose some practical considerations. Efforts to digitally

capture and disseminate specimen data tradi­ tionally have been led by botanists and verte­ brate biologists. However, in the short time since the publication of the first edition of this book, such efforts have begun to become part of the standard operating procedure in system­ atics and biodiversity studies in general. In the context of the United States, this is evidenced by two changes effected by the US National Science Foundation: (i) all grant proposals must now include a data management plan; and (ii) a new program, Advancing Digitization of Biodiversity Collections, and a national hub, iDigBio (www.idigbio.org), were established to promote digitization, employment of best practices, and sharing of data. “Big data” is just one of the latest hot fields to arise, and univer­ sities around the world are scrambling to develop programs to produce data scientists. Although there are more species and more individuals of insects than in any other group of terrestrial animals, evidence from entomol­ ogy on global issues such as the impact of cli­ mate change are typically anecdotal. On the hopeful side, the pace of work is accelerating, so we may soon achieve the critical mass of data that will enable us to understand the diver­ sity of life on the planet, conserve and preserve it for future generations, and use those data to help solve real‐world problems.

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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18.1 ­Biodiversity Data Introductory entomology courses commonly require students to make an insect collection. The effort and personal investment required to capture, examine, and identify the specimens are thought to contribute significantly to the learning process. One of the first things that we seek to emphasize to the students as they pre­ pare their specimens is the importance of proper labeling. Specimens each must be documented by means of a label that is physically attached. Such labels were once handwritten, but now typically are printed. On the label is docu­ mented, minimally, the collecting locality and the date(s) of collection. These elementary pieces of information are the core of the data domain of biodiversity informatics. The small size of most insect specimens dictates that the labels also be small, typically somewhere on the scale of 1.0 × 1.5 cm, and printed in 4‐point type. By contrast, a herbarium sheet has extensive space available not only for the collecting data, but also for comments to be added to the speci­ men by scientists who study it. Hence, insect labels commonly use abbreviations to conserve space and reduce writer’s cramp. These abbre­ viations, however, can be problematical. As one example, collectors commonly used the abbre­ viation “Ar.” for the state of Arizona, an abbre­ viation that now, with the standardization of postal codes in 1963, refers to the state of Arkansas. Time and place may be supplemented by additional data, such as the person(s) making the collection (agents), the method used to col­ lect the specimen, the habitat or microhabitat in which the specimen was found, and other organisms that were associated with the speci­ men (e.g., the host of a parasitoid). A final cru­ cial element is the identification of the specimen. These data constitute a primary specimen‐ occurrence record (Chapman 2005). Beyond the museum, observations have all of the same data elements as specimens, differing only in that a physical voucher is not preserved. Akin to birdwatching, butterfly and odonate

watching are rapidly growing in popularity, both in sciences and as a hobby. The lack of any phys­ ical evidence in support of the identification of the organism seen can be problematical. Nevertheless, this might have to suffice in cases of well‐known taxa, such as monarch butter­ flies, or highly endangered populations (e.g., the whooping crane). Photographs, videos, and sound recordings may be thought of as speci­ men surrogates, bridging the gap, and providing some documentation in support of the identifi­ cation. Tremendous masses of data are based on observations of birds (eBird.org), plants (plants. usda.gov), and species important in fisheries (oceanadapt.rutgers.edu). By contrast, the dis­ tribution in time and space of the vast majority of insect species is based entirely on preserved specimens. From these core data, biodiversity informatics also touches on a range of other domains. As suggested earlier for observations, digital media are important as documentation, and can some­ times serve as effective substitutes for an actual specimen. In some contexts, the term “digitiza­ tion” specifically refers to the capture of a digital image of a specimen. In others, the focus is on converting text from labels (or field notes) into a digital format, and sometimes both activities are implied. Digital media today include images, three‐dimensional models, videos, and sounds. Data such as time and place of occurrence are extrinsic to the organism itself. Intrinsic fea­ tures are of equal interest to researchers, includ­ ing gender, life stage, age, physical characteristics (e.g., size and color), and biochemical features, particularly DNA sequences. Traditionally, these features probably would be called charac­ ters or character states, but in popular jargon they are also referred to by the terms “pheno­ type”, its derivative “phenoscape” (e.g., phe­ noscape.org), and “traits” (e.g., Kleyer et  al. 2008; www.leda‐traitbase.org). The characteris­ tics of organisms are, arguably, what make them interesting to most people. Therefore, managing those data and linking them to their sources – the specimens and observations – is crucial.

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18.2 ­Technical Infrastructure The primary tool used for data storage and retrieval is a relational database, and numerous books on relational theory are available (e.g., Date 2004). A number of applications have been developed for the management of primary spec­ imen‐occurrence data, which provide a soft­ ware layer between the database management system and the user. The iDigBio portal offers brief reviews of a number of available products (www.idigbio.org/content/biological‐collections‐ databases). These packages sometimes are criticized as being overly complicated, but this assessment underplays the fairly complex nature of biodiversity data. Effectively handling the taxonomic names associated with species requires consideration of issues of synonymy, homonymy, and alternative and changed classi­ fications. Geographic names and the bounda­ ries of the areas they represent change with time and governments. Recording the names of the people that make the collections or determine the identity of the specimens is important in many contexts. The time of collection may be expressed as a single day, a range of days, or even a specific time of day. Finally, each taxo­ nomic group has its idiosyncratic data require­ ments, such as host or microhabitat. Developing a single piece of software to meet such varied needs inevitably results in more complexity than is required by any single user. The choice of a database‐management system and a database application to facilitate the pro­ cess of data entry and retrieval should be based on the needs of the user. As those needs and desires for the system increase over time, a more robust and general solution might be able to accommodate such growth more easily than a relatively simple, but specific, application. Migration of data from one system to another can be done, but it is never a pleasant process. A user might find it necessary to create a new cus­ tom software application to meet the needs of a project. Modular software design and open‐ source development may help to accelerate the

further development of biodiversity informatics software. Two different approaches to information management will be encountered in the litera­ ture and on the Internet. These may be termed a “taxon‐based approach” versus an “event‐ based approach.” As its name implies, a taxon‐ based database is organized on the basis of the taxa involved, aggregating the information on distribution, phenology, ecology, and other attributes. One prominent example is the Fauna Europaea project (www.faunaeur.org). More powerful, at least in theory, are event‐based databases, such as the one on caterpillars of the Guanacaste Conservation Area (Janzen and Hallwachs 2005). These databases document individual events, such as the collection or accession of a specimen or the rearing of a para­ sitoid. These data then can be aggregated and the results displayed in the same format as a taxon‐based database. An event‐based approach also provides the ability to organize the data along dimensions other than taxonomic group. This flexibility and power is achieved at the cost of processing time, overall database size, and programming requirements. The costs of both kinds of approach have dropped dramatically in recent years. Discussions of specimen databases are usually made in the context of collection management. A database can be a valuable administrative tool, enabling a curator to keep abreast of the status of loans, document the holdings of the collection in detail, and quickly respond to que­ ries for information. However, such a database can be invaluable for the practicing biodiversity scientist. It can facilitate the management of incoming loans of specimens, annotation of individual specimen records (e.g., for anoma­ lous features), correlation of features with geo­ graphic and temporal data, production of accurate and consistent documentation of the material examined in a study, mapping and comparison of geographic distributions, and quantitative documentation of the flight peri­ ods of adults. For the consumer of scientific

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products, databased specimen‐level informa­ tion provides an “audit trail” by which readers can judge whether the conclusions in the paper are supported by the evidence. Prospective capture of specimen‐occurrence data (i.e., recording the collecting information at the time that specimens are initially pro­ cessed) is relatively straightforward. A typical collecting regimen, such as a Malaise trap sam­ ple, will have large numbers of specimens, all of which share the same data on the time, place, method, habitat, and names of collectors. Those people with first‐hand knowledge of the collect­ ing event are often available to resolve any ambiguities. Retrospective data capture (i.e., recording data from existing collections, per­ haps with specimens collected more than a cen­ tury ago) brings many additional problems. Because of the small size of insect labels, impor­ tant data elements might be abbreviated or omitted entirely and assumed to be implicit. The meaning of the string “4/9/06” could be 9 April 2006, or 4 September 1906, or something else entirely. Handwritten labels are often diffi­ cult to decipher. These ambiguities and the time needed to resolve them raise the overall cost of data capture. In some cases, these issues can be resolved only by those with a detailed under­ standing of the collectors, the institutions, or  the taxa involved. The Entomological Collections Network (ECN) endorsed the idea that retrospective data capture be incorporated into the workflow of systematic research (Thompson 1994). The scientists involved in revisionary studies are often in the best position to interpret the sometimes cryptic information on insect labels. Georeferencing is the conversion of textual descriptions of places into a coordinate system. A specimen that is not georeferenced is rarely of any use in any biologically interesting sense. Plotting of the georeferenced localities on a map makes egregious data‐entry errors immediately apparent. In addition, the process of searching for latitude and longitude for named places reveals alternative or incorrect spellings of locality names. Chapman and Wieczorek (2006)

have developed a best‐practices document for georeferencing. A number of sources are avail­ able online to determine latitude and longitude for named localities (Chapman and Wieczorek 2006, Johnson 2007). The coordinates of named places, of course, rarely represent the precise location where a specimen was collected. Therefore, additional calculations might be nec­ essary to indicate more accurately the position of the collecting locality. A Web‐based applica­ tion for this purpose was developed as part of the Mammal Networked Information System (manisnet.org/gci2.html). A measure of proba­ ble error, commonly represented as a radius from a point (Wieczorek et al. 2004), is crucial for assessing the “fitness for use” of the data (Chapman 2005b). One of the implications of a relational data­ base is that the information for each record must be individually identifiable, that is, it needs some sort of unique identifier. In the case of specimens, the identifier is linked to the physi­ cal specimen, normally by adding a label. This process is a fairly traditional accession practice in many types of collections. But in insect col­ lections with several million specimens, it defi­ nitely has not been standard procedure. The use of barcode labels has been promoted as a mech­ anism to facilitate the link between data in the computer and the specimen to which it pertains (e.g., Janzen 1992, Thompson 1994). (To be absolutely clear, I am using the term barcode to refer to a mechanically readable set of symbols, not the fragment of mitochondrial or nuclear DNA used as a means of identifying taxa.) The ECN advocated the use of a Code 49 stacked barcode for insect specimens, primarily because of its compact size. Subsequently, however, two‐ dimensional formats have been developed that combine small size, easier scanning, and a greater capacity for information storage. The ECN proposed that the identifier consist of an abbreviation for the institution generating the initial record – not necessarily the owner of the specimen – and a number, the combination of which should be unique. The institutional abbreviations have typically been taken from

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Arnett et  al. (1993). This publication has been supplanted by biocol.org (Global Registry of Biodiversity Repositories). The identifier information should be both encoded in the barcode and printed in a human‐ readable form. In practice, the format of the barcode and whether it uses a machine‐readable format are not the critical elements. Rather, the uniqueness of the identifier is of utmost impor­ tance. The advantage of having a barcode is that it allows the identifier to be read and entered automatically into a computer, thus reducing the rate of input error. Creating a locally unique identifier is relatively easy, requiring only a min­ imal amount of bookkeeping to avoid the inad­ vertent reuse of a number. Guaranteeing that the identifier is globally unique is quite another matter. Chapman (2005b) provides a review of issues involved in data‐quality assurance. Mistakes in data entry are unavoidable. They can be reduced by the use of careful protocols and with good user interface design, but they will still occur. Many plant collections image the entirety of their herbarium sheets, extracting the part of the image containing labels and annotations, and using optical character recognition to convert those parts of the image into text (Drinkwater et al. 2014). Such technologies have not yet been applied widely to insect specimens. Drop‐down pick‐lists are commonly touted as a cure for typing errors, but mistakes still occur. Errors are simply inevitable, and a protocol for data review and correction should be estab­ lished. Guralnik and Neufeld (2005) describe one such methodology used to identify georef­ erencing errors, and Lampe and Striebing (2005) describe the data capture and quality‐assurance protocol for a large insect collection.

18.3 ­Standards Sharing of specimens and their data are an essential component of the biodiversity research agenda. The insect collections of the largest natural history museums, such as the National

Museum of Natural History in Washington DC, the American Museum of Natural History in New York, The Natural History Museum in London, and the Muséum National d’Histoire Naturelle in Paris, each hold more than 10 mil­ lion specimens. In spite of the size of their col­ lections (and accepting the accuracy of their estimates), each institution has on average a maximum of only one‐ or two‐dozen specimens of each species, simply due to the magnitude of insect diversity – rough estimates put the global number of insect species at between 1 million to 30 million. More to the point, this approxima­ tion indicates that for the vast majority of groups, the holdings of a single institution are unlikely to suffice for a well‐founded scientific investigation. Researchers commonly borrow materials for study from several collections, temporarily pooling the holdings to obtain the best sampling of biodiversity possible within the constraints of time and funding. With the advent of widespread networking in the past 20 years, it has become practical for institutions, and even individual scientists, to share their data with others. In a one‐on‐one exchange of information, this process is fairly straightforward. The provider supplies a description of the structure of their data – the metadata  –  to the consumer, specifying how a data record is put together and what the indi­ vidual elements of each record are intended to represent. The consumer can then either adopt the provider’s data structure or map it to their own. However, as the number of data providers and consumers increases, this straightforward exchange can quickly spiral out of control with­ out a common agreement on data structure. Hence, we enter the realm of data standards. Ideally, data standards represent a commu­ nity‐wide consensus, or at least a compromise, on the structure, meaning, and interrelationship of individual pieces of information. At the most basic level, this may mean specification of the types of data represented, such as text, num­ bers, and dates, and how they are represented – for example, as UTF‐8 encoding, floating point numbers, integers, or W3C DTF. These issues

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are common to a wide variety of fields, and a great number of international standards are available from which to choose. More problem­ atic is the development and acceptance of stand­ ards for domain‐specific subjects. A good example of community data standards that precedes the Internet era is the International Code of Zoological Nomenclature (iczn.org), which specifies the criteria necessary for estab­ lishing the scientific names of animals, provides the means to decide among names in cases of conflict, and provides the conventions for how those names should be represented. Today, when we come across something like Megacyllene robiniae, the use of italics and capi­ talization of the first, but not the second word immediately indicates to a biologist that the words represent the name of a species. These conventions – the binomen, the use of a distinc­ tive font face (typically italics), and capitaliza­ tion patterns  –  are specifications found in the Code. Many zoological journals require that authors adhere to the Code in order for a manu­ script to be accepted for publication. The Code initially went into effect in 1905 and is now in its fourth edition (iczn.org/iczn/index.jsp), illus­ trating that standards can, in fact must, change over time to retain their relevance. Similar data standards began to be developed in 1985 under the auspices of a small convoca­ tion called the “Taxonomic Databases Working Group,” usually referred to as TDWG (pro­ nounced “tad‐wig” or “tad‐wog”). The initial makeup of TDWG was heavily biased toward botany and gained little traction in the zoologi­ cal or entomological communities. This has changed over subsequent years, spurred in large part by the development of the Internet, vastly increased and affordable computing power, and the accessibility of information technologies. In 2007, the group changed its formal name to the perhaps more accurate, but clumsier moniker “Biodiversity Information Standards (TDWG).” Its current mission is to “develop, adopt and promote standards and guidelines for the recording and exchange of data about organ­ isms” (www.tdwg.org/about‐tdwg).

The data standard that has achieved probably the greatest penetration in the community is the Darwin Core (DwC). The DwC was designed to present a simple format to define and represent the data elements associated with primary spec­ imen‐occurrence records. It is typically unstruc­ tured: each record consists of a series of data elements all at the same level, without any hier­ archical or other relationship between them. The specification for DwC is accessible through the TDWG website at rs.tdwg.org/dwc/. Use of DwC was significantly spurred by a simple implementation of it called the Darwin Core Archive file (Remsen et al. 2012), which allows for the highly efficient sharing of data sets. Minimally, this consists of a core data file and a metadata file. In the data file, each line (row) represents one data item, and fields within that line contain data for each data element. The identity of those elements is specified in the metadata file. Darwin Core Archive files are an effective means of sharing the large data sets associated with taxonomic papers in a format that is amenable to further analysis by users other than the original authors. As of March 2015, only three proposed stand­ ards have gone through the full process of devel­ opment and received approval from TDWG: the DwC, an applicability statement concerning the use of Life Sciences Identifiers (LSIDs) as glob­ ally unique identifiers for data objects, and TAPIR (the TDWG Access Protocol for Information Retrieval). TAPIR and its predeces­ sor, DiGIR (Distributed Generic Information Retrieval), are XML‐based protocols for defin­ ing both a query to a data provider and structur­ ing the desired response from that provider. The elements used in both query and response are DwC data elements. As initially designed (Robertson et al. 2014), the corpus of biodiver­ sity occurrence data was a distributed network with each data provider being responsible both for the data content and providing access to those data. Data aggregators, such as the Global Biodiversity Information Facility (www.gbif. org), served as a central mechanism to generate a single query that would then be sent to all

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relevant providers, aggregate the individual responses, and deliver that package back to the original user. As the network has grown, it has been modified so that GBIF harvests data records at regular intervals from data providers, maintains an indexed, cached copy of all data, and responds to queries from that centralized cache. The most common tool data providers use to expose data to the network is the Integrated Publishing Toolkit (IPT; Robertson et al. 2014). A standard such as the DwC works only if it is understood what each of the concepts (e.g., sci­ entificName) is intended to mean. If we attach a tag to a string of text that specifies its meaning, then we can be assured that the data encoded within that string is relevant to the question at hand. For example, the string “ACT” means quite different things when it is interpreted as a DNA sequence, a protein sequence, or a geo­ graphic entity. Labeling the string, such as ACT, specifies the meaning, especially if the “reader” is not a human who can infer the meaning from the context. Concepts, however, are rarely iso­ lated elements: they are related to other con­ cepts. Understanding and encoding those relationships makes it possible for a computer to “reason” that two items, although labeled dif­ ferently, are related to one another. Ontologies are the formal methods of specify­ ing entities and the relationships between them. Perhaps the most widely implemented ontology in the biological sciences is the Gene Ontology (geneontology.org, Gene Ontology Consortium 2015). A few ontologies for arthropods are avail­ able or are in development, including the Biological Collections Ontology, Biological Imaging Methods, Biological Spatial Ontology, Drosophila Gross Anatomy, Fly Taxonomy, Hymenoptera Anatomy Ontology, Mosquito Gross Anatomy and Tick Gross Anatomy. An extensive list of ontologies is available at www. obofoundry.org. Mabee et al. (2007) discuss the potential for linking and leveraging ontologies and semantic mark‐up to connect the seemingly disparate domains of genes, anatomy, and tax­ onomy to understand evolutionary history.

18.4 ­Current Status and Impediments to Progress Digitization of the data associated with speci­ mens is rapidly becoming standard operating procedure for collections. Fifteen years ago, the number of institutions engaged in capturing their data and making it accessible over the Web was minimal. Today, GBIF boasts that it pro­ vides access to more than 528 million occur­ rence records (data as of 13 March 2015). The US central aggregator, iDigBio (www.idigbio. org), claims to do the same for more than 27 million records. The hope is that these gains will stimulate further development and implemen­ tation of standards, and advances in the quan­ tity and quality of data made accessible to the public will continue. Half a billion records is a truly remarkable achievement, especially in the short timeframe of 10–15 years. A closer look, however, reveals significant shortcomings. Insects, arguably the most species‐rich group of terrestrial animals, make up only 7.8% of the GBIF records, and 15.4% of the iDigBio total. These records repre­ sent data sets from 656 and 29 sources, respec­ tively. Beyond specimens and occurrence data, no comprehensive listing exists for the species of insects that have been described and named. Among the largest orders of insects, compre­ hensive taxonomic databases are available for only the Orthoptera (orthoptera.speciesfile.org) and Diptera (www.diptera.org). Why the paucity of data? One issue is cost, both in time and money. Few, if any, rigorous data sets are available that document the costs of (i) data digitization, (ii) georeferencing, (iii) obtaining and maintaining high‐quality identifi­ cations of specimens, and (iv) overall quality assurance of the data. Even a rough working estimate of US$1 per specimen for all of these tasks amounts to millions for a modestly sized insect collection. The task is made larger because, unlike vertebrate or plant collections, accession of individual specimens and record­ ing of data at the time of accession has not been

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standard practice. Hence, a digitization project will typically face decades of backlogged data to be recorded. Individual curators will also differ, sometimes substantially, in their threshold of criteria in order to declare that data sets are suitable for release to the public. There should be a minimal level of accuracy in data transcription and pars­ ing before publication, but community stand­ ards on that level have not been reached. More importantly, however, it seems that the level of quality assurance in the taxonomic names applied to specimens is the overwhelming impediment. Without master data dictionaries for taxonomic names, it is difficult for curators to be assured that the names they are using are those currently considered valid. And no collec­ tion, not even the largest, has sufficient taxo­ nomic expertise on their staff to ensure that the identifications themselves are of the highest possible quality. Thus, some have suggested to me that releasing a data set with apparently inaccurate identifications is worse than releas­ ing no data at all. With that standard, precious few data sets would be made public. The coun­ ter‐argument is that exposing data, along with its possible flaws, is the most efficient way to find and correct those errors. It often turns out that the specialist’s understanding of the distri­ butional range of species and range of variation in characters must be amended. Thus, a flawed data set  –  assuming reasonable data cleansing for typographical errors and orthography  –  is not necessarily the result of a cavalier attitude toward data quality, but a sincere effort to actu­ ally increase that quality. Finally, another impediment to the publica­ tion of more data sets is the moving target of technical infrastructure. Hardware, software, and data standards are evolving far faster than the pace of data capture and publication. I pur­ posely have avoided discussion of topics such as RDF, XML, and JSON, as these change so rap­ idly. Long‐term maintenance of digital resources is an issue that hovers over all such efforts. Archived data, using simple data structures in standard encoding (e.g., DwC Archives), are

valuable and necessary. A greater problem is maintaining access to the functionality of a digi­ tal resource over the long term. As in all areas of human endeavor, uncertainty leads to delay in undertaking initiatives.

18.5 ­Prospects In our times of restricted and, it seems, ever constricting budgets, it is crucial to be able to document and demonstrate the value of speci­ mens and collections. Providing ready access to data increases the ability of researchers to find materials relevant to the questions they are ask­ ing, makes it economically more feasible to include those data in their projects, and thus increases the impact of every collection on research. With few exceptions, no single collec­ tion possesses the depth and breadth of repre­ sentation of a taxon to serve as the sole resource for good science. Either because of historical factors or conscious choice, the holdings of col­ lections are largely complementary. Even the smallest regional collection often provides data available nowhere else, thus contributing to the quality of the work. These resources must be cherished and protected, and the first step toward this is being able to demonstrate their impact nationally and internationally. The efforts that the community has invested in biodiversity informatics imply that such data are valuable. This may seem a truism, but it is only relatively recently that the data underlying the results in scientific publications have begun to be made explicitly available for use or re‐use. The concept of open, linked data (i.e., electroni­ cally accessible), in conjunction with open access to scientific works, puts the emphasis squarely on the societal investment in science and the return on that investment to the public at large. I see two advantages to this. First, it provides an explicit and verifiable empirical basis for biodiversity science. The evidence leading to the conclusions reached in a study can be independently assessed, leading to great­ ­er confidence in the results and highlighting

18  Insect Biodiversity Informatics

needs for further data and increased transpar­ ency in the scientific process. Second, the data collected for one purpose may be reused to address another question, often a question that never entered the mind of the original researcher. Particularly striking is an anecdote cited by Murray‐Rust (2008): “…what scientific quantity could possibly be deduced from ancient Chinese eclipse records? Yet, K. D. Pang, K. Yau, and H.‐H. Chou [1995] showed that this gave a value for the variation of the earth’s rotation during the postglacial rebound and from this deduced a value for the lower mantle viscosity of the earth.” The support for the general princi­ ple of open biodiversity data is embodied in the Bouchout Declaration, signed by 96 organi­ zations and more than 200 individuals (www. bouchoutdeclaration.org). Innovations in science seem to follow a life cycle akin to business. Today, scanning electron microscopes and DNA sequencing are common and widespread, but both were technological innovations that swept into systematics and tax­ onomy with profound consequences. Initially, however, publications using these tools were more in the vein of demonstration projects that illustrated their potential. Actually integrating them into the toolbox of biodiversity scientists and leveraging them to address important ques­ tions was a more long‐term and laborious process. Information technologies seem to be follow­ ing the same developmental arc as other inno­ vations. For more than a decade, publications have touted the potential of using such tools both to better understand the past and predict the future. The time has come to realize that potential, and we know some of the important tasks that are needed. The metadata for speci­ mens in collections must be captured, parsed, and made accessible. Taxonomic names and concepts are the glue that connects data domains relevant to biodiversity. We urgently require authoritative and complete digital resources that document the names available, their correspondence to one another and to tax­ onomic concepts, and documentation of their

history and use  –  all of this, of course, while implementing community data standards. Finally, bringing the increasing number of so‐ called “dark taxa” to light – that is, taxa recorded in databases such as GenBank but not identified to a named taxon – will require a great deal of fundamental alpha taxonomy to be done, work that is already significantly facilitated through open access to data and printed and electronic literature. Moving beyond interesting, but lim­ ited demonstration projects will require the resolve and resources to undertake and see major tasks through to completion. The ways to do this are already in place, but it remains for the means to be allocated to the task.

­Acknowledgments I thank L. Musetti, D. Agosti, and J. Cora for dis­ cussions and stimulating interest in this area.

­References Arnett, R. H., G. A. Samuelson, and G. M. Nishida. 1993. The insect and spider collections of the world. 2nd edition. Sandhill Crane Press, Gainesville, FL. 310 pp. Chapman, A. D. 2005a. Uses of primary species‐ occurrence data, version 1.0. Report for the Global Biodiversity Information Facility, Copenhagen. www.gbif.org/resource/80545 [Accessed 23 March 2015]. Chapman, A. D. 2005b. Principles of Data Quality, Version 1.0. Global Biodiversity Information Facility, Copenhagen. 58 pp. Chapman, A. D. and J. Wieczorek (eds). 2006. Guide to Best Practices for Georeferencing. Global Biodiversity Information Facility, Copenhagen. 80 pp. Date, C. J. 2004. An Introduction to Database Systems. 8th edition. Pearson/Addison Wesley, Boston, MA. 983 pp. Drinkwater, R. E., R. W. N. Cubey and E. M. Haston. 2014. The use of Optical Character Recognition (OCR) in the digitization

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of herbarium museum label. PhytoKeys 38: 15–30. Gene Ontology Consortium. 2015. Gene Ontology Consortium: going forward. Nucleic Acids Research 43: D1049–D1056. Guralnik, R. P. and D. Neufeld. 2005. Challenges building online GIS services to support global biodiversity mapping and analysis: lessons from the Mountain and Plains Database and Informatics Project. Biodiversity Informatics 2: 57–69. Janzen, D. H. 1992. Information on the bar code system that INBio uses in Costa Rica. Insect Collection News 7: 24. Janzen, D. H. and W. Hallwachs. 2005. Caterpillars, pupae, butterflies & moths of the ACG. janzen. sas.upenn.edu [Accessed 23 March 2015]. Johnson, N. F. 2007. Biodiversity informatics. Annual Review of Entomology 52: 421–438. Kleyer, M., R. M. Bekker, I. C. Knevel, J. P. Bakker, K. Thompson, M. Sonnenschein, P. Poschlod, J. M. Van Groenendael, L. Klimes, J. Klimesová, S. Klotz, G. M. Rusch, M. Hermy, D. Adriaens, G. Boedeltje, B. Bossuyt, A. Dannemann, P. Endels, L. Götzenberger, J. G. Hodgson, A.‐K. Jackel, I. Kühn, D. Kunzmann, W. A. Ozinga, C. Römermann, M. Stadler, J. Schlegelmilch, H. J. Steendam, O. Tackenberg, B. Wilmann, J. H.C Cornelissen, O. Eriksson, E. Garnier, and B. Peco. 2008. The LEDA Traitbase: A database of life‐history traits of Northwest European flora. Journal of Ecology 96: 1266–1274. Lampe, K.‐H. and D. Striebing. 2005. How to digitize large insect collections: preliminary results of the DIG project. Pp. 385–393. In B. A. Huber, B. J. Sinclair and K.‐H. Lampe (eds). African Biodiversity: Molecules, Organisms, Ecosystems. Springer Science/Business Media, New York.

Mabee, P. M., G. Arratia, M. Coburn, M. Haendel, E. J. Hilton, J. G. Lundberg, R. L. Mayden, N. Rios, and M. Westerfield. 2007. Connecting evolutionary morphology to genomics using ontologies: a case study from Cypriniformes including zebrafish. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 308B: 655–668. Murray‐Rust, P. 2008. Open data in science. Serials Review 34: 52–64. Pang, K. D., K. C. Yau and H.‐H. Chou. 1995. The Earth’s palaeorotation, postglacial rebound, and lower mantle viscosity from analysis of ancient Chinese eclipse records. Pure and Applied Geophysics 145: 459–485. Remsen, D., S. Knapp, T. Georgiev, P. Stoev and L. Penev. 2012. From text to structured data: converting a word‐processed floristic checklist into Darwin Core Archive format. PhytoKeys 9: 1–13. Robertson, T., M. Döring, R. Guralnick, D. Bloom, J. Wieczorek, K. Braak, J. Otegui, L. Russel and P. Desmet. 2014. The GBIF Integrated Publishing Toolkit: facilitating the efficient publishing of biodiversity data on the Internet. PLoS ONE 9 (8): e102623. Soberón, J. and A. T. Peterson. 2004. Biodiversity informatics: managing and applying primary biodiversity data. Philosophical Transactions of the Royal Society B 359: 689–698. Thompson, F. C. 1994. Bar codes for specimen data management. Insect Collection News 9: 2–4. Wieczorek, J., Q. Guo and R. Jijmans. 2004. The point‐radius method for georeferencing locality descriptions and calculating associated uncertainty. International Journal of Geographical Information Systems 18: 745–767.

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19 Parasitoid Biodiversity and Insect Pest Management John Heraty Department of Entomology, University of California, Riverside, California, USA

The regulation of insects by other insects involves predators, parasites, or parasitoids. Predators consume multiple hosts, and parasites take their nutrition from a host but do not necessarily kill it. Parasitoids, however, use and kill a single host individual (Askew 1971). An understanding of the species richness of parasitoids, where they are most diverse, and how they interact is necessary for implementing effective insect pest management. The diversity of natural enemies is usually lowest or non‐ existent for newly introduced pests. In a system out of balance with its natural enemies, pest populations can explode, with devastating consequences. Niche specialization, keystone species, potential cascade effects with parasitoid extinction, and the ecological importance of parasitoids are all factors affecting this delicate balance (Greathead 1986, Hawkins et  al. 1992, LaSalle and Gauld 1993, Hawkins 1994). Introduced pests may be brought under control through the addition of one or more natural enemies from the country of origin, or through the effect of host shifts by native predators or parasitoids (Huffaker 1969, Clausen 1978, Caltagirone 1981, Smith 1993, Van Driesche and Bellows 1996). Biological control programs in agricultural systems over the past century provide key insights into future problems that will be caused by habitat fragmentation, climate change, and loss of primary habitat in all ecosys-

tems. This information can not only help us to manage pests within urban, forest, or agricultural systems, but also provide the impetus for preserving native habitat and conserving parasitoid biodiversity. Is parasitoid diversity necessary for effective pest management? The number of parasitoid species necessary to provide control remains an important and controversial issue (Myers et  al. 1989, Rodríguez and Hawkins 2000, Muller and Brodeur 2002, Cardinale et al. 2003, Bianchi et al. 2006, Crowder and Jabbour 2014). Suppression of introduced pests can be achieved through the introduction of a single parasitoid. Cassava mealybug was controlled by Apoanagyrus lopezi (Encyrtidae) (Neuenschwander 2001), and the Rhodesgrass mealybug was controlled by Neodusmetia sangwani (Encyrtidae) (Clausen 1978). A combination of predator and parasitoid might be necessary for control. The Comstock mealybug is controlled by a predator, Rodolia ­cardinalis (Coccinellidae), and the parasitoid  Cryptochaetum iceryae (Cryptochaetidae) (Huffaker 1969). A complex of several parasitoids might be necessary, as in control of the woolly whitefly by Amitus spinifrons (Platygastridae) and Cales noacki (Aphelinidae) (DeBach and Rose 1971), and the citrus leaf‐miner by a diverse array of both introduced and native parasitoids (Peña et al. 1996, 2000). One species might be sufficient, but in general, better control can be achieved with

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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a diverse array of parasitoids and surrounding habitat diversity (Bianchi et al. 2006, Bennett and Gratton 2012, Crowder and Jabbour 2014). At what level does parasitoid biodiversity and distribution affect our ability to control pest insects? A common assumption in biological control is that pest populations are regulated by one or more insects in their native range. Importance, therefore, is placed on replacing this balance of native control agents against the introduced pest. Simple replacement, however, might not be effective for a number of reasons. Even within a single species, genetic, behavioral, and even associated endosymbiont attributes across the native range can differ significantly, making matches between hosts and effective parasitoids difficult. Morphologically similar (cryptic) species can interfere with each other through ineffective mating, decreasing their ability to lower pest populations (Stouthamer et al. 2000b, Havill et al. 2012). Different environmental conditions in the new host range can favor the host over the most effective natural enemy, and in some cases it then becomes more important to find different populations or species more suitable to these conditions. Lastly, in large monocultures with little access to secondary habitats, the biodiversity of natural enemies can decline and affect natural insect control (Kruess and Tschartke 1994, Fisher 1998, Landis et  al. 2005, Bianchi et  al. 2006, Crowder and Jabbour 2014). This last factor affects not only the introduced populations of a pest that arrive without their natural enemies, but also can lead to novel pest status for species in their native range as parasitoid reservoirs are depleted. Under these circumstances, conservation of natural enemies within native ranges assumes even greater importance. How many parasitoids are there? Parasitoid abundance and diversity in most ecosystems remain a mystery, with the proportion of described versus undescribed (estimated) species surprisingly small. Taxonomists remain focused on morphological species recognition, but now molecular methods are revealing numerous morphologically distinct but ­reproductively isolated cryptic species

of parasitoids. The expected decline and extinction of these parasitoids as a result of habitat fragmentation, agricultural expansion, and climate change will have a dramatic effect on pest abundance and species richness. Without any real idea of the diversity and abundance of parasitoids, we have no idea what we are losing. We must, as a society, develop a better understanding of parasitoids and their diversity, distribution, and behavior if we can ever expect to control the primary trophic levels of insect diversity, especially before these changes become irreversible on a global scale.

19.1 ­What Is a Parasitoid? Parasitism is defined as the relationship between two organisms, whereby the parasite obtains some or all of its nutrients from the other (Askew 1971). Among insect parasites, hosts generally are confined to the animal kingdom, although in its most extreme form, parasitism has been defined to include specialist herbivorous insects (Price 1980). This latter definition has not been accepted. The parasitoid lifestyle is a specialized subset of parasitism that includes those species that feed on and kill a single arthropod host, although even here the boundaries can be vague and problematic. The act of parasitism (i.e., how hosts are located and eggs deposited) is essentially the same for parasites and parasitoids, and the use of a distinct term such as “parasitoidism” (Eggleton and Belshaw 1992) is unwarranted. Eggleton and Gaston (1990) applied the term parasitoid only to an organism that “develops on or in another single (‘host’) organism, extracts nourishment from it, and kills it as a direct or indirect result of that development.” Eggleton and Belshaw (1992) restricted their definition to exclude (i) facultative relationships, in which an organism feeds on a host that is already in the process of dying but not dying as a direct result of parasitism; (ii) species that feed on multiple individuals, such as eggs, in an enclosed space; (iii) social insect parasites, in which an organism is responsible for killing a colony; (iv) species that castrate but do not kill their host; and (v)

19  Parasitoid Biodiversity and Insect Pest Management

herbivores, including seed predators. Phorid flies in the genus Apocephalus provide a good example of facultative parasitoids. Adult flies lay their eggs in recently dead or dying ants – they are not the direct cause of death (Morehead et al. 2001). The ancestral habit for related phorids in this case might be either saprophagy or parasitism. Social insect parasites are largely aculeate wasps that specifically target reproductive females in a host colony; these social parasites have invariably developed from a closely related, non‐parasitic ancestor. Castration or behavioral modification interfering with reproductive success occurs commonly in strepsipteran parasites. In Strepsiptera, the Mengenillidae may be true parasitoids of Thysanoptera and kill the host, but the remaining Strepsiptera act as castrators, with the host surviving the parasitic event. Certain parasitoid groups excluded by the above restrictions have a clear phylogenetic association with a parasitoid ancestor. Species that attack eggs in enclosed sacs or multiple larvae in insect galls or seeds usually have been considered specialized predators, but in many cases, especially in Hymenoptera, they are considered to have developed from a parasitoid ancestor. Seed predators such as Megastigmus (Torymidae) and Bruchophagus (Eurytomidae) feed individually on seeds of Rubiaceae or Fabaceae, respectively. Both genera are descended from ancestors that were insect parasitoids, and in many respects they are simply specialized parasitoids. Cleptoparasitoids are a subset of insect parasitoids that use both the host and its provisioned resources or only its provisioned resources for growth, and have evolved multiple times in Coleoptera, Diptera, and Hymenoptera. Parasitoids are generally terminal evolutionary units that do not evolve into other lifestyles, except for those groups within Hymenoptera that have subsequently evolved into gall‐forming and endophytic phytophages, host‐directed cleptoparasites, predators of eggs and larvae, provisioning predators (Aculeata), and provisioning omnivores (Formicidae) (Eggleton and Belshaw 1992). Irrespective of some of the nuances of distinguishing a ­parasitoid from a predator, s­aprophage, or parasite, the

semantics are important. The issues affecting ecological biodiversity, host usage, and phylogenetic radiation can be distinctly different, assuming different levels of taxon inclusiveness (cf. Wiegmann et al. 1993). Among insects, true parasitoids are found only in the Holometabola, with only larvae acting as the parasitic stage. Parasitoids can be solitary, gregarious (multiple eggs deposited), or polyembryonic (multiple larvae developing from a single egg). All life stages of a host can be attacked, although eggs and immature stages are the most commonly used host stages. Parasitoid larvae can develop on a single host stage (idiobiont) or through multiple host stages (koinobiont) (Quicke 1997). Generally, most idiobionts are ectoparasitoids (external) and most koinobionts are endoparasitoids (internal). More rarely, a parasitoid can use a combination of strategies. For example, in hyperparasitic Perilampidae (Hymenoptera), the first‐instar larva is endoparasitic in multiple instars of the primary host, then ectoparasitic on the primary parasitoid larva, and finally ectoparasitic on the parasitoid pupa (Smith 1912, Laing and Heraty 1981, Heraty and Murray 2013). Parasitoid lifestyles are further complicated by species that attack previously parasitized hosts (hyperparasitoids), place eggs of different sexes in individuals of the same parasitoid species (autoparasitism), or place eggs in different host species (heteronomy) (Quicke 1997, Hunter and Woolley 2001). Together, these life‐cycle strategies are embodied in a tremendously diverse community of parasitoids attacking almost every possible host niche available (Hawkins et al. 1992, Hawkins 1994).

19.2 ­Biodiversity and Success of Insect Parasitoids The number of insect species is staggering. Conservative estimates range from 2.4 million to 10 million species (Gaston 1991, LaSalle and Gauld 1992, Gaston et  al. 1996, Grissell 1999, Noyes 2000, Mora et al. 2011). Of these, just over 900,000 species have been described (Chapman

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2009). Eggleton and Belshaw (1992) estimated the total number of insect parasitoids to be 87,000 species, or roughly 10% of all described insects. A review of recent estimates suggests that there could be as many as 700,000 species of parasitoids (Table 19.1). The biology and biodiversity of parasitoids has been thoroughly reviewed by Clausen (1940), Askew (1971), and Quicke (1997), with an excellent summary of their biology and biodiversity in Eggleton and Belshaw (1992). Parasitoids are distributed among seven different orders of Holometabola (Coleoptera, Lepidoptera, Diptera, Neuroptera, Strepsiptera, Trichoptera, and Hymenoptera), with by far the greatest species biodiversity and numerical abundance in Hymenoptera. Parasitoids are proposed to have developed only once in Hymenoptera, Strepsiptera, Neuroptera, and Trichoptera, but independently at least 10 times in Coleoptera, twice in Lepidoptera, and 21 times in Diptera (Eggleton and Belshaw 1992). Parasitism of a single host is not necessarily a universally successful adaptation. Parasitoids are rare in the Lepidoptera, Neuroptera, and Trichoptera, and most common in the Diptera and Hymenoptera. Parasitic Hymenoptera, and Tachinidae and Phoridae within the Diptera, are species rich and numerically abundant, but most other parasitic groups are not diverse and are rarely encountered. To determine whether parasitism was a successful adaptation, Wiegmann et  al. (1993) compared the relative species richness of parasitic and non‐parasitic sister groups for 15 lineages, including lice, fleas, and other groups that are not true parasitoids. Some parasitic groups, such as Phoridae, were not considered in their analyses because of uncertain phylogenetic relationships between parasitic and non‐parasitic taxa in the family. Only six of the parasitic groups were more diverse than their non‐parasitic sister taxa, suggesting that parasitism overall is not a strategy leading consistently to rapid diversification of a group. Even when the analysis was restricted to 11 “parasitoid” taxa, only four (Mantispinae, Sarcophagidae (Blaesoxipha), Tachinidae, and

Hymenoptera) were more diverse than their non‐parasitoid sister taxa. Although the evolution of a parasitoid lifestyle might not be consistently successful, the numerical abundance and diversification, especially of parasitic flies and wasps, is difficult to dispute and worth examining further. In terms of their overall contribution to parasitoid biodiversity, the Hymenoptera, Phoridae, and Tachinidae deserve special attention. These three groups contain roughly 74,000 described species, with potentially as many as 670,000 morphologically distinct species (Table 19.1). The Tachinidae and Hymenoptera are by far the most important groups in agroecosystem pest management (Genier 1988, LaSalle 1993). Other parasitoid groups have importance in the control of their insect hosts, but few of these have been used for biological control (cf. Huffaker 1969, Clausen 1978, Caltagirone 1981). Some rare cases of agroeconomic importance include the release of the moth parasitoid Chalcoela (Pyralidae) against Polistes (Vespidae) in the Galápagos Islands, and Cryptochaetum iceryae (Cryptochaetidae) against the cottony cushion scale. 19.2.1  Hymenoptera (Apocrita)

More than 80% of all parasitoid species (about 115,000 species have been described) belong to the Hymenoptera (Eggleton and Belshaw 1992, Quicke 1997). The order contains 20 superfamilies and 89 families, with its highest biodiversity in the suborder Apocrita (Goulet and Huber 1993). The Hymenoptera are comprised of two suborders, the paraphyletic Symphyta, which are either herbivores or mycophages, and the Orussidae  +  Apocrita (Vespina sensu Rasnitsyn 1988), with the evolution of true parasitoids as a shared feature of both groups. Within Apocrita, phytophagy, egg‐sac predation, provisioning predators (Sphecidae, Pompilidae), and provisioning omnivores (ants and bees) have evolved several times (Eggleton and Belshaw 1992). The vast species richness and numerical abundance of parasitoids are contained in just four superfamilies, the Ichneumonoidea, Cynipoidea, Platygastroidea, and Chalcidoidea,

19  Parasitoid Biodiversity and Insect Pest Management

Table 19.1  Described and estimated species of parasitoids Taxon

Described spp.

Estimated spp.

Neuroptera

503

503,*

12

1012,*

Trichoptera

10

Lepidoptera

113

Strepsiptera

10

3

Coleoptera

1,6003,*

113,* 103 3,*

Diptera

15,600

‐ Tachinidae

9,98913 14

1,6003,* 50,600* 20,00013 20,000–25,00014

‐ Phoridae

3,657

Hymenoptera

60,0003,*

630,000*

11

60,5002,5

‐ Ichneumonidae

23,331

‐ Braconidae

17,60511 2,4

‐ Platygastroidea

4,022

‐ Cynipoidea

2,8276

20,000–25,0002,5,8 10,0005 25,0001

10

‐ Chalcidoidea

22,000

Rough total

77,000

375,000–500,0007,9,10 680,000

1) Nordlander 1984. 2) Gaston 1991. 3) Eggleton and Belshaw 1992. 4) Gaston 1993. 5) Goulet and Huber 1993. 6) Ronquist 1995. 7) Noyes 2000. 8) Dolphin and Quicke 2001. 9) Heraty and Gates 2003. 10) Noyes 2007. 11) Yu et al, 2004. 12) Wells 2005. 13) Stireman 2006. 14) B. V. Brown (personal communication) estimates that as many as half of all phorids (40,000–50,000 species) are parasitic. *These numbers of parasitoid species were not estimated by these authors; the values for Diptera and Hymenoptera were increased by including estimates from other papers.

which together contain more than 54,000 described species (Table 19.1). The number of estimated species in each of these groups is vastly out of proportion with the numbers of described species, with as many as 620,000 species estimated (Table 19.1). Values as high as 6 million species have been proposed, using estimates based on the biodiversity of all insect species (LaSalle and Gauld 1993). Chalcidoidea are by far the least understood and potentially most diverse group of parasitoids.

The taxonomy of this superfamily has been hindered by their small size (1–2 mm on average) and extremely high biodiversity around the world. Estimates based on comparing tropical and temperate faunas have established a range of 375,000 to 500,000 morphologically distinct species (Noyes 2000, 2014; Heraty and Gates 2003). Paralleling the biodiversity of hymenopteran parasitoids, the most economically important groups are found in two families of Ichneumonoidea

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(Ichneumonidae and Braconidae) and four families of Chalcidoidea (Encyrtidae, Aphelinidae, Eulophidae, and Pteromalidae) (Fig. 19.1). In part, their importance for pest management is determined by their tendency to attack economically important pest groups of sessile Hemiptera (aphids, scales, and whiteflies), Lepidoptera, Coleoptera, and phytophagous Hymenoptera. More than 800 species of Chalcidoidea have been used in biological control programs and overall have had the greatest rate of establishment and success (Noyes 2014). 19.2.2 Phoridae

Phoridae are minute flies that can be scavengers, detritivores, facultative “scavengers” that attack dying or recently dead ants, or true parasitoids (Disney 1994, Feener and Brown 1997, Morehead et  al. 2001, Folgarait et  al. 2005). Of the 3657 described species, 611 are true parasitoids (B. V. Brown, personal communication). Most of the described parasitoids belong to the genera Apocephalus, Melaloncha, and Myriophora, which together might contain another 500 undescribed species (B. V. Brown, personal communication), but many of the thousands of undescribed species of the genus Megaselia might be parasitoids as well. Phoridae are an immense group, and their total biodiversity could reach 30,000– 50,000 species (Gaston 1991; B. V. Brown, personal communication). Robinson (1971) proposed that, at least in the genus Megaselia, new host records tended to favor a reduction in the overall proportion of true parasitoids in the group; however, Brown suggests that potentially half of the family might be parasitoids  –  nearly 15,000 species! Phorids are parasitic on a number of insect groups, including bees, beetles, scale insects, millipedes, and adult and pupal coccinellids, but they have the greatest importance and influence as parasitoids of adult ants. Phorids attack dead, dying, or living ants. In the latter case, their effect is not only direct mortality, but also changes in the behavior of foraging ants to protect the susceptible castes (soldiers), which comes at a high general cost to the colony: worker

foraging rates can be reduced by as much as 75% (Askew 1971, Feener and Brown 1992). At least two species of Pseudacteon have been released against the imported fire ant in the southeastern United States. Both have established and become abundant, but at least for Pseudacteon tricuspis, the flies have not yet been shown to have a significant effect on reducing fire ant populations (Morrison and Porter 2005). 19.2.3 Tachinidae

Tachinidae are predominantly parasitoids of Lepidoptera and other herbivores, including Heteroptera, Hymenoptera, and Orthoptera, but they also parasitize a wide range of other arthropods, including centipedes, scorpions, and spiders (Stireman et  al. 2006). All Tachinidae are endoparasitic, with most species attacking the larval stage and emerging from the pupa; 5–10% attack adult arthropods (Stireman et  al. 2006). Recent estimates suggest that 8200 species of Tachinidae have been described in 1530 genera (Stireman et al 2006, Cerretti et al. 2014). This total potentially represents half of the estimated species richness of Tachinidae, with most species occurring in tropical countries. Most tachinids are large and showy insects, and perhaps as much as 90% of the species in the northern hemisphere are known. However, the large biodiversity of tropical species remains practically untouched. Of 300 species sampled at one forest site in Costa Rica, 80% are undescribed (Janzen and Hallwachs 2005, Stireman et al. 2006). Tachinid flies are an important factor in the management of macrolepidopteran pests, and more than 100 species have been used in biological control programs for crop or forest pests with partial or complete success (Greathead 1986, Genier 1988). Many of the agriculturally important tachinid species share the same host species or use alternative hosts in native habitats, which then act as a parasitoid refuge (Marino et  al. 2006). Tachinids also have been used as an example of biological control at its worst. Compsilura concinnata originally was introduced for control of the gypsy moth in the

19  Parasitoid Biodiversity and Insect Pest Management

Encyrtidae 40

Total host families = 124

Aphelinidae 40

Total host families = 37

20

20

Ar Or He SA Dc

Ne Cl Dp Hy Le Ot

Ar

Eulophidae 40

Total host families = 144

Or He SA Dc Ne Cl Dp Hy Le Ot host group

host group

Pteromalidae 40

Total host families = 131

20

20

Ar Or He SA Dc Ne Cl Dp Hy Le Ot host group 60

Ar

Or He SA Dc Ne Cl Dp Hy Le Ot host group

60

Ichneumonidae

Braconidae

Total host families = 137

Total host families = 126

40

40

20

20

Ar Or He SA Dc Ne Cl Dp Hy Le Ot host group

Ar

Or He SA Dc Ne Cl Dp Hy Le Ot host group

Figure 19.1  Summary of distribution of host families by parasitoid family. Host groups: Ar, Araneae; Or, Orthoptera; He, Heteroptera; SA, Sternorrhyncha (primarily) and Auchenorrhyncha; Dc, Dictyoptera; Ne, Neuroptera; Cl, Coleoptera; Dp, Diptera; Hy, Hymenoptera; Le, Lepidoptera; Ot, other groups. Gray bars indicate host groups with the largest numbers of economically important pest groups. Redrawn with permission from Noyes and Hayat (1994).

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northeastern United States and, along with another tachinid, Blepharipa scutellata, might effect a combined mortality rate of as much as 50% on the moth. However, C. concinnata is highly polyphagous: it has subsequently been found attacking more than 200 species in dozens of families and three orders of native insects, and it is having a direct effect on native biodiversity (Boettner et al. 2000). 19.2.4  Other Groups

In the Lepidoptera, Chacoela (Pyralidae) are larval or pupal parasitoids of Polistes wasps (Hodges et al. 2003); Sthenauge (Pyralidae) feed as ectoparasites of saturniid larvae; and Epipyropidae are parasitoids of hemipteran nymphs or lepidopteran larvae (Eggleton and Belshaw 1992). Mantispidae (Neuroptera) are ectoparasitoids of larvae and pupae of Coleoptera, Lepidoptera, or Hymenoptera in soil, or of spider egg sacs (Eggleton and Belshaw 1992). Trichoptera in the genus Orthotrichia (Hydroptilidae) develop as parasitoids of pupae of Chimarra (Philopotamidae) (Wells 1992, 2005). In the Strepsiptera, Eggleton and Belshaw (1992) included only the Mengenillidae (about 10 species) as true parasitoids. The array of parasitoids in Coleoptera and Diptera is reviewed by Eggleton and Belshaw (1992), but beyond phorids and tachinids, parasitoids in these orders are comparatively uncommon, with only an estimated 1600 described species of Coleoptera parasitoids and 15,600 described species of Diptera parasitoids (Table 19.1). 19.2.5  Where Are Parasitoids Most Diverse?

A number of factors affect parasitoid biodiversity at the community level. They include characteristics of the host and its food plants, ecological complexity, successional stage of the community, plant architecture, and climate (Price 1991, 1994; Hawkins 1994; Marino et al. 2006; Crowder and Jabbour 2014). In general, agricultural landscapes lack the biodiversity and ecological complexity of natural ecosystems and support a lower overall biodiversity of parasitoids (Benton et  al. 2003,

Landis et al. 2005, Bianchi et al. 2006). Agricultural intensification, reduction of forests and hedgerows, and continuous planting schemes are all having an effect on native parasitoid and host biodiversity. In temperate agricultural systems, the surrounding vegetation is important in supporting parasitoids that attack pest species. Late successional stage vegetation most commonly supports a higher proportion of generalist species shared with agricultural systems (Landis et al 2005, Marino et al. 2006). Early successional vegetation, however, might support a higher proportion of oligophagous specialist parasitoids that are also of importance (Marino et al. 2006). The landscape surrounding agricultural monocultures is an essential resource for maintaining parasitoid abundance and biodiversity (Kruess and Tschartke 1994, Landis et  al. 2005, Bianchi et al 2006, Moradin et  al. 2014). Some studies have argued that simplified agricultural systems provide a level of control that is equal to or greater than that of complex systems (Rodríguez and Hawkins 2000, Martin et al. 2013). However, in a general survey of 15 studies comparing ecologically complex versus simple agricultural landscapes, 74% had higher natural enemy populations and 45% had lower pest pressure (Bianchi et al. 2006). 19.2.6  Leaf‐mining Parasitoids and Native Landscapes

Parasitoids of smaller gracillariid leaf‐mining Lepidoptera are a good example of the interaction between native indigenous parasitoids and leaf‐ mining pests. In southern Ontario, a survey of 38 species of gracillariids on 14 host plants produced 65 species of parasitoids, of which 63% were eulophid wasps (Fig. 19.2a). Of the 28 parasitoid species reared from apple leaf miner, Phyllonorycter blancardella (Fig. 19.2b), the overall proportion of species was similar, with most species (78%) overlapping between agricultural and native habitats. A similar composition of parasitoids attacked gracillariid leaf miners in southern California (Fig. 19.2c). The invasive citrus leaf miner has attracted more than 90 species of indigenous parasitoids worldwide, but no braconid parasites have yet

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Figure 19.2  Proportion of higher level hymenopteran parasitoids attacking (a) lepidopteran leaf miners of broadleaf plants in southern Ontario (J.H., unpublished data); (b) Phyllonorycter blancardella in an unsprayed apple orchard in Ontario (J.H., unpublished data); (c) lepidopteran leaf miners of broadleaf plants in California (Braconidae not broken out to genus and species) (Gates et al. 2002); and (d) Phyllocnistis citrella worldwide (no Ichneumonoidea parasitoids) (Schauff et al. 1998). Parts (a), (b), and (d) are based on number of species sampled; (c) is based on the number of individuals. Numbers of genera and species are in parentheses. Years refer to sampling periods.

been reported (Fig. 19.2d). In Florida, native parasites of eight genera of Eulophidae parasitized more than 50% of citrus leaf miner larvae in the first few years of the latter’s establishment (Peña et al. 1996, 2000). In southern California, several indigenous species have already shifted to citrus leaf miner since it arrived in 2000, including some, such as Closterocerus utahensis (Eulophidae), that were only rarely encountered prior to the invasion of the leaf miner (Heraty unpublished). Four gen-

era of Eulophidae (Cirrospilus, Pnigalio, Sympiesis, and Zagrammosoma) are common in each of the leaf miner systems (Fig. 19.2). Species in these genera are generalist, idiobiont parasitoids that attack a wide variety of hosts including leaf‐mining Agromyzidae and other parasitic Hymenoptera as hyperparasites. Similar to a study focused on macrolepidopteran pests of agricultural crops (Marino et al. 2006), late s­ uccessional vegetation (trees and shrubs) was correlated with the greatest species

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richness and numerical abundance of generalist parasitoids and is, therefore, a potentially beneficial resource for control of pest populations. As well as providing a parasitoid refuge, hedgerows and native ecosystems provide a source of flowers, nectar, and other factors that can help enhance both the numbers and species richness of parasitoids (Corbett and Rosenheim 1996, Bostanian et al. 2004, Lavandero et al. 2006, Rezende et al. 2014). With agricultural intensification, we need to consider planning for diverse landscapes that promote parasitoid biodiversity (Landis et al. 2005, Bianchi et al. 2006, Bennett and Gratton 2012). 19.2.7  Are Parasitoids More Diverse in Tropical Versus Temperate Climates?

When we consider parasitoid communities in agricultural landscapes, do we need to modify our expectations based on latitudinal gradients? Should we expect higher biodiversity in equatorial ecosystems? The biodiversity of Tachinidae increases dramatically toward the equator, with a forest site in Costa Rica yielding more than 300 species, of which 80% were undescribed (Stireman et  al. 2006). Phoridae are extremely diverse in both temperate and tropical latitudes, although there is a change in composition of taxa and a greater proportion of parasitoid taxa in tropical regions. Small parasitic Hymenoptera and egg parasitoids increase in diversity in tropical regions (Hespenheide 1979, Noyes 1989). Increased biodiversity, for the most part, is correlated with a higher proportion of host taxa. However, the Ichneumonidae either lack the distinct latitudinal gradient (Janzen 1981) or even decline in diversity toward the tropics (Owen and Owen 1974, Gaston et al. 1996). Both the Ichneumonidae and Tachinidae attack similar hosts, but the Tachinidae are less susceptible to the chemical defenses accumulated by the larval hosts, and the “nasty host hypothesis” has been used to explain the ichneumonid anomaly (Gauld et al. 1992, Hawkins et al. 1992, Sime and Brower 1998). A number of issues surround these trends in biodiversity, and in the Ichneumonidae, different subfamilies may have opposite relationships between biodiversity and

latitudinal gradients (Gaston et  al. 1996). These patterns of latitudinal diversity gradients may also be an error based on the poor taxonomic knowledge of tropical parasitoids, especially in the Ichneumonoidea (Jones et al. 2012, Quicke 2012). Overall, parasitoids are shown to increase in biodiversity toward the tropics. The influence of greater parasitoid biodiversity should transfer to agroecosystems where habitat biodiversity is left intact. In Cacao plantations in Brazil, parasitoid biodiversity can be both abundant and diverse, and similar in complexity to that in native forests (Sperber et al. 2004). Does increased control in agricultural landscapes correlate with increased parasitoid diversity as we approach the tropics? Hawkins et al. (1992) found no significant correlation between parasitoid richness in agricultural hosts and latitudinal variability, although koinobionts had greater richness in northern North America. However, this finding does not address the control of hosts in the same context. In the leaf‐ miner example (Fig. 19.2), parasitoid diversity is higher for native leaf miners in California (USA) and the citrus leaf miner (which has a general tropical distribution) than for apple leaf miners and a more northern leaf‐miner landscape in Ontario (Canada). Both insects remain pests in their respective systems, although parasitoids can usually effect control below an economically important threshold in mature orchards.

19.3 ­Systematics, Parasitoids, and Pest Management The importance of valid identification of both pest and parasitoid for successful establishment and cost savings in biological control programs has been discussed numerous times in the literature (Compere 1969, Rosen and DeBach 1973, Heraty 1998, Schauff and LaSalle 1998). Cassava mealybug was a major pest in Africa and threatened this major food source across the continent. Because of an initial misidentification, foreign exploration efforts were misdirected to the wrong host in northern South America, and parasitoids

19  Parasitoid Biodiversity and Insect Pest Management

i­ntroduced from these efforts did not accept the African host. The correct host species, Phenacoccus manihoti, was known to occur only in southern South America. After correct identification by taxonomists, refocused collection efforts resulted in the establishment of a single parasite species, Apoanagyrus lopezi (Encyrtidae), and long‐term control of the pest (Neuenschwander 2001). Control of Florida red scale on citrus was delayed because of misidentification of the parasite, Aphytis lingnanensis (Aphelindae), attacking California red scale; the correct parasite, Aphytis holoxanthus, which occurs in Israel and Hong Kong, was imported to Florida and economically important levels of control were achieved (Clausen 1978). Augmentative control by Trichogramma egg parasitoids is often stymied by a lack of proper identification of the correct species collected, reared, or released (Stouthamer et al. 2000b). Currently, most of our pest management decisions, including choice of biological control agents, are based on a morphological understanding of species. The involvement of taxonomists early in a project can solve some of these problems, but even if expertise is available, the taxon of interest might be poorly surveyed or inherently difficult to identify (Schauff and LaSalle 1998). Beyond identification, systematics is focused on the collection, databasing, and maintenance of parasitoid collections from all habitats (museum‐based studies), and phylogenetic studies are gaining importance for understanding host relationships and the evolution of behavior and other traits of interest (Gauld 1986; Heraty 1998, 2004, Munro et  al. 2011, Heraty et  al. 2013). By merging research from museum collections and the literature, two important databases, we can now incorporate a vast amount of data on nomenclature, geographic distribution, biology, and host relationships for Ichneumonoidea (Yu et al. 2004), and Chalcidoidea (Noyes 2014). The ichneumonoid database includes information on more than 63,000 taxonomic names and 28,000 literature citations. The chalcidoid database has information on more than 31,000 taxonomic names and

incorporates more than 40,000 literature citations. These databases provide a good start toward understanding what we know about the biodiversity of parasitoids, host associations, and their potential effects in natural and agricultural ecosystems. 19.3.1  Molecules and Parasitoid Biodiversity

Molecular methods offer a new ability to identify species, albeit not without some of the same caveats for morphological discrimination. A variety of molecular markers are available for diagnosing all levels of divergence in insect parasitoids (Unruh and Woolley 1999, Heraty 2004, Macdonald and Loxdale 2004). Comparative nucleotide sequences are currently the most common choice for species recognition, identification, and phylogenetic analysis. For both hosts and parasites, various nuclear and mitochondrial ribosomal transcript regions and protein‐coding genes have been used to identify and discriminate insect populations. For species‐level discrimination, these have usually involved comparisons of nuclear 28S ribosomal DNA (rDNA) transcripts and the associated internal transcribed spacer regions (ITS1 and ITS2) and mitochondrial cytochrome c oxidase subunit I (COI), COII, 16S rDNA, and 12S rDNA. The ribosomal transcript regions (28S, 16S, and 12S) are conserved and considered appropriate for comparisons from the subfamily to the species level, whereas the ITS regions and COI and COII are more variable, offering information from the population or species level and above (Heraty 2004). Because of rapid divergence and changes in sequence length, ITS regions rarely can be aligned for taxa beyond closely related species. All of these gene regions occur in numerous identical copies in the genome, making their extraction and amplification relatively trivial, even for poorly preserved insect samples. Additional single‐copy nuclear genes being explored among parasitoids include elongation factor 1alpha (EF1alpha) (Rokas et  al. 2002), phosphoenolpyruvate carboxykin-

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ase (PEPCK), DOPA decarboxylase (DDC), arginine kinase (ARGK), long‐wavelength sensitive opsin (LOP), and wingless (WNT) ­ (Rokas et al. 2002; Desjardins et al. 2007; Heraty et al. 2007; R. Burks, personal communication). Although these single‐copy genes are important for phylogenetic purposes, they are more difficult to obtain and are not likely to be used as extensively as 28S, ITS, and COI for purposes of species recognition. Rapid advances are being made in the gathering of data from whole‐ genome sequencing and annotation (cf. Werren et  al. 2010 for Nasonia vitripennis), transcriptomes, and targeted enrichment methods (i.e., Lemmon et  al. 2013). These techniques will make standard the use of genomic data sets with hundreds to thousands of gene loci for comparison at all levels of analysis. Molecular methods will have an increasing influence on research into agricultural pests, identification of pests and parasitoids, and surveys of biodiversity at the pest‐management level. The use of molecular markers may be essential for the discovery of cryptic species complexes in parasitoids (Mottern and Heraty 2014a). There is also a drive to develop a standardized method of barcoding in all insects, not only for the recognition of existing species, but also for the discovery of new, even morphologically distinct species. Important questions can be addressed with these new tools. What species are shared between agricultural and native habitats? How far do parasitoids disperse between habitats? Do cryptic species interfere with or complement each other in pest management? Do cryptic species fare better in different climatic zones? Am I releasing the correct species? These are all questions that directly affect our ability to monitor parasitoids and control insect pests in urban, agricultural, and native landscapes. However, these tools are being applied against the tremendous background noise of undescribed taxa and the associated geographic variability. The discovery of cryptic species and identification, using molecular tools, will have a tremendous effect on our ability to use and manipulate insect parasitoids.

19.3.2  Cryptic Species

Cryptic species are morphologically similar but reproductively isolated populations that can differ in important physiological, ecological, or behavioral traits. Numerous cryptic species have been recognized over the past few decades through better discrimination of populations using molecular techniques. In the past, these species have been discovered through differences in behavior, reproductive incompatibility (Heraty et  al. 2007), or isozyme or random amplification of polymorphic DNA (RAPD) marker differences (Unruh et  al. 1989, Antolin et al. 1996, Heraty 2004). Two cryptic species of phasiine tachinids were discovered by their attraction to different host pheromones (Aldrich and Zary 2002). However, the direct comparison of nucleotide sequences has led to even greater discovery of cryptic species complexes in a variety of parasitoids. COI was useful in discriminating 17 morphospecies of Belvosia tachinid flies, as well as discovering an additional 15 cryptic species among them (Smith et al. 2006). Cryptic species in the Cotesia melitaearum complex (Braconidae) associated with different host butterflies were recognized by as little as 1.6% divergence in COI and microsatellites (Kankare et  al. 2005a, 2005b). Cryptic species of Nasonia (Pteromalidae) were distinguished with rDNA sequences (ITS2 and 28S‐D2) (Campbell et  al. 1993). Morphologically indistinct species of Encarsia (Aphelinidae) can be separated using mitochondrial (COI) or nuclear (28S or ITS) gene regions (Babcock and Heraty 2000, Babcock et al. 2001, Polaszek et  al. 2004, Monti et  al. 2005). Monti et  al. (2005) used a COI‐sequence divergence of 10% to separate morphologically indistinguishable Pakistani and Spanish populations of Encarsia sophia that differ in reproductive compatibility and karyotype; similar morphologically distinct species of Encarsia differ by as little as 6.5–8.7%. Trichogramma minutum and Trichogramma platneri (Trichogrammatidae) can be distinguished only by a single fixed COI substitution (Stouthamer et al. 1998, 2000a). Combinations of gene regions might be necessary to differentiate species. Sympatric, cryptic

19  Parasitoid Biodiversity and Insect Pest Management

species of Gonatocerus (Mymaridae) were recognized using a combination of 28S‐D2, COI, COII, ITS1, and ITS2, with all but 28S being highly variable within reproductively compatible populations (Triapitsyn et al. 2006). The relationships and identity of six reproductively isolated species in the Aphelinus varipes complex (Aphelinidae) could be recognized only through a combination of six gene regions (28S, ITS1, ITS2, COI, COII, and ArgK) (Fig.  19.3; Heraty et  al. 2007). The

genetic differences between cryptic species are often minute, but in Cales noacki (Chalcidoidea), a parasite of woolly whitefly, cryptic species have been discovered that differ by enough base pairs (3% for 28S and 17% for COI) that they could be considered distinct genera or even subfamilies, compared with other Chalcidoidea (Mottern and Heraty 2014a, b). The effect of the discovery of cryptic species complexes on our estimates of the biodiversity of

A. kurdumovi (R. padi / Georgia) A. kurdumovi (R. padi / Georgia) A. hordei (D. noxia / France) Zhu et al. 2000 (Palaearctic/South Africa; ITS2) A. atriplicis (D. noxia / Georgia) A. atriplicis (D. noxia / Georgia) A. varipes (R. padi / France) encounter

A. albipodis (R. padi / Israel) Wu et al. 2004 (Wyoming, USA; ITS1) A. certus (A. glycines / China) A. certus (A. glycines / China) 28S-D2 ITS1 ITS2 COI COII ArgK indels

acceptance

5 changes

A. certus (A. glycines / Japan) A. certus (A. glycines / Japan) A. certus (A. glycines / Japan) A. certus (A. glycines / Japan) A. certus (A. glycines / Korea) A. certus (A. glycines / Korea) Wu et al. 2004 (Japan; ITS1)

Figure 19.3  Problems of barcoding using only cytochrome c oxidase subunit I (COI). Presented is a phylogram for distinct genotypes from different geographic populations of cryptic species in the Aphelinus varipes complex, with their source aphid host, geographic locality of collection, and whether they are reproductively compatible (gray line) or reproductively incompatible (dashed line) (Heraty et al. 2007). The phylogeny is based on six genes and insertion/ deletion events, and includes three populations (bold) from published partial sequences as indicated. COI changes are indicated with black bars (unique changes) and gray bars (homoplastic changes). COI changes are not correlated across the phylogeny with reproductive incompatibility, which supports a minimum of five species. The three previously published populations would not be correctly associated or discriminated using COI alone. The populations from Zhu et al. (2000) and Israel were not tested for compatibility. Populations tested by Wu et al. (2004) and the Georgia (Diuraphis noxia), China, and Japan populations tested by Heraty et al. (2007) were partially compatible with each other based on hybrid dysgenesis in backcrosses to Japan. In all cases, males will pursue and court heterospecific females, but females reject heterospecific males before mating (K. Hopper, unpublished data). Photographs courtesy of Keith Hopper.

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insect parasitoids is staggering. The above examples of cryptic species complexes involve the chalcidoid families Mymaridae (1424 species), Aphelinidae (1160 species), and Pteromalidae (3506 species) (species numbers from Noyes 2014). Surveys of tropical rainforest canopies already have suggested a much greater biodiversity of morphological species, with samples in Sulawesi yielding as many as 150 morphologically distinct species of mostly undescribed species of Encarsia (Noyes 1989). Even under the most conservative schemes, we might have to double or triple our estimates of extant species in all parasitoid taxa currently recognized by morphological criteria (Table 19.1). 19.3.3  DNA Barcoding and Biodiversity of Parasitoids

Considerable discussion has occurred over the use of molecular methods to barcode species for easier recognition (Cameron et  al. 2006, Goldstein and DeSalle 2011). Sequencing is becoming cheaper and more reliable, and the taxonomist shortage might be circumvented by comparing sequences to those obtained from known vouchers of identified species (Wheeler et  al. 2004). Genetic markers such as 28S‐D2, ITS, and COI are most appropriate for the recognition of insect species or populations. Trichogramma species are minute and difficult to identify based on features of the genitalia, but identification keys to species can be built using differences in ITS length and sequence divergence (Ciociola et  al. 2001, Pinto et  al. 2002). These markers are not only useful for the identification of known species or populations by non‐specialists, but also can be used in studies of larval parasitism. Typically, the dissection or rearing of hosts to assess internal parasites is laborious. COI and ITS markers can be used to discriminate between the host and its parasitoids in both laboratory trials and field‐collected hosts (Tilmon et al. 2000, Zhu et al. 2000, Zhu and Williams 2002, Ashfaq et  al. 2004, Agusti et  al. 2005, MacDonald and Loxdale 2004, Greenstone 2006, Rougerie et al. 2011).

The ease of DNA sequencing and utility of markers for species identification is developing into a movement to barcode numerous individuals of vouchered material for use in the general identification of all species and for the discovery of new species (Hebert et  al. 2003, Hajibabaei et  al. 2005). Agriculturally important pests or parasitoids are strong candidates for a barcoding initiative. The species involved are generally known and could be sampled for a number of genes across their entire geographic ranges. These markers would be useful for identification of pests at quarantine points; verification of natural enemies for importation, culture and release from quarantine; and post‐release tracking of parasitoids. Barcoding can and does work efficiently in some cases, but there are a number of problems. Genetic variation within and between populations makes it difficult to assess the level of species discrimination and association (Meier et al. 2006), and considerable difference in the rates of variation between taxa might make it difficult to choose a single appropriate gene (Heraty 2004). The problem is exacerbated with the inclusion of unknown species. Further, the choice of gene, number of genes chosen, number of taxa sampled over a geographical range, representation of taxa in current databases, and mistakes inherent in existing sequences in databases all cause further problems (Cameron et  al. 2006, Hickerson et  al. 2006, Meier et al. 2006). Among parasitoids, genetic divergence within a single gene region may or may not correspond with reproductive compatibility. Two morphologically cryptic species of Trichogramma were separated by two fixed‐substitution differences in COI, but not by the usually more variable ITS2 region (Stouthamer et al. 2000a; Pinto et al. 2002; R. Stouthamer, personal communication). Similarly, COI has proved useful for separating cryptic species of Encarsia (Monti et  al. 2005). Within the A. varipes species complex (Aphelinidae), six gene regions and their insertion/deletion events were necessary to discriminate and determine relationships among the different populations (Heraty et  al. 2007).

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Although the most basal and genetically divergent lineages were reproductively isolated from all others, in the more derived lineages, the eastern Palearctic populations were all reproductively isolated from each other, whereas the Asian populations were not (Fig. 19.3). COI changes in the A. varipes complex are sparse and scattered and do not have a direct correlation with isolation. They would not be useful in placing populations previously cited in the literature that (i) do not have any COI information available, and (ii) could not be separated from other lineages if only COI sequences were available for comparison (Fig. 19.3). COI variation can have no bearing on reproductive isolation. In Megastigmus transvaalensis, a seed parasite of various species of Rhus and Schinus in Africa, 29 haplotypes were found for COI that were distinct enough to provide bootstrap support correlated with the different countries of origin (Scheffer and Grissell 2003). In Gonatocerus ashmeadi, a parasitoid of the glassy‐winged sharpshooter, reproductively compatible populations were fixed for 28S‐D2, but highly variable for COI (nine substitutions) and ITS2 (19 substitutions) (Triapitsyn et  al. 2006). By contrast, morphologically distinct and geographically isolated species of Pnigalio (Eulophidae) are identical for 28S‐D2, but COI readily distinguishes both morphologically distinct and cryptic ­species (M. Gebiola, personal communication). Admittedly, these problems of associating molecular divergence of COI with speciation are most problematic for discriminating recently evolved species. However, any barcoding initiative will have to deal with the problems of intraspecific variation, which can be excessive in some species. Molecular sequences can be used to discriminate distinctive or cryptic species, even with a single gene region, but often these findings can be verified only in conjunction with traditional methods of observing morphological divergence, behavioral distinctness, geographic separation, and studies of reproductive compatibility. With non‐destructive PCR extraction methods, each specimen in a given research project conceivably might be vouchered by DNA

sequences (GenBank deposition) and digital images (MorphBank deposition), with all information freely available through online databases. As these data accumulate, perhaps we can better evaluate the use of barcoding tools and also our general interpretation of speciation processes and boundaries. 19.3.4  Can Molecular Markers Be Applied to Understanding Biodiversity?

Parasitoids are extremely diverse. At our best guess, there are at least 680,000 morphologically distinct species (Table 19.1). If we begin to revise our estimate to include the vast number of cryptic species that also remain to be discovered, we must assume that even with a low estimate, there are easily more than a million species. Documenting molecular markers for species on a grand scale will be costly, requiring samples of multiple markers, multiple individuals, and multiple populations (Meier et al. 2006). Molecular sequences can be used to discriminate distinctive or cryptic species, even with a single gene region, but often these findings can be verified only in conjunction with traditional methods of observing morphological divergence, behavioral distinctness, geographic separation, and studies of reproductive compatibility.

19.4 ­Summary More than 680,000 morphologically distinct species of parasitoids are estimated, with the possibility of a vast underlying biodiversity of cryptic species. Most of these species are unknown to science. Molecular tools will be important in the recognition and tracking of species, especially of these new cryptic species, but as with other methods, they are merely a tool to be used along with more traditional methods of morphological systematics, behavioral and host studies, and community relationships. Parasitoids are more diverse in ecologically complex systems than in simple

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landscapes. Generalist parasitoids may be more common in late‐succession communities (trees and shrubs), compared with oligophagous species, which dominate in early‐succession communities (ruderals and shrubs). Latitudinal gradients affect parasitoid biodiversity, generally with increasing biodiversity toward the tropics; however, within each group, there are shifts or distinctly different trends with the members of a group, such as in different subfamilies of Ichneumonidae that can be differentiated onto different host groups. Biological control has demonstrated that many pests can be controlled by one or more introduced parasitoids. There is still controversy over continuing to increase parasitoid biodiversity against these pests over and above the previously established species, especially if they are already providing control below economic thresholds. However, studies of natural and adjacent agricultural systems suggest that an increased biodiversity of parasitoids is important for controlling pests (Bianchi et al. 2006, Marino et al. 2006, Crowder and Jabbour 2014). Agriculture is usually synonymous with monoculture. Ecologically diverse native vegetation is suffering under agricultural intensification and potentially reducing the pool of available parasitoids that are available for control of newly introduced or resident pest species. To support conservation in association with agricultural practices, we need more research on the shared pool of parasitoid biodiversity. Many pest species have come from a different country, arriving without their parasitoids. However, if a general habitat decline is associated with habitat loss, we might see an increasing number of pests developing in their native area of origin. Biological control programs of the past may give us insights into strategies necessary to deal with these emergent pests. In addition, we are entering a new age of transgenics in crops, and the impact of this on crops and pests and the associated effects on parasitoids are far from being understood (Davidson et  al. 2006, White and Andow 2005, Beale et al. 2006).

­Acknowledgments I would like to thank Bob Foottit, Peter Adler, Peter Mason, Jason Mottern, and an anonymous reviewer for comments on the manuscript, and Brian Brown for information on phorid flies. This work was supported, in part, by US National Science Foundation grant DEB‐1257733.

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White, J. A. and D. A. Andow. 2005. Host‐ parasitoid interactions in a transgenic landscape: spatial proximity effects of host density. Environmental Entomology 34: 1493–1500. Wiegmann, B. M., C. Mitter and B. Farrell. 1993. Diversification of carnivorous parasitic insects – extraordinary radiation or specialized dead‐end. American Naturalist 142: 737–754. Wu, Z. S., K. R. Hopper, R. J. O’Neil, D. J. Voegtlin, D. R. Prokrym and G. E. Heimpel. 2004. Reproductive compatibility and genetic variation between two strains of Aphelinus albipodus (Hymenoptera: Aphelinidae), a parasitoid of the soybean aphid, Aphis glycines (Homoptera: Aphididae). Biological Control 31: 311–319. Yu, D. S., K. van Achterberg and K. Horstmann. 2004. World Ichneumonoidea 2004, Taxonomy, biology, morphology and distribution. Taxapad. Privately published by Dr D. S. Yu. Available at www.taxapad.com [Accessed 8 September 2014]. Zhu, Y. C., J. D. Burd, N. C. Elliott and M. H. Greenstone. 2000. Specific ribosomal DNA marker for early polymerase chain reaction detection of Aphelinus hordei (Hymenoptera: Aphelinidae) and Aphidius colemani (Hymenoptera: Aphidiidae) from Diuraphis noxia (Homoptera: Aphididae). Annals of the Entomological Society of America 93: 486–491. Zhu, Y. C. and L. Williams III. 2002. Detecting the egg parasitoid Anaphes iole (Hymenoptera: Mymaridae) in tarnished plant bug (Heteroptera: Miridae) eggs by using a molecular approach. Annals of the Entomological Society of America 95: 359–365.

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20 The Taxonomy of Crop Pests: The Aphids Gary L. Miller1 and Robert G. Foottit2 1 2

Systematic Entomology Laboratory, Plant Science Institute, Agricultural Research Service, US Department of Agriculture, Beltsville, Maryland, USA Canadian National Collection of Insects, Arachnids and Nematodes, Agriculture and Agri‐Food Canada, Ottawa, Ontario, Canada

For the most part, the most economically important insect and mite pests are known to science, and their position in our classification system is resolved. (Anonymous, US Department of Agriculture, ARS Research Action Plan, 2004) There is a perception that certain insect pests of crops are well‐studied biologically and that their taxonomy is in good order. This perception might lead to the impression by those who are unfamiliar with the intricacies of acquiring taxonomic understanding of biological diversity that we know all there is to know. In fact, science is a discipline that is continually building on its previous discoveries and technologies as it advances our knowledge. Much research is needed even in economically important insect groups whose taxonomy might be regarded as advanced. In this chapter, using the Aphidoidea as an example and in particular using early works of North American aphidology as background, we explore various dimensions of taxonomic knowledge in this pest group.

20.1 ­Historical Background Plants have been cultivated and traded since perhaps 8000 bc (Huxley 1978), and insect pests

have long plagued humans and their crops. Ancient civilizations recorded swarms of locusts and other insect pestilence (Harpaz 1973, Konishi and Ito 1973). As humans expanded crop cultivation, associated insect problems soon followed. The European colonists of the New World faced their own set of insect‐related problems with the cultivation of both native and introduced crops. For example, tobacco, which is native to the New World, experienced insect damage from hornworms and flea‐beetles from the outset of its cultivation (Garner 1946). The introduction of new plants also began early during European colonization. Sugarcane was transported from the Canary Islands to Hispaniola on Columbus’s second voyage in 1493 (Deerr 1949). Some of those early introduced plants also had their associated pests, including aphids. The close association of aphids with their hosts meant those insects and their eggs were being transported through commerce as well (Howard 1898). The cabbage aphid, Brevicoryne brassicae (Linnaeus), was noted in North America as early as 1791 (Miller et al. 2006). Early entomologists were well aware that commerce and travel were responsible for the transport of some of these pests. In 1856, Asa Fitch speculated that B. brassicae was brought along with cabbage plants on shipboard cargo (Miller et al. 2006).

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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20.2 ­Economic Importance and Early Taxonomy Aphids are small, soft‐bodied insects mostly ranging between 1.5 and 3.5 mm in length (Backman and Eastop 2000); they use piercing‐ sucking mouthparts to feed on plants. In addition to causing mechanical damage by this action, aphids serve as the largest group of vectors of plant viruses (Eastop 1977, Chan et  al. 1991). The damage is further compounded by fouling of the host plant with honeydew. Noted as long ago as in Réaumur’s (1737) work, honeydew is excreted from the anus and is high in plant sugars and other compounds. Besides having an influence on predators (Glen 1973) and parasitoids (Faria 2005), it serves as a substrate for the growth of fungal complexes that cause sooty mold (Baker et al. 2002). In addition to reducing the photosynthetic ability of plants, sooty mold reduces a plant’s aesthetic market value (Worf et al. 1995). More than 250 species of the Aphidoidea (in the families Adelgidae, Phylloxeridae, and Aphididae) feed on agricultural or horticultural crops (Blackman and Eastop 2000). Although this figure only represents approximately 5% of the world aphid fauna, the economic consequences of aphid damage are huge. For example, Wellings et al. (1989) estimated that aphids contribute about 2% of the total losses attributed to insects for 13 selected crops, and they thought that figure was a gross underestimate. Aphids are one of the most important vegetable pests (Capinera 2002). Of the 80 groups of vascular plants in the world, only eight lack aphids, and they represent only 3% of the plant species (Eastop 1978). Most aphid references refer to economic impact, and some of the very earliest works of the 16th and 17th centuries have been noted by Blackman and Eastop (2000). Although aphids are extraordinarily damaging to horticulture, some of society’s early interest in these insects

involved their beneficial or positive attributes. Galls of some aphid species (e.g., Baizongia pistaciae (Linnaeus) and Schlechtendalia chinensis (Bell)) have been used in medicine, tanning, and dyeing for centuries (Fagan 1918). Woodcuts as early as 1570 illustrate galls of B. pistaciae on Pistacia (Blackman and Eastop 1994), and by 1596, “Chinese galls” of S. chinensis on Rhus javanica (a sumac) were noted as insect induced (Eastop 1979). Prior to Linnaeus’s (1758) work, many of the papers concerning aphids had little taxonomic value. One notable exception is Réaumur’s (1737) Mémoires pour servir à l’histoire des insectes. This work included information on aphid life history and biology as well as detailed illustrations. Linnaeus (1758) used Réaumur’s (1737) work as a reference in connection with a number of the species he named. The nominal species, Aphis sambuci Linnaeus (1758), is illustrated in habitus and in several detailed figures on one of Réaumur’s (1737) plates (Fig. 20.1a). For aphids (sensu lato), Linnaeus (1758) described one genus (Aphis) and 25 species, as well as the genus Chermes, which contained one adelgid species.

20.3 ­Early Aphid Studies – A North American Example Some of the earliest, if not the earliest, systematic work on North American aphids was that of Rafinesque1 (1817, 1818), who described 36 species and four subgenera. Rafinesque’s (1817) interest and intent “to study all the species of this genus [Aphis] found in the United States” was initiated by his observations that they were “often highly injurious” to their host plants. Other early North American workers often 1  Hottes (1963) proposed to suppress Rafinesque’s aphid names, and subsequent workers (e.g., Remaudière and Remaudière 1997) have recorded his names as unavailable.

20  The Taxonomy of Crop Pests: The Aphids (a)

(b)

Macrosiphum rosae (L.)

Aphis sambuci L.

Figure 20.1  (a) Some of the early aphid work produced by Réaumur (1737) included his woodcuts, which were used for identification. Linnaeus (1758) referenced both of the aphid species shown here in his work. Figures 1–4 depict Aphis rosae (= Macrosiphum rosae), and figures 5–15 depict Aphis sambuci. (b) Nearly three centuries later, taxonomists are categorizing M. rosae and A. sambuci with DNA barcodes – short DNA sequences taken from a uniform locality of the genome.

treated the economic importance of aphids. For example, Harris’s (1841) report on insects injurious to vegetation includes sections on “plant‐ lice.” Although little taxonomic information

was included, Harris did incorporate observations on life history, biology, predators, host plants, and control. Fitch’s work (e.g., Fitch 1851) in the mid‐1800s not only included life history information on aphids, but also new species descriptions. Between 1851 and 1872, Fitch proposed names for 58 species of Aphidoidea (Barnes 1988). Walsh’s (1863) treatment of the Aphididae (sensu lato) included his “Synoptical Table of U. S. Genera,” which was essentially a key. By the 1870s to 1880s, entomologists such as Thomas (1877), Monell (1879), and Oestlund (1886) were specializing in the study of aphids. Difficulty in distinguishing aphids was noted as early as Linnaeus (Walsh 1863), and early workers in North America also lamented the lack of study and knowledge of the aphids. Walsh (1863), in Illinois, complained about the need for “Public Scientific Libraries” that his more fortunate “Eastern brethren” had. He added that the “specific distinctions” of the aphids themselves were “generally evanescent in the dried specimen.” Thomas (1879) reiterated Walsh’s comments and thought that the reasons for the neglected study of aphids rested on two issues: the difficulty in preserving specimens and the paucity of systematic works, most of which were European. With delays of months to years to procure a reference work (Oestlund 1886), the situation for some was daunting. In 1886, Oestlund still considered the systematics of the aphids “unsatisfactory,” but regarded the lack of literature as the greatest want for the “frontier naturalist.” Later, Oestlund’s (1919) tone changed when his concern focused on the then‐recent aphid classification difficulties “on account of the great number of new genera and species made known.” It is noteworthy that Oestlund (1886) did not mention any difficulty with preserving specimens among his concerns. By the 1860s, North Americans, along with their European counterparts, were making progress in preserving pinned insect specimens in cabinets (Sorensen 1995). Instead of being pinned or glued on small boards, aphids were routinely preserved on microscope

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slides2. Changes in the way aphids were being studied and preserved were accompanied by changes and improvements in species descriptions and tools for identification. The earliest North American aphid descriptions (e.g., Rafinesque 1817, 1818; Haldeman 1844) were based almost entirely on coloration, general appearance, and host association. Subsequent workers (e.g., Walsh 1863, Riley 1879, Miller et al. 2006) relied on descriptions of general appearance but also routinely included body length and wing‐ length measurements in their species descriptions. Walsh’s (1863) generic descriptions added comparisons to other morphological structures (e.g., relative length of siphunculi in comparison to tarsal length), a practice that was uncommon at the time. By the late 1880s, a new dimension was added to descriptions of aphid morphology. Relative descriptors of antennal segment length, such as “about half as long as the preceding” (e.g., Monell 1879) or “subequal” (e.g., Oestlund 1886), were being replaced with discrete measurements in hundredths of a millimeter (e.g., Oestlund 1887). These changes corresponded with major advances that were being made in microscopy, especially the development and design of microscope objectives and lenses that maximized both magnification and resolution.

2  Pergande’s ledger and card file at the US Aphidoidea Collection, Beltsville, Maryland, provides an excellent record of the progression of preserved aphid specimens. His earliest ledger entries, while he was in St Louis, Missouri (1877), record collected aphid specimens as being pinned, mounted on boards, or preserved in alcohol. By 1878 in Washington, DC, he noted aphids as being “mounted in balsam” and preserved in alcohol. Other aphidologists were also using balsam-mounted specimens, as Pergande noted the receipt of “Pemphigus aceris n. sp.” from aphidologist Monell that were “mounted on slide” in 1878. At the US National Museum of Natural History, Pergande was evidently still gluing specimens to pieces of board as late as 1880, but he also “mounted some on a slide.” In 1903, Pergande recorded that he examined “the old Fitch collection of Aphides” for Aphis mali Fitch, which were “pinned” and then “mounted all of them in balsam.” Slide mounting had indeed become a standard way to study and preserve the aphids by the turn of the century.

Other changes were taking place in aphid taxonomy in North America. Earliest works reflected Linnaeus’s (1758) simple classification (e.g., Haldemann 1844). The list of aphid species referable to Linnaeus’s single genus, Aphis, was being expanded. The taxonomic works of European aphidologists such as Kaltenbach (1843), Koch (1854), Passerini (1860), and Buckton (1876) influenced the early taxonomic studies of the North American workers (Walsh 1863; Thomas 1877, 1878, 1879). Although these works included keys to genera and tribes, species treatments consisted of simple descriptions and lists. Monell’s (1879) contribution is worth mentioning because he also developed identification keys for related species of select genera. The use of species keys advanced the ability to identify aphids. Oestlund’s (1887) study of Minnesota aphids provided detailed keys to subfamilies, genera, and species of select genera. In what was a synthesis of the knowledge of North American aphids, he also included detailed species descriptions, an up‐to‐date literature review of North American authors, and a host plant list. It was also a reflection of the fruits of government‐sponsored entomology at that time (Sorensen 1995). Of the 65 publications listed in Oestlund’s (1887) aphid bibliography, nearly 75% of the works reflect this government‐sponsored or government‐­ associated entomology. A major work published at the beginning of the 20th century, Hunter’s (1901) catalog The Aphididae of North America, provided much of  the pertinent literature on and taxonomy of North American aphids. Various authors had published lists of described species, and Hunter (1901) not only contributed an expanded species list but also included the known systematic and economic literature referable to the species, along with host plant information. Knowledge of North American aphid species had grown from 36 species proposed by Rafinesque (1817, 1818) to 166 species identified by Monell (1879), an increase of nearly five times. In the early 20th century, Hunter (1901) identified 325 species, an increase of more than nine times in less than a

20  The Taxonomy of Crop Pests: The Aphids

century. The compilation of the North American aphid fauna would continue to grow to 1416 species (Foottit et al. 2006).

species status could be given to a biologically recognizable anholocyclic group derived from a sexual ancestor (Blackman and Brown 1991, Foottit 1997, Havill and Foottit 2007). One way to observe trends in aphid systematics is to compare the rates of synonymy and the accumulation of new taxa: as more research is done, more species are described, and new synonymies are discovered (Fig. 20.2). From Linnaeus (1758) until 1840, the number of described, valid aphid species (sensu lato) and cumulative aphid names was only 109, and the difference between the two parameters remained relatively small. Starting around 1841, shortly before Kaltenbach’s (1843) work, the difference between the number of cumulative aphid names and cumulative valid names over time began to increase, albeit gradually, until about the late 1910s. The number of valid species increased nearly eightfold from 129 to 1011 species between 1841 and 1919. Between 1840 and 1949, there were nearly twice as many

20.4 ­Recognizing Aphid Species As the number of recognized aphid species has grown since Linnaeus (1758) (Fig. 20.2), there have been difficulties in recognizing or even defining an aphid species (e.g., Shaposhnikov 1987). The conceptual and operational use of species concepts and definitions in aphid taxonomy throughout the world is complicated by their reproductive biology. Aphids are characterized by cyclical parthenogenesis, but there may also be purely anholocyclic populations that do not manifest the sexual phase of the life cycle. Recommendations have been made for the taxonomic treatment of aphid populations that are permanently parthenogenetic; formal

cumulative number proposed names cumulative number of currently valid species

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Figure 20.2  (Insert) Cumulative aphid names proposed versus cumulative currently valid aphid names from 1758 to 2015. (Main) Number of proposed aphid names versus valid aphid names from 1758 to 2000.

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proposed names as valid names (3891 versus 2000). During the 20th century, a steady and dramatic rise in both cumulative and valid names was realized, with the exception of the period of the Second World War. From 1920 to the present, the number of valid aphid names increased from 1026 to 5385, a fivefold increase. Activities slowed over the last several decades of the 20th century and in the early 21st century. From 1950 to 2000 there were 1.3 times the number of proposed names versus valid names (3495 vs. 2721) (Fig. 20.2). This trend might reflect a slowing of activity, but it could also reflect a lack of opportunity to reassess previous work. Taxonomic study continues on the Aphidoidea with the description of new species as well as the reassessment of old synonymies (Eastop and Blackman 2005). Historically, and even recently, the number of aphid species (sensu lato) has been estimated (e.g., Oestlund 1886, Kosztarab et al. 1990), but these estimates have always been too low. There are currently more than 5000 valid aphid species (Favret 2016, Remaudière and Remaudière 1997), but many more species remain to be discovered. Data on the synonymies of aphid species can be further extracted from the most recent world aphid catalogs. The catalog by Eastop and Hille Ris Lambers (1976) listed 21 species as having 10 or more synonyms (Ilharco and Van Harten 1987). Remaudière and Remaudière’s (1997) catalog recorded 28 species with 10 or more synonyms. The five species with the highest number of synonyms, as listed in Remaudière and Remaudière’s (1997) catalog, include polyphagous, economically important species: Brachycaudus helichrysi (Kaltenbach) (47 synonyms), Aphis gossypii Glover (42) , Aulacorthum solani (Kaltenbach) (37), Aphis fabae Scopoli (36), and Myzus persicae (Sulzer) (32). The large number of synonyms for some species (e.g., B. helichrysi) could be partly explained by polyphagy and morphological variation on different hosts (Hunter 1901, Ilharco and Van Harten 1987) or by poor communication between aphid workers (Ilharco and Van Harten 1987). Because aphid morphology is strongly influenced by environmental factors, establishing valid species boundaries and determining synonymies remain

problematic (Eastop and Blackman 2005). Still other reasons for synonymy could include a lack of funding for follow‐up investigations on previously collected samples from a limited geographic range or the “publish or perish” syndrome, which may put pressure on taxonomists to describe new species from small samples (Eastop and ­ Blackman 2005).

20.5 ­The Focus Becomes Finer Technological advances in 19th‐century microscopy were followed by equally significant advances in 20th‐century microbiology and statistical analyses. An early pioneer in aphid genetic work was Nobel Laureate Thomas Hunt Morgan, who is better known for his later work with Drosophila melanogaster and the establishment of the chromosome theory of heredity. Some of Morgan’s (1906) earlier studies included karyological drawings of various phylloxerids. Unfortunately, many of the earliest studies on aphid karyology are suspect owing to uncertainties in proper identification of the respective aphid species (Kuznetsova and Shaposhnikov 1973) and lack of voucher material. Subsequent karyotype studies of aphids have been used at various taxonomic levels. For example, the karyotype is often stable at the generic level, although exceptions do occur (e.g., Amphorophora), and in several genera, differences in gross chromosomal morphology are taxonomically important (Blackman 1980a). The importance of the aphid (sensu lato) karyotype and chromosomal numbers has been addressed in detailed reviews by several authors (e.g., Kuznetsova and Shaposhnikov 1973; Blackman 1980a, 1980b, 1985; Hales et al., 1997). By the early to mid‐1980s, aphid karyotype analysis had moved toward measuring the density of the stained nucleus as a tool for determining DNA content (Blackman 1985). Molecular genetic techniques were shifting in the late 1980s. DNA restriction fragment length polymorphism (RFLP) was being applied to aphid taxonomy and systematics (Foottit et  al. 1990). The early to mid‐1990s saw aphid systematics further benefiting from the use

20  The Taxonomy of Crop Pests: The Aphids

of polymerase chain reaction (PCR) and sequencing techniques (e.g., Sorensen et  al. 1995, von Dohlen and Moran 1995). These techniques continue to be refined today (e.g., von Dohlen et al. 2006, Havill et al. 2007, Coeur d’acier et al. 2008, Von Dohlen 2009, Bai, et al. 2010). Morphometrics – the quantitative characterization, analysis, and comparison of biological form (Roth and Mercer 2000) – has been used to examine morphological variation in aphids and adelgids and has influenced taxonomic decision making. Several such studies have examined geographic variation and morphological character variation in aphids (e.g., Pemphigus spp. by Sokal 1962 and Sokal et al. 1980; Adelges piceae (Ratzeburg) by Foottit and Mackauer 1980; and Cinara spp. by Foottit and Mackauer 1990, Foottit 1992, and Favret and Voegtlin 2004). Morphometric approaches, combined with the analysis of other types of data, have been used to analyze morphological patterns in complexes of pest aphid species (e.g., Myzus spp. by Blackman 1987, Rhopalosiphum maidis (Fitch) by Blackman and Brown 1991, and Myzus antirrhinii (Macchiati) by Hales et al. 2000). Increasingly, molecular approaches are being used to resolve taxonomic problems throughout the Aphidoidea at all taxonomic levels. These techniques have developed rapidly in recent years and include RFLP (Foottit et al. 1990, Valenzuela et  al. 2007) and the sequencing of nuclear and mitochondrial markers (Havill et al. 2007), microsatellites (Hales et al. 2000), and other molecular markers (Hales et  al. 1997). DNA barcoding of aphids (Foottit et  al. 2008; Fig. 20.1b) has been recently used to aid species identification. Barcode reference libraries are being developed for North America (Foottit et al. 2008), the Korean Peninsula (Lee et  al. 2011), Europe (Coeur d’acier et  al. 2014), China (e.g., Tang et  al. 2015), and other regions as we progress toward a global reference library. The resolution is finer using molecular techniques (Fig. 20.1b), but workers are still uncovering problems that require even newer approaches. Evidence suggests that phytophagous insects such as aphids acquire new plant hosts and adapt

rapidly to new conditions (Raymond et al. 2001). This results in genetic diversity among aphid populations and even in cryptic species, making it difficult, if not impossible, to determine this diversity using comparative morphological techniques alone (Eastop and Blackman 2005). A combination of classical approaches and new molecular genetic applications will likely prove necessary to determine the extent of diversity in aphid populations and species complexes (e.g., Lozier et  al. 2005), including the presence of cryptic species (e.g., Foottit et  al. 2010). Morphologically indistinguishable species that are differentiated genetically will require a re‐ evaluation of species concepts and the handling of clonal lineages (Foottit 1997). These situations may require a workable nomenclatural system of indexable names for infraspecific taxa (Kim and McPheron 1993).

20.6 ­Adventive Aphid Species Society depends on agronomic, horticultural, and forest plants for its survival, growth, and development. As phytophagous insects, aphids are intimately tied to their host plants and cause significant economic crop losses through direct feeding damage and transmission of plant viruses. With increased international trade and the consequent increased movement of commodities, the connection between aphids and their hosts has resulted in increased rates of introductions (Foottit et al. 2006). In the absence of natural control measures, some of these aphids have had a major economic impact. In North America alone, the establishment of the soybean aphid, Aphis glycines Matsumura, the brown citrus aphid, Aphis (Toxoptera) citricidus (Kirkaldy), and the Russian wheat aphid, Diuraphis noxia (Kurdjumov), has resulted in millions of dollars’ worth of crop losses in recent years (Foottit et al. 2006). Although some notable world treatments address adventive aphid species (e.g., Blackman and Eastop 1994, Blackman and Eastop 2000, Blackman and Eastop 2006), as do recent regional

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taxonomic inventories (e.g., Foottit et  al. 2006, Mondor et  al. 2007, Coeur d’acier et  al. 2010), thorough taxonomic analyses of other regional faunas are needed. Where aphid faunas have been developed, the proportion of adventive species is high. For example, the percentage of adventive species ranges from 19% for the North America aphid fauna (Foottit et al. 2006) to 100% for the Hawaiian aphid fauna (Mondor et  al. 2007). Adventive aphids represent an increasing threat in most regions of the world; their detection will require new approaches such as DNA barcoding (Armstrong and Ball 2005). Historically, questions concerning the taxonomic determination of conspecific aphid species from different biogeographic regions have concerned aphid taxonomists (e.g., Hunter 1901, Foottit et al. 2006). The biogeographic origins of some adventive aphids can be complicated or ill defined. An example of this, among many (Foottit et  al. 2006), is that of the woolly apple aphid, Eriosoma lanigerum (Hausmann). Also known as the American blight, it gained notoriety as an apple pest in Europe, where it was considered to have originated from America. Although generally considered to be native to North America (e.g., Smith 1985), the true origin of this species has long been questioned (Harris 1841, Eastop 1973). Both the ability to identify the source region of pest aphid species and the ability to identify such species in the region of introduction rely on accurate taxonomic information. We need extensive sampling to encompass the range of aphid variability across different hosts in different regions. To make predictions for possible future introductions and formulate necessary regulations, timely identifications based on sound taxonomic science are crucial.

20.7 ­Conclusions From an examination of the taxonomic history of the Aphidoidea, several conclusions can be drawn. Extensive study at all taxonomic levels is needed, including faunal studies, revisionary work, and development of a stable classification

system for species and genera. Given the complex life cycles of aphids and their parthenogenetic mode of reproduction, taxonomy has to be developed at the infraspecific level. Society has an increasing need to understand processes involving adventive species, as well as the management and protection of crops generally and the effects of climate change. Given these needs, it is important to deliver timely and accurate taxonomic information. This delivery can be accomplished most efficiently through an accessible Web‐based system. Although aphids may be considered a well‐ studied pest group, much work remains to be done. Those aphids that garnered Réaumur’s (Fig. 20.1) attention nearly three centuries ago remain a group in need of study, albeit in finer detail.

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21 Adventive (Non-Native) Insects and the Consequences for Science and Society of Species that Become Invasive Alfred G. Wheeler, Jr1 and E. Richard Hoebeke2 1 2

Department of Plant and Environmental Sciences, Clemson University, Clemson, South Carolina, USA Georgia Museum of Natural History and Department of Entomology, University of Georgia, Athens, Georgia, USA

Much of invasion biology’s conceptual frame­ work rests on Darwinian thought (Williamson 1996, Ludsin and Wolfe 2001, Cadotte 2006). An awareness of immigrant species in North America predates Darwin’s work (Inderjit et al. 2005). Before Darwin (1859) published his trea­ tise on the origin of species, entomologists had warned about the establishment of European plant pests in the New World, a concern moti­ vated by a desire to protect agriculture from foreign pests rather than to conserve native bio­ diversity. George Marsh, however, not only was aware of the presence of immigrant insects in the United States, but also other human‐induced changes to the environment. His book Man and Nature (Marsh 1864) “revolutionized environ­ mental thought” (Lowenthal 1990) and pres­ aged the disciplines of conservation biology and invasion ecology. Two classic works inspired interest in adventive species: Elton’s (1958) The Ecology of Invasions by Animals and Plants, which initiated the science of invasion biology (Parker 2001, Richardson 2011; cf. Simberloff 2011b), and The Genetics of Colonizing Species (Baker and Stebbins 1965). The books differ in their empha­ sis. Elton’s (1958) book deals mainly with faunal history, population ecology, and conservation. The book Baker and Stebbins (1965) edited stresses evolutionary rather than ecological

issues and does not address the effects of adventive species on environmental conserva­ tion (Davis 2006). Bates (1956) examined the role of humans as agents in dispersing organisms ranging from microbes to vertebrates. He observed that anthropogenic influences, such as modification of environmental factors and movement of organisms, offer opportunities for experimental studies that could contribute to issues in theo­ retical ecology and clarify evolutionary mecha­ nisms. Invasion biology assumed prominence during the 1980s (Kolar and Lodge 2001, Davis 2006), receiving impetus from the Scientific Committee on Problems of the Environment of the International Council of Scientific Unions and its early symposia on biological invasions (Macdonald et  al. 1986, Mooney and Drake 1986, Drake et  al. 1989, Simberloff 2011b). Invasion biology now has a central role in biotic conservation, and invasive species are used as  tools for biogeographic, ecological, and evolutionary research (Vitousek et  al. 1987, Williamson 1999, Sax et  al. 2005, Davis 2006). Invasion biology’s principal hypotheses, such as biotic resistance and enemy release, were reviewed by Jeschke (2014). An increased mobility of humans and their commodities, coupled with human‐induced habitat disturbances and global warming,

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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enables plants and animals to breach once insurmountable geographic barriers and become established in distant lands and waters (Soulé 1990, Mack et  al. 2000, Mooney and Cleland 2001, Walther et al. 2009). Human colo­ nization has increased the geographic scope, frequency, and taxonomic diversity of biotic dispersal (US Congress 1993, Vitousek et  al. 1997, Mack et  al. 2000). A global estimate of the number of adventive species, including microbes, approaches half a million (Pimentel et al. 2001). The spread of adventive organisms might rank only behind habitat destruction as the greatest threat to biodiversity (Wilson 1992, Wilcove et al. 1998; cf. Davis 2009). Invasion biology, featured in both scientific and popular writings (Simberloff 2004), is fraught with misconceptions and characterized by polemical writing, emotionalism, and contro­ versy. Richardson and Ricciardi (2013) catego­ rized and refuted the various criticisms of invasion ecology. Debate continues over issues such as patterns and processes affecting the movement and success of invaders; the invasibil­ ity of mainland areas compared to islands; the ecological consequences of invasion; the extent to which invaders cause (drive) declines in biodiver­ sity rather than being facilitated by habitat distur­ bances (e.g., fire), which then cause further declines; and the relative importance of direct compared to indirect effects on ecosystems. Moreover, should biological invasions be viewed generally as part of ecological change, and as enriching, rather than impoverishing biodiversity (e.g., Sagoff 2005; cf. Simberloff 2005a)? Whether all invasions should be considered bad and whether a global decline in biodiversity necessar­ ily is bad (Lodge 1993b) depend, in part, on per­ spective: scientific, or moral and social (Brown and Sax 2004; cf. Cassey et al. 2005). Few invasion biologists would endorse the view that all non‐ native species are bad; instead, they are more concerned about the economic and environmen­ tal harm that such species can cause (Simberloff 2003a, 2005a). Also uncertain is the extent to which the effects of invaders are tempered over time, and the extent to which ecological changes

are resolved through evolution and succession in the new ecosystems (Daehler and Gordon 1997, Morrison, 2002, Strayer et  al. 2006). Con­ troversies that continue to pervade invasion biol­ ogy (e.g., Valéry et al. 2013, Blondel 2014) will be difficult to resolve, owing to divergent world views (Simberloff 2012). A recent encyclopedia of biological invasions (Simberloff and Rejmánek 2011) provides the general public with the means for understanding the myriad topics falling within the purview of invasion ecology, and presents researchers in disparate fields of study with a syn­ thesis of current knowledge. Invasion ecology (or biology) is such an inte­ grative discipline that “invasion science” might be a more appropriate designation (Richardson and Ricciardi 2013). We, thus, cannot treat all facets of invasion biology or all cultural, ethical, historical, management, philosophical, political, psychological, and socioeconomic aspects of the invasive‐species problem. We treat adventive insects that are immigrant (not deliberately introduced) or introduced (deliberately so), with an emphasis on North America. Examples deal mainly with human‐assisted movement of insects between countries, even though intracountry changes in range are common among immi­ grant taxa (e.g., the glassy‐winged sharpshooter (Homalodisca coagulata) and western corn root­ worm (Diabrotica virgifera) within the United States). Such range extensions can be as detri­ mental as those between countries (Simberloff 2000a, McKinney 2005). We give little attention to immigrants that arrive on their own by active flight, or by passive conveyance on convective air currents (Southwood 1960) or strong winds associated with El Niño events (Roque‐Albelo and Causton 1999), but discuss those that expand their ranges as the result of global climate change (Musolin and Fujisaki 2006, Musolin 2007).

21.1 ­Terminology Invasion ecology’s status and public appeal is due partly to language that is emotive and militaristic (Colautti and MacIsaac 2004, Larson 2005,

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Coates 2006, Simberloff 2006, Lockwood et  al. 2013, Davis 2009). Indeed, insects have a long history of use as weapons of war (Lockwood 2009). An emphasis on “headline invaders” (Davis et al. 2001) also has contributed to the dis­ cipline’s prominence. Elton (1958) did not define the terms “invader” and “invasion,” which per­ meate the literature on invasive species (Richardson et  al. 2000, Rejmánek et  al. 2002). Terms relating to the concept of “not native” are used interchangeably, even though they are not strictly synonymous (Simberloff 1997, Mack et al. 2000, Sax et al. 2005). Non‐native species have been designated as adventive, alien, exotic, foreign, immigrant, imported, or introduced, sometimes in the same paper (e.g., Sailer 1978, Devine 1998, Clout 1999). Lockwood et al. (2013) listed 20 additional terms used to refer to our non‐native biota. “Newcomer,” a more neutral term than invader, has gained some recent favor (Coates 2006, Acorn 2007). The term “neozoa” is used mainly in the European literature to refer to non‐native animals intentionally or unintention­ ally introduced since 1492 (Occhipinti‐Ambrogi and Galil 2004, Rabitsch and Essl 2006). Entomologists have not been as involved as botanists and plant ecologists in trying to clar­ ify terminology. Zimmerman (1948) catego­ rized insects not native to Hawaii as either immigrant (unintentionally brought in by humans) or introduced intentionally (e.g., for biocontrol purposes). Frank and McCoy (1990) similarly reserved introduced for species delib­ erately introduced, and used immigrant for hitchhikers and stowaways, as well as species that disperse under their own power. Atkinson and Peck (1994), however, regarded bark beetles that have colonized southern Florida by natural dispersal  –  immigrant according to Frank and McCoy’s (1990) terminology  –  as native. It is not always possible to determine whether the arrival of even clearly adventive species involved deliberate human intervention (Simberloff 1997). Certain predators and parasitoids introduced for biocontrol already were established, but undetected, as immigrants at the time of their release (Frick 1964; Turnbull 1979, 1980).

We distinguish adventive taxa as either immi­ grant or introduced (Frank and McCoy 1990, 1995b; Frank 2002), and follow Cowie and Robinson (2003) by using “vector” to refer to the vehicle or mechanism that transports a species and “pathway” for the activity or purpose by which a species is introduced (cf. Carlton and Ruiz 2005). The use of “invasive” has been par­ ticularly problematic. Invasive has been used inconsistently and can refer to all non‐native species, only to non‐native species that spread rapidly in their non‐native ranges, or to those rapidly spreading non‐native species that also cause economic loss, ecological harm, or impair human health (e.g., Richardson et  al. 2000, Colautti and MacIsaac 2004, Pyšek and Richardson 2006, Colautti and Richardson 2009, Davis 2009, Simberloff 2013). We use invasive, despite its subjectivity (Colautti and Richardson 2009), in the sense of a non‐native (adventive) species that is rapidly spreading and, from a human perspective, is “producing undesirable impacts” (Davis 2009). Table 21.1 gives defini­ tions of these and other key terms used herein. The meaning of nativeness typically is not perceived as problematic (Frank 2002), although global climate change is blurring distinctions between native and adventive species (Webber and Scott 2012). We do not define the term native, but refer readers to Chew and Hamilton’s (2011) discussion of biotic nativeness.

21.2 ­Distributional Status: Native or Adventive? Immigrant insects typically are associated with disturbed habitats, but can be found in relatively pristine communities and in isolated areas (Wheeler 1999, Klimaszewski et  al. 2002, Gaston et al. 2003). Whether a species should be considered native or adventive can be problem­ atic (Claassen 1933, Buckland 1988, Whitehead and Wheeler 1990, Woods and Moriarty 2001) and has been complicated by recent range shifts due to global warming (Walther et al. 2009). An apparent immigrant of restricted geographic

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Table 21.1  Some key terms as used in this chapter. Term

Definition

Comments

Adventive

Not native (adj.)

A more neutral term than “alien” or “exotic,” encompassing both immigrant and introduced species (Frank and McCoy 1990); in botanical literature, can refer to non‐native species only temporarily established (Novak and Mack 2001)

Immigrant

Non‐native species not deliberately or intentionally introduced (n.); pertaining to species not deliberately introduced (adj.)

Accidentally or unintentionally introduced (Sailer 1978, McNeely et al. 2001); includes species arriving on their own (Frank and McCoy 1990; cf. Atkinson and Peck 1994): “true immigrants” (sensu Simberloff 2003b)

Introduced

Pertaining to non‐native species deliberately or intentionally introduced (adj.)

Sometimes used broadly to refer to all non‐native species (e.g., Simberloff 2003b, Davis 2009)

Invasive

Pertaining to species that cause socioeconomic or environmental damage or impair human health (adj.)

Variously defined term and subjective, value‐based measurement (Hattingh 2001, Ricciardi and Cohen 2007); sometimes applied to any non‐native species

Pathway

Purpose or activity for which adventive species are introduced, either intentionally or unintentionally (n.)

Follows Cowie and Robinson (2003); for alternative uses, see Richardson et al. (2003), Carlton and Ruiz (2005)

Precinctive

Pertaining to a native species known from no other area (adj.)

More restrictive term than indigenous; often misused for endemic (Frank and McCoy 1990)

Vector

Mechanism or vehicle (physical agent) by which adventive species are transported (n.)

Follows Cowie and Robinson (2003), Ruiz and Carlton (2003); “pathway” often is used to refer to both pathways and vectors (Carlton and Ruiz 2005)

range in its area of invasion poses a conserva­ tion dilemma if eradication of the potentially ecologically disruptive species is considered; an effort to resolve distributional status should be made before any attempt is made to eliminate what might be a rare precinctive (endemic) spe­ cies (Deyrup 2007). Distributional status is particularly difficult to evaluate in the case of vertebrate ectoparasites, pests of stored products, certain ants, cock­ roaches, and other cosmopolitan insect groups (Buckland et  al. 1995, McGlynn 1999, Kenis 2005). By the late 18th century, the honeybee (Apis mellifera) had become so common in the United States that it appeared to be native to the New World (Sheppard 1989). There is much doubt over the distributional status (native or immigrant) of major North American pests (Webster 1892) such as the Hessian fly

(Mayetiola destructor) (Riley 1888, Pauly 2002), a species that is officially listed as endangered in Britain (Samways 1994). Some insects that were once thought to be Holarctic are likely to be immigrants in North America (Turnbull 1979, 1980; Wheeler and Henry 1992), and certain insects that were initially thought to represent new species were later correctly identified as immigrants (e.g., Thomas et  al. 2003). Other immigrants actually were undescribed at the time of their detection (Kim et al. 2004). Thus, a species is not necessarily native to the continent or island from which it was described (Cox and Williams 1981, Green 1984, Gagné 1995, Mound and Morris 2007). The status of certain insects described from North America can be immi­ grant, the species being conspecific with previ­ ously described Old World species (Wood 1975, Wheeler and Henry 1992, Booth and Gullan

21  Adventive (Non-Native) Insects

2006). Certain Eurasian species in North America should be regarded as native to the Pacific Northwest but immigrant in the north­ eastern United States (Lindroth 1957, Turnbull 1980, Sailer 1983). An anthocorid bug (An­­ thocoris nemoralis), which was apparently an immigrant in the northeastern United States, was introduced for biological control in western North America (Horton et al. 2004). Lindroth (1957) discussed historical, geo­ graphic, ecological, biological, and taxonomic criteria that are useful in evaluating distribu­ tional status. His criteria are particularly appro­ priate for the North Atlantic region (Sadler and Skidmore 1995), including Newfoundland, Canada, which has received numerous western Palearctic insects, often via ships’ ballast (Lindroth 1957, Wheeler and Hoebeke 2001, Wheeler et al. 2006). Certain species are likely to be immigrant in North America even though they do not meet any of Lindroth’s (1957) crite­ ria for immigrant status (Turnbull 1979). The 10 criteria used to assess the distributional status of a marine crustacean (Chapman and Carlton 1991) also are appropriate for terrestrial insects. The accuracy of criteria used to resolve distri­ butional status depends on how well the bio­ nomics of the insects in question are known (Turnbull 1980). Molecular genetics can be used to address long‐standing questions about the origin of certain immigrant pests (Howard 1894), sometimes revealing the geographic sources of adventive insects and their invasion histories, including the detection of overlapping or sequential invasions (e.g., Austin et al. 2006, Carter et al. 2010, Xu et al. 2014). In some cases, the area of origin of a plant‐feeding immigrant can be inferred from host plants in the insect’s native area that show maximum resistance and, thus, a coevolved relationship with the herbi­ vore (Messing et al. 2009). Biogeographers and ecologists often consider a species to be native if information is insuffi­ cient to resolve its distributional status, but they do so with unwarranted confidence (Carlton 1996). Whitehead and Wheeler (1990) sug­ gested the opposite approach: when in doubt,

consider the species to be adventive (“non‐ indigenous”). The term “cryptogenic” refers to species that demonstrably are neither native nor adventive (Carlton 1996).

21.3 ­Global Transport: Pathways and Vectors An immense and complex system of world trade supports continually changing pathways and their vectors, allowing increasing numbers of insects to be moved in commerce. Record levels of world tourism are aided by air passen­ ger traffic that increases by about 6% annually (Bright 1998). Approximately 90% of world commerce moves across the oceans every year. The use of containerized cargo has grown rapidly and is concentrated at a few large maritime ports; Los Angeles and Long Beach together handle about 37% of all containers that enter the United States. Container trade at these ports increased by nearly 61% between 2000 and 2011, roughly equal to the increase of container cargo overall (Strocko et al. 2014). Interception data from inspections at major seaports and airports help to identify high‐risk pathways for certain groups of insects. The Port Information Network (PIN), an electronic data­ base initiated by the US Department of Agriculture (USDA) Animal and Plant Health Inspection Service (APHIS) in 1984, comprises records of pests intercepted during inspections of baggage, cargo, conveyances, and related items arriving at US ports of entry and border crossings. Data are available (1985–2005) for bark‐ and wood‐boring Coleoptera intercepted in the continental United States with solid wood packaging material (Haack and Cavey 2000; Haack 2001, 2006). The movement of exotic species, especially those associated with com­ mercial cargo, is well documented (Ridley et al. 2000, McNeely et al. 2001c, Dobbs and Brodel 2004, McCullough et al. 2006, Work et al. 2005, Caton et al. 2006).

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Historically significant pathways in North America included ship ballast and nursery stock, especially before countries adopted plant‐quarantine legislation (Sailer 1983, Wheeler and Hoebeke 2001). We provide

examples (and select references) of immigrant insects moved by three major pathways: trans­ port, agriculture and horticulture, and forestry and  forest products (Table 21.2, Table 21.3, Table 21.4).

Table 21.2  Vectors and examples of insects moved by transport‐related conveyances. Pathway

Vector

Insect group

Reference

Transport related

Early sailing ships (stowaways, hitchhikers)

Cockroaches, bedbugs, fleas, ants, house flies, face and stable flies, clothes moths, carpet beetles, flour and grain pests

Myers 1934, Waterhouse 1991

Soil ballast

Coleoptera (ground beetles, rove beetles, weevils); sawflies, ants; some lygaeoid Heteroptera

Lindroth 1957

Soil associated with living plants

Coleoptera (Carabidae), Gryllotalpidae (mole crickets)

Spence and Spence 1988, Nickle and Castner 1984

Cargo containers

Agricultural, timber, and stored‐ product pests; Coleoptera (Khapra beetle); leaf‐mining Diptera

Stanaway et al. 2001, Work et al. 2005, Caton et al. 2006, Dobbs and Brodel 2004, Spencer 1989

Tourism (travelers)

Fruit pests, e.g., medflies, other fruit flies (Tephritidae)

McNeely 2001b

Airline passenger baggage

Homopterans (aphids, scale insects, Liebhold et al. 2006, Spencer 1989, Carey 1991 mealybugs), Diptera (leaf miners), Coleoptera (Khapra beetle), Diptera (fruit flies)

Used tires

Diptera (mosquitoes)

Moore et al. 1988, Moore 1999, Peyton et al. 1999

Wheel bays of aircraft, fuselage, and passenger cabin

Lepidoptera, Coleoptera, Diptera

Nentwig 2007b; Russell 1987, 1991; Russell et al. 1984; Laird 1951, 1984; Smith and Carter 1984; Takahashi 1989

Illegal smuggling of plants

Diptera (fruit flies), homopterans (scale insects, aphids, mealybugs, psyllids, whiteflies), Thysanoptera (thrips), Coleoptera (weevils), Lepidoptera

Thomas et al. 2011, Hoddle 2006

Military vehicles, used vehicles, machinery and equipment

Soil‐associated insects (Coleoptera, Crooks et al. 1983, US Congress 1993 e.g., weevils, ground and rove beetles; some Heteroptera); soil and soil‐borne pests, and plant pest egg masses

Mail, private delivery services, Internet, catalogue sales

Coleoptera (Khapra beetle), Diptera US Congress 1993, Roques 2010 (medflies)

Homopterans (scale insects, aphids, leafhoppers), Heteroptera (plant bugs, lace bugs), Coleoptera (leaf beetles, wood borers, predators), Diptera (leaf miners, fungus gnats) Mealybugs, scale insects Diptera (leaf miners), Thysanoptera (thrips), Hemiptera (plant bugs), homopterans, (mealybugs), Lepidoptera “Spermatophages” (seed chalcids: Megastigmus spp., coffee berry borer) Diptera (screw‐worm)

Nursery stock (live plants)

Potted plants

Cut flowers

Cones, fruits, and seeds

Domestic and wild animals

Bram and George 2000

Roques et al. 2003

Spencer 1989, Areal et al. 2008, Dymock and Holder 1996, Klassen et al. 2002, Pogue and Simmons 2008, Whattam et al. 2014

Miller et al. 2002, Miller and Miller 2003, Miller et al. 2005

Hamilton 1983, Wheeler and Henry 1992, Wallenmaier 1989, Sæthre et al. 2010, Liebhold et al. 2012, Rabitsch 2008

Reid and Malumphy 2006, Venette and Gould 2006, Dale and Maddison 1984, Waage et al. 2009

Reference

Vector

Coleoptera (various wood borers), Isoptera (termites)

Imported wood and wood products

Tkacz 2002

US Department of Agriculture Forest Service 1991, 1992, 1993; Liebhold et al. 1995

McCullough et al. 2006; Ridley et al. 2000; Haack 2002, 2006; Haack et al. 1997; Smith and Hurley 2000; Wallenmaier 1989; Cappaert et al. 2005; Mattson et al. 2007

Coleoptera (wood borers, Cerambycidae, Buprestidae; bark and ambrosia beetles, Scolytinae; pinhole borers; powderpost beetles, timber borers), Hymenoptera (Siricidae, Xiphydriidae), Isoptera (termites) Lepidoptera (Asian and European gypsy moth, nun moth), Coleoptera (Scolytinae), Hymenoptera (Siricidae)

Reference

Insect group

Logs and minimally processed wood

Forestry and Solid wood packaging forest products material (crates, pallets, dunnage, spools)

Pathway

Table 21.4  Vectors and examples of insects that are moved in association with forestry and forest products.

Diptera (fruit flies), ants, Coleoptera, Heteroptera, Lepidoptera, Thysanoptera, homopterans (scale insects, aphids)

Agricultural products (for consumption)

Agriculture and horticulture

Insect group

Vector

Pathway

Table 21.3  Vectors and examples of insects that are moved in agriculture and horticulture.

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Insect Biodiversity: Science and Society

21.4 ­Early History of Adventive Insects in North America Other organisms accompanied Homo sapiens during each major invasion: from Africa, where humans apparently evolved, to Eurasia; thence to Australia, the Americas, and, eventually, to the far reaches of the Pacific (McNeely 2001b, 2005). Lice might have been the first insects to have been transported (Laird 1984). As early as the 9th century, Norse colonists were responsi­ ble for the establishment of European insects in  Greenland (Sadler 1991). Spanish galleons (sailing ships) were responsible for the global transport of insects by the 16th century (Gotzek et al. 2015). Insects probably arrived in the New World with landfall by Columbus, who “mixed, mingled, jumbled, and homogenized the biota of our planet” (Crosby 1994). Insects probably arrived in North America with the Mayflower’s landing in 1620 and continued to enter with every ship that brought additional people and supplies from Europe (Sailer 1978, 1983). Earlier, the housefly (Musca domestica) might have been brought to tropical latitudes of the Western Hemisphere via canoe or raft by pre‐ Columbian inhabitants of Central or South America (Legner and McCoy 1966). Outside North America, the Polynesians who colonized Hawaii in prehistoric times might have brought with them a few insects, such as vertebrate ectoparasites, the housefly, and a cockroach (Balta similis) (Gagné and Christensen 1985, Beardsley 1991). Early‐arriving insects in the United States and elsewhere mostly were those that could survive a several‐month sea voyage under adverse phys­ ical conditions: associates of stored products, ectoparasites and blood suckers of humans and their livestock, inhabitants of their excrement, and soil dwellers in dry ballast brought aboard sailing ships (Lindroth 1957, Sailer 1978, Turnbull 1979, Buckland et al. 1995). For many other insect groups, long sea voyages functioned as inadvertent quarantines years before formal plant quarantines were adopted (Gibbs 1986).

Among early immigrants in the northeastern United States were the bed bug (Cimex lectu­ larius), head (and body) louse (Pediculus humanus), and oriental cockroach (Blatta ori­ entalis) (Sasscer 1940; Sailer 1978, 1983). Pestiferousness of the stable fly (Stomoxys calci­ trans) perhaps led to hasty adoption of the Declaration of Independence (Kingsolver et al. 1987). Crop pests generally were not among the early arrivals (Sailer 1978), although archeologi­ cal evidence has shown that certain pests were present much earlier than once thought (Bain and LeSage 1998). On the West Coast, where 18th‐century agriculture was limited to Spanish missions in southern California, various weevils entered with food and seed cereals. Livestock ships brought several species of muscoid flies to California; fur, hide, tallow, and whaling ships allowed additional stored‐product insects to enter (Dethier 1976). Thirteen immigrant insects apparently became established in the United States by 1800 (McGregor et al. 1973), and the total number of adventive species was about 30 (Sailer 1983); Simberloff’s (1986) total of 36 seems to include the mite species noted by Sailer. Numerous other immigrant insects, common in England but not detected in North America until after 1800, probably were present by the 18th century (Sasscer 1940, Sailer 1983). Even with establish­ ment of European plant pests such as the codling  moth (Cydia pomonella), Hessian fly (M.  destructor), oystershell scale (Lepidosaphes ulmi), and pear sawfly (Caliroa cerasi), neither native nor immigrant insects were particularly problematic in the northeastern United States (Dethier 1976; Sailer 1978, 1983). Pest outbreaks did occur, and cessation of burning by the Native Americans favored additional problems from insects (Cronon 1983). Yet, crops in the American colonies mostly were free from the insects that plague modern agriculture (Popham and Hall 1958). The minimal damage from insects was due partly to a lack of extensive and intensive crop production and scarcity of immi­ grant pests; damage might have been greater

21  Adventive (Non-Native) Insects

because some crop losses went unrecognized (Davis 1952). Drought, however, was the main enemy of colonial farmers (Dethier 1976). Before the 19th century, soil exhaustion and limiting socioeconomic conditions also remained more important than insects as deterrents to agricul­ ture (Barnes 1988). The subsistence‐level agriculture of early European settlers, and their cultivation of crops such as corn and squash, did little to disrupt evolutionary relationships between plants and insects (Dethier 1976, Barnes 1988). Increasingly, however, insects emerged as consistent agricul­ tural pests. It is not true, as a politician in a west­ ern state contended, that the United States lacked destructive insects until the country had entomologists (Webster 1892). Increasing trade with Europe, more rapid means of transportation, planting of additional European crops, and expanding crop acreages favored the arrival and establishment of new insects from Europe. As humans altered ancient relationships between plants and insects, they unwittingly ushered in an era of immigrant pests (Dethier 1976). In roughly 200 years, a “new ecology” had been created, setting the stage for damage by native insects and the entry of additional European species (Barnes 1988). The slow accumulation of immigrant insects, lasting until about 1860 (Sailer 1978), gave way to a “continuous, persistent procession” of immigrants (Herrick 1929).

21.5 ­Numbers, Taxonomic Composition, and Geographic Origins of Adventive Insects No continent or island is immune to invasion by immigrant organisms. Changes in transport technology and types of commodities trans­ ported have affected the predominance of certain groups of insects at different time peri­ ods in every world region. Our discussion of the immigrant insect fauna will emphasize the 48 contiguous US states, a principal focus of Sailer’s (1978, 1983) seminal work. The specific

composition of the US adventive insect fauna is influenced not only by changes in pathways, vectors, and trade routes, but also by the kinds of natural enemies imported for biocontrol, the availability of taxonomists who can identify insects in particular families, taxonomic bias in the kinds of insects collected in detection sur­ veys, and changes in quarantine‐inspection procedures. Faunal lists are important but labor intensive and time consuming; thus, few up‐to‐date, comprehensive inventories or databases of immigrant insects exist for most world regions. Lists of adventive taxa, however, allow an analy­ sis of their geographic origins, the number of established species, and the systematic compo­ sition of the most successful groups, as well as comparisons among biogeographic regions. From data on immigrant insect faunas, we focus on select countries on different continents, oce­ anic islands or atolls, and several agriculturally important US states (Table 21.5). The immi­ grant insect fauna of the United States is one of the best studied and most thoroughly docu­ mented (McGregor et  al. 1973; Sailer 1978, 1983). Of more than 3500 species of adventive arthropods that reside in the continental United States (Frank and McCoy 1992), more than 2000 insect species are established, represent­ ing about 2–3% of the insect fauna (US Congress 1993). Sailer’s (1978, 1983) analysis revealed several major trends among adventive insects in the US fauna. The ubiquitous use of dry ballast during the era of early sailing ships (17th to early 19th century) was responsible for an early dominance of Coleoptera. At British ports, beetles and ground‐dwelling bugs (Hemiptera: Heteroptera) were common in dry ballast (Lindroth 1957). After the American Civil War, Hemiptera arrived with nursery stock and other plant material from Western Europe. Sailer (1978) determined that homopterans (non‐heteropteran Hemiptera) contributed the largest number of adventive spe­ cies, but in his later analysis, hymenopterans, with approximately 390 species (23%), pre­ dominated (Sailer 1983). The introduction of

649

284

463 356

12,500

7,998

~13,740

21,833

NA

29,292

152

Hawaii

Austria

United Kingdom

Italy

Japan

Galápagos Islands ~2,013

5,579

Florida

New Zealand (Coleoptera only)

Tristan da Cunha Islands

55.3

6.4

23

9.7

NA

1.5

~1.5

~32

7.6–10

7.4

2–3

NA

1.4 spp./yr (1950–1987), 1.7 spp./yr (1988–1997)

20.7 spp./yr (1996–2004)

4.0 spp./yr (1945–1995)

4.0 spp./yr (1975–1995)

4.5 spp./yr (1970–2004)

NA*

12.4 spp./yr (1912–1935), 14.5 spp./yr (1937–1961), 18.1 spp./yr (1962–1976)

12.9 spp./yr (1971–1991), 7.7 spp./yr. (1970s), 12.0 spp./yr (1980s)

6.1 spp./yr (1955–1988)

11.0 spp./yr (1910–1980), 6.2 spp./yr (1970–1982)

Estimated rate of annual detection

*Not available. †Includes immigrant (“alien”) species and those of doubtful status.

84†

162

325

212

2,598

945

208

~28,000

California

>2,000

~90,000

Conterminous United States

Geographic area

Number of Number of Percentage described immigrant of total species species composition

Table 21.5  The adventive insect fauna of selected geographic areas.

Powell and Hogue 1979, Dowell and Gill 1989

Hoebeke and Wheeler 1983, Sailer 1983, US Congress 1993, Arnett 2000, Papp 2001

Reference

Kiritani 1998, Morimoto and Kiritani 1995, Kiritani 2001

Pellizzari and Dalla Montà 1997, Pellizzari et al. 2005

Williamson and Brown 1986, Smith et al. 2005

Rabitsch and Essl 2006

Klimaszewski and Watt 1997 Hemiptera (86.7), Coleoptera Holdgate 1960, 1965 (46.5), Lepidoptera (45.5)

NA

Hemiptera (25.5), Coleoptera Peck et al. 1998, Causton (24.0), Diptera (14.3) et al. 2006

Coleoptera (32.0), homopterans (27.8), Lepidoptera (12.3)

Homopterans (64), Coleoptera (12), Lepidoptera (7)

Homopterans (11.5), Coleoptera (2.6)

Coleoptera (1.1), Lepidoptera (0.6)

Thysanoptera (78.9), Diptera Beardsley 1962, 1979, 1991; (44.3), homopterans (43.4) Simberloff 1986; Howarth 1990; Nishida 1994; Eldredge and Miller 1995, 1997, 1998; Miller and Eldredge 1996

Coleoptera (33), Lepidoptera Frank and McCoy 1992, Frank and (24.9), homopterans (16.3) McCoy 1995b, Frank et al. 1997

Homopterans (33.7), Coleoptera (12.0), Lepidoptera (11.5)

Homopterans (20.5), Coleoptera (20.3), Lepidoptera (7.4)

Orders with most immigrants (% of total)

21  Adventive (Non-Native) Insects

numerous parasitic wasps to help control adven­ tive pest arthropods and weeds was thought to be responsible for the disproportionate increase in Hymenoptera. Next in abundance of species were the Coleoptera (372), homopterans (345), Lepidoptera (134), and Diptera (95). Immigrant arthropods in the United States originate mainly from the western Palearctic (66.2%), followed by the Neotropical (14.3%), and eastern Palearctic and Oriental regions (13.8%) (Sailer 1983). Florida has the highest percentage of adven­ tive insects in the conterminous United States (only Hawaii has a higher percentage); about 1000 such species are established, representing about 8% of Florida’s insect fauna (Frank and McCoy 1995a). Although many of the species entered with commerce (e.g., as stowaways in plant material), others arrived by aerial disper­ sal from Caribbean islands (Cox 1999). Although Floridian immigrants originate from many world regions, they arrive mainly from the Neotropics and Asia. Beetles were best represented (~26%) among the 271 species of immigrant insects newly recorded from Florida from 1970 to 1989. Coleoptera were followed by Lepidoptera (~19%), Hymenoptera (~15%), and homopter­ ans (~13%) (Frank and McCoy 1992). A similar study in Florida for 1986 to 2000 listed 150 adventive insects (Frank and Thomas 2013). Unlike Frank and McCoy’s (1992) study, hom­ opterans contributed the largest number of spe­ cies (~35%), followed by Coleoptera (~26%). The proportion of Coleoptera was similar, but that of homopterans increased substantially (~13% to ~35%), whereas that of Lepidoptera declined (~19% to ~3%). From 1970 to 1989, the majority of immigrant species in Florida arrived from the Neotropics (~65%) (Frank and McCoy 1992). By contrast, from 1986 to 2000, the num­ ber of Asian immigrants increased substantially (~50%) (Frank and Thomas 2013). Between 1994 and 2000, the number of quarantine pest interceptions at Florida ports of entry increased by 162% (Klassen et al. 2002). Immigrant insects have a long history of crop  damage in California, another important

agricultural state. Between 1955 and 1988, infes­ tations of 208 immigrant invertebrates were dis­ covered. Homopterans, followed by coleopterans and lepidopterans, made up the greatest number of insects; the majority originated from other regions of North America, followed by the Pacific region and Europe. After 1980, the immi­ gration rate from Asia, Australia, Europe, and the Pacific region increased, especially that by dipterans, hymenopterans, and homopterans (Dowell and Gill 1989). R. V. Dowell (California Department of Food and Agriculture, Sacra­ mento; cited by Metcalf 1995) compiled a partial list of adventive insects (460 species) established in California between 1600 and 1994. Hawaii is the most invaded region of the United States because of its particular geogra­ phy, climate, and history. Approximately 350– 400 species of insects (“original immigrants”) colonized the islands before human settlement, probably arriving by ocean or air currents (US Congress 1993). Commerce with the outside world followed the European discovery of the Hawaiian Islands, which allowed additional immigrant insects to enter. Nearly 4600 adven­ tive species have become established, more than half (> 2500) of which are arthropods (Nishida 1994, Miller and Eldredge 1996, Eldredge and Miller 1998). More than 98% of pest arthropods are immigrant (Beardsley 1993), and 28% of all Hawaiian insects are adventive (Simberloff 1986), including the entire aphid and ant faunas (Holway et  al. 2002, Krushelnycky et  al. 2005, Mondor et al. 2007). The rate of establishment of adventive species remains high: an average of 18 new insect species annually from 1937 to 1987 (Beardsley 1979). Since 1965, about 500 immigrant arthropods have become established in the Hawaiian Islands, an annual rate of about 20 species (Beardsley 1979, 1991). With many immigrant pests having become established in Hawaii over the past century, classical biocon­ trol has been much used (Funisaki et al. 1988). Canada also is home to numerous adventive insects, with the immigrants of British Columbia, Newfoundland, and Nova Scotia best known. Turnbull (1980) listed 155 immigrant

651

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Insect Biodiversity: Science and Society

insects in Canada, including human ectopara­ sites and species associated with dwellings, stored products, cultivated crops and forest trees, and domesticated animals. The Canadian fauna also includes more than 300 species intro­ duced for biological control (Turnbull 1980). The Coleoptera and Hemiptera are reasonably well known in Canada, with recent checklists available for both groups. Of the nearly 7500 coleopteran species recorded in Canada (includ­ ing Alaska), 469 are considered immigrant (“introduced”) in North America (6.2% of the total) (Bousquet 1991). More than 300 species of adventive Hemiptera have been documented in Canada (and Alaska), representing approxi­ mately 7.7% of the nearly 3900 species (Maw et al. 2000); 81 adventive heteropterans, mainly from the western Palearctic, are known from Canada (Scudder and Foottit 2006). Gillespie’s (2001) review of adventive insects detected in British Columbia from the late 1950s to 2000 included information on immi­ grant lepidopterans such as the codling moth (C. pomonella) and winter moth (Operophthera brumata). Among the 48 immigrant lepidopter­ ans are 19 species of Tortricidae (Gillespie and Gillespie 1982). The adventive fauna of British Columbia also includes 42 leafhopper (cicadel­ lid) species (9%) (Maw et al. 2000), 32 plant bug (mirid) species (9%) (Scudder and Foottit 2006), and 10 orthopteroid species (8%) (Scudder and Kevan 1984). The immigrant fauna of Newfoundland and Nova Scotia has received considerable attention (e.g., Brown 1940, Lindroth 1957, Morris 1983). Recent collecting has yielded numerous addi­ tional immigrants (e.g., Hoebeke and Wheeler 1996, Wheeler and Hoebeke 2005, Majka and Klimaszewski 2004, Wheeler et al. 2006). Of the 325 adventive invertebrate plant pests  that became established in Great Britain between 1787 and 2004, nearly half of the spe­ cies (48.6%) have been recorded since 1970 (Smith et  al. 2005). Homopterans (37.1%) and lepidopterans (31.3%) dominate. Nineteen per­ cent of the adventive plant pests originated from Europe; since 1970, 35.6% of the species

originated from continental Europe, 20.3% from North America, and 13.6% from Asia. At least 500 adventive animal species (~1% of  the country’s entire fauna) have become established in Austria since 1492 (Essl and Rabitsch 2002, Rabitsch and Essl 2006). The majority (60%) are insects, with Coleoptera and Lepidoptera best represented. About 30% of the Coleoptera are Palearctic (mostly Mediter­ ranean), 23% are Oriental, 18% are Neotropical, and 7% are Nearctic. Nearly 33% of the Lepidoptera originated from the Palearctic Region, 22% from the Nearctic Region, 19% from  the Oriental Region, and 10% from the Neotropical Region. The Asian long‐horned beetle (Anoplophora glabripennis; from China) and western corn rootworm (D. virgifera; from North America) are notable coleopterans detected since 2000. Insects are the most numerous of all adven­ tive organisms in Switzerland; more than 300 species have become established via human activities (Kenis 2005). Much of this fauna is Mediterranean, although large numbers of trop­ ical or subtropical insects are found in green­ houses (thrips and whiteflies) or are associated with stored products (beetles and moths). Adventive Coleoptera comprise more than 120 species (~40% of the total adventive insect fauna), including the North American Colorado potato beetle (Leptinotarsa decemlineata) and western corn rootworm. Fewer than 20 species of adventive Diptera are established in Switzerland (Kenis 2005). Of the insects documented in the Japanese islands, 239 species (0.8%) were considered adventive (Morimoto and Kiritani 1995), but Kiritani (1998) noted that 260 adventives (“exotic species”) had been introduced since 1868. Kiritani and Yamamura (2003) increased the number of adventive insect species known from Japan to 415. Coleoptera (31.2%), homopterans (25.8%), Hymenoptera (11.2%), and Lepidoptera (12.3%) have the largest number of adventive species. Approximately 76% of the immigrant insects are considered pests, whereas only 8% of  native Japanese insects are pestiferous

21  Adventive (Non-Native) Insects

(Morimoto and Kiritani 1995). Although the southern islands represent only 1.2% of Japan’s land area, about 40% of all immigrant species first became established in these islands (Kiritani 1998). More than 2000 invertebrate species (mostly insects) in New Zealand are adventive (Broc­ kerhoff and Bain 2000). The ant fauna consists of 28 immigrant and 11 native species (Ward et  al. 2006). Several important pests of exotic trees have become widely established (Scott 1984, Charles 1998); additional, potentially important species are routinely intercepted at ports of entry (Bain 1977, Keall 1981, Ridley et al. 2000). More than 350 adventive beetle spe­ cies are known from New Zealand (Klimaszewski and Watt 1997). A recent survey of adventive beetles that attack trees or shrubs in New Zealand yielded 51 immigrants in 12 families, most of which were of Australian (58%) and European (25%) origin (Brockerhoff and Bain 2000). Hoare (2001) reported 27 lepidopteran species new to New Zealand since 1988; the majority (67%) represented migrants from Australia, whereas certain others arrived via commerce with Asia or Europe. The extent of the Australian insect fauna and number of adventive species is unknown (New 1994). More than 2000 adventive species are considered to be established, but the actual number might be much greater (Low 2002). More than half of the insect orders include an adventive component (New 1994). About 80% of some 150 aphid species are immigrant (New 2005). Adventive insects are most diverse and have had greatest impact in areas most strongly influenced by European settlement (“cultural steppe”) (Matthews and Kitching 1984, New 1994). Analyses and lists of the adventive insects in other countries, islands, and regions include those for Central Europe (Kowarik 2003), France (Martinez and Malausa 1999), Germany (Geiter et al. 2002), Israel (Bytinski‐Salz 1966, Roll et al. 2007), Italy (Pellizzari and Dalla Montà 1997, Pellizzari et al. 2005), Kenya (Kedera and Kuria 2003), the Netherlands (van Lenteren et  al.

1987), Serbia and Montenegro (Glavendekić et  al. 2005), southern oceanic islands (Chown et al. 1998), Spain (Perez Moreno 1999), Tristan da Cunha (Holdgate 1960), and Venezuela (MARN 2001). The USDA’s National Agri­ cultural Library created the National Invasive Species Information Center in 2005; its website (http://www.invasivespeciesinfo.gov/about. shtml) provides access to sites that contain data on immigrant insects of additional countries and regions.

21.6 ­Impact of Adventive Insects Early concerns about the consequences of immi­ grant insects in the United States involved agri­ culture and losses to crop production. Direct effects from ectoparasitic and blood‐sucking insects would have been apparent to the colo­ nists, but they probably gave no thought to whether the offending species were native. Arthropod‐borne diseases were endemic in the colonies from New England to Georgia (Duffy 1953, McNeill 1976, Adler and Wills 2003), and an outbreak of yellow fever in Philadelphia in 1793 was attributed to trade with the West Indies (Inderjit et al. 2005). It was not until the late 19th or early 20th century that mosquitoes and certain other arthropods were demon­ strated to transmit the causal organisms of major human diseases (Mullen and Durden 2002). Every organism that colonizes a new area can affect native communities and ecosystems (Smith 1933, Lodge 1993a). Most immigrant insects, other than several widespread species of mosquitoes, are terrestrial; as invaders, aquatic insects tend to be underrepresented (Karatayev et  al. 2009). Other aquatic immigrants include the midges Goeldichironomus amazonicus in California and Florida (Wirth 1979, Sublette and Mulla 1991, Frank et al. 1997) and Polypedilum nubifer in Florida and Hawaii (Jacobsen and Perry 2007), two Asian corixids in Florida (Polhemus and Rutter 1997, Polhemus and Golia 2006), and perhaps a blackfly in the Galápagos Islands (Roque‐Albelo and Causton 1999).

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Not all adventive species produce quick and  dramatic effects on native ecosystems (Richardson 2005). Many immigrant insects produce minimal or no observable effects (Williamson 1996, Majka et  al. 2006) and may never become problematic; they seemingly become integrated into novel communities as benign or innocuous members of the fauna (Turnbull 1967, Sailer 1978). Although certain immigrants undergo rapid spread, for example, the leucaena psyllid (Heteropsylla cubana) (Beardsley 1991) and erythrina gall wasp (Quadrastichus erythrinae) (Li et al. 2006), oth­ ers remain localized. An oak leaf‐mining moth (Phyllonorycter messaniella) has spread little in Australia since being detected in 1976 and has remained innocuous, with only occasional out­ breaks (New 1994). Two immigrant webspinners (Embiidina) in Australia (New 1994), immigrant beetles in Switzerland that live in decaying plant material and litter (Kenis 2005), scavenging microlepidopterans in the western United States (Powell 1964), and most immigrant psocopter­ ans in North America (Mockford 1993) will probably remain innocuous and obscure. Some immigrants remain rarely collected years after their detection: for example, two Palearctic het­ eropterans in North America, a lace bug (Kalama tricornis) (Parshley 1916, Bailey 1951) and lepto­ podid (Patapius spinosus) (Usinger 1941, Lattin 2002). Three immigrant heteropterans (rhyparo­ chromid lygaeoids) that feed on fallen seeds likely would have been predicted to be little‐ known additions to the fauna of western North America. Instead, these immigrant bugs attracted media attention when they invaded homes, libraries, schools, and businesses, creating anxiety, affecting local economies, and necessi­ tating control measures (Henry and Adamski 1998, Henry 2004). An immigrant thrips (Cartomothrips sp.) in California (Arnaud 1983) would have been expected to remain an obscure faunal addition, but it has been said (without evi­ dence, except that it probably feeds on fungi in decaying vegetation) to have the potential to affect ecosystem processes such as decomposi­ tion and nutrient cycling (Mooney et al. 1986).

Labeling most adventive insects as “innocu­ ous” should be done with caution because their potential for adverse effects might never have been investigated (National Research Council 2002). Studies of immigrant herbivores typically involve their effects on economically important plants rather than possible injury to native plants, many of which in Hawaii are endangered (e.g., Messing et al. 2007). In addition, extended lag times between establishment and explosive population growth are relatively common (Carey 1996, Crooks and Soulé 1999, Loope and Howarth 2003, Crooks 2005), and competitive exclusion on continental land masses might not take place for long periods (New 1993). The environmental effects of invasive species sometimes are thought to have received sub­ stantial attention only in the 20th century, mainly after Elton’s (1958) book appeared. Yet Marsh’s (1864) book, which stresses global anthropogenic disturbances, often is overlooked by current conservationists and invasion biolo­ gists. In discussing civilization’s effects on the insect fauna of Ohio, Webster (1897) noted veg­ etational changes such as the reduction of for­ ested areas, apparent disappearance of some native insects, and establishment of European insects. He did not, however, suggest that adventive insects cause environmental changes. We now know that diverse systems are as vul­ nerable to invasion as those of low diversity, perhaps more so (Levine 2000, D’Antonio et al. 2001; cf. Altieri and Nicholls 2002 with respect to agroecosystems); that, in some cases, invasive species drive global environmental change (Didham et  al. 2005; cf. MacDougall and Turkington 2005); and that biotic mixing can involve the introduction of alien alleles and gen­ otypes (Petit 2004). According to the “tens rule” (Williamson 1996, Williamson and Fitter 1996), about 10% of invaders become established, and about 10% of established species become pests. The rule, despite its statistical regularity, involves con­ siderable variability (Williamson and Fitter 1996, White 1998); it should be considered a working hypothesis (Ehler 1998) and perhaps

21  Adventive (Non-Native) Insects

disregarded for predictive purposes (Suarez et al. 2005). Immigrant insects can become pes­ tiferous at rates almost 10 times higher than for native species (Kiritani 2001). Despite impending homogenization of our biota, immigrants are not uniformly dispersed and, as might be predicted, show less cosmo­ politanism than plant pathogens (Ezcurra et al. 1978). For example, the distributions of immi­ grant insects that are forest pests in the United States are concentrated in the northeastern United States, where propagule pressure has been greatest (Liebhold et al. 2013). The distri­ butions of immigrant insects are not necessarily niche conservative  –  in areas of invasion, they can adapt to environments in a way that would not have been predicted (e.g., da Mata et  al. 2010). Immigrant species essentially are every­ where: national parks, nature reserves, and rela­ tively pristine communities (Macdonald et  al. 1989, Cole et al. 1992, Pyšek et al. 2003), as well as boreal areas (Simberloff 2004, Sanderson et  al. 2012) and Antarctica (Block et  al. 1984, Frenot et  al. 2005, Hughes et  al. 2013). Fewer immigrant insects have become established in remote areas than along major trade routes and in other areas subject to human disturbance, as is true generally for invasive species (Sala et al. 2000, McNeely 2005; cf. Gaston et  al. 2003). Urban areas serve as foci of entry for invaders (Frankie et  al. 1982, McNeely 1999, Colunga‐ Garcia et al. 2010, Koch et al. 2011), with immi­ grant insects (Wheeler and Hoebeke 2001, Majka and Klimaszewski 2004) typically being concentrated around shipping and other trans­ port hubs (US Congress 1993, Floerl and Inglis 2005, Colunga‐Garcia et  al. 2010, Koch et al. 2011). The ecological effects of adventive species tend to be severe on old, isolated oceanic islands (Vitousek 1988, Coblentz 1990; cf. Simberloff 1995). The economic effects of such species can be particularly devastating to developing nations (Vitousek et  al. 1996). Countries that experience the greatest effects from invasive species are heavily tied into systems of global trade (Dalmazzone 2000, McNeely 2006), as

shown by the rise in biological invasions trig­ gered by China’s recent economic growth (Ding et al. 2008). Invasive species generally have had greater impact in the United States than in continental Europe, where traditionally they have  been regarded as a less serious threat (Williamson 1999). Europe, although largely an exporter of species, has experienced recent increases in immigrant species (Pellizzari and Dalla Montà 1997, Essl and Rabitsch 2004, Kenis 2005, Roques 2010). More attention, therefore, is being devoted to the problem (Scott 2001, Reinhardt et al. 2003). In addition to the United States (US Congress 1993), countries such as Australia, New Zealand, and South Africa have been substantially affected by immigrant insects (Macdonald et al. 1986, McNeely 1999, Pimentel 2002). By 2100, adverse effects from invasive species are expected to be most severe in Mediterranean ecosystems and southern tem­ perate forests (Sala et al. 2000). The various consequences of invasive species create what Barnard and Waage (2004) termed a “national, regional, and global development problem.” In contrast to most other human‐ induced environmental disturbances – ­pollution and inappropriate use of resources, such as poor farming or the draining of wetlands – the inva­ sive species problem is harder to ameliorate and often ecologically permanent (Coblentz 1990). Mooney (2005) created 13 categories for the harmful effects of invasive species, some rele­ vant mainly or solely to plants. At least six, how­ ever, relate to insects: animal disease promoters, crop decimators, forest destroyers, destroyers of homes and gardens, species eliminators, and modifiers of evolution. Whereas invasion biolo­ gists and conservationists generally agree that the consequences of invasive species are sub­ stantial, they disagree on how best to measure the impact of invaders (Parker et  al. 1999, National Research Council 2002). Adventive insects can be viewed differently in different regions and considered either positive or negative, depending on the observer’s per­ spective. For example, a North American plant­ hopper (Metcalfa pruinosa) immigrant in

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Europe has become a plant pest, but honeybees collect its honeydew in producing a honey that Italian apiarists market as “Metcalfa honey” (Wilson and Lucchi 2007). Our perceptions of adventive species can be fluid, modified as the result of environmental change, subsequent introductions (US Congress 1993, Simberloff et al. 1997), or as the status of natural enemies that have been introduced for biocontrol changes with changing values (Syrett 2002). The arrival of immigrant fig wasps allowed certain fig species to become weedy in New Zealand and elsewhere (McKey 1989, Kearns et al. 1998). Two immigrant seed wasps detected in Florida in the 1980s, one associated with Brazilian pep­ per (Schinus terebinthifolius) and the other with laurel fig (Ficus microcarpa), would have been considered detrimental when these plants were valued as ornamentals, but can be viewed as beneficial now that both plants are considered weeds (Nadel et al. 1992, Frank et al. 1997). The presence in Florida of other Ficus‐associated insects reveals the complexity of evaluating the status of adventive species. The Cuban laurel thrips (Gynaikothrips ficorum), which upon detection was considered to be a pest of orna­ mental figs, now is regarded as a beneficial nat­ ural enemy of F. microcarpa. Another immigrant fig insect, an anthocorid bug (Montandoniola moraguesi), until recently would have been viewed as beneficial because it preys on laurel thrips. With the reversal in the fig’s status, the anthocorid has become an unwanted enemy of a thrips that inflicts severe foliar damage to an undesirable tree (Bennett 1995). In Hawaii, the anthocorid’s status changed from a predator introduced to control the Cuban laurel thrips to one that impaired the effectiveness of a thrips that was introduced for weed biocontrol (Reimer 1988). 21.6.1 Beneficial

With an emphasis on the adverse effects of immigrant insects, it is easy to overlook their benefits. Insects are crucial to human existence and ecosystem functions (Waldbauer 2003).

The ecological services provided in the United States by mostly native insects are estimated to be worth nearly US$60 billion annually (Losey and Vaughan 2006). Comparable data on adven­ tive species are unavailable, but such insects also contribute important ecological services. Cochineal, shellac, silk, and other insect prod­ ucts are well known and have been used where the insects are not native (Metcalf and Metcalf 1993, New 1994). The cochineal industry helped to save the Canary Islands from starvation after the grape phylloxera (Daktulosphaira vitifoliae) devastated the islands’ vineyards in the late 19th century (Cloudsley‐Thompson 1976). Locally, adventive insects sometimes can be viewed as ecologically desirable additions to a fauna, such as carabid beetles in impoverished arctic communities (Williamson 1996). In west­ ern Canada, immigrant synanthropic carabids were regarded as enriching the fauna; they appear not to threaten native Carabidae because only one native species is strictly synanthropic (Spence and Spence 1988). Immigrant natural enemies arriving with, or separately from, immi­ grant pests provide fortuitous, although often ineffective, biocontrol (DeBach 1974, Colazza et al. 1996, Nechols 2003). An immigrant para­ sitoid, however, might provide effective control of the San Jose scale (Quadraspidiosus pernicio­ sus) in the United States (Sailer 1972). Immigrant insects, such as the blowfly (Chrysomya rufifacies) in Hawaii, are useful in forensic entomology for establishing postmor­ tem intervals (Goff et al. 1986). The alfalfa leaf­ cutter bee (Megachile rotundata) is an important pollinator of alfalfa in the United States (Cane 2003). In nature, adventive species can facilitate native species by providing trophic subsidies (Rodriguez 2006). Immigrant insects provide food for numerous birds, mammals, amphibi­ ans, reptiles, and insects and other inverte­ brates. In the northeastern United States, a European weevil (Barypeithes pellucidus) con­ tributes substantially to the diet of a native sala­ mander (Plethodon cinereus); other predators, including birds, small mammals, snakes, and

21  Adventive (Non-Native) Insects

invertebrates, also prey on the weevil (Maerz et  al. 2005). An immigrant leafhopper (Opsius stactagalus) of the invasive saltcedar (Tamarix ramosissima) provides food for native birds and riparian herpetofauna in southwestern states (Stevens and Ayers 2002). Although the prominence of Drosophila mel­ anogaster as a research organism does not depend on its immigrant status, the fly has been studied on continents where it is not native. Experimental work on this immigrant fly has led to four Nobel prizes (Berenbaum 1997). An Old World congener (Drosophila subobscura) now established in North and South America (Beckenbach and Prevosti 1986) is being used to enhance our understanding of the predictability and rate of evolution in the wild (Huey et al. 2005). Sterile insect technique, a new principle in population suppression and a “technological milestone in the history of applied entomology” (Perkins 1978), was developed to eradicate the screw‐worm fly (Cochliomyia hominivorax) from the southern United States (Knipling 1955, Klassen and Curtis 2005). Other immigrants, including the Hessian fly (M. destructor), had key roles in the development of resistant crop varieties in the United States (Painter 1951, Kogan 1982), and the cereal leaf beetle (Oulema melanopus) contributed to the modeling of population dynamics and pattern of spread (Kogan 1982, Andow et al. 1990). The identifi­ cation and synthesis of sex‐attractant phero­ mones of lepidopterans that are immigrants in North America, such as the European corn borer, helped to elucidate chemical communi­ cation in insects (Cardé and Baker 1984) and shed light on their evolution (Roelofs et al. 2002). Even the red imported fire ant (Solenopsis invicta) has proven beneficial in some ways. A useful predator under certain conditions (Reagan 1986, Tschinkel 2006; cf. Eubanks et al. 2002), it provided insights into the evolution of social organization in insects (Ross and Keller 1995) and helped to shape the career of Edward O. Wilson (Wilson 1994), indirectly promoting studies in insect biodiversity.

21.6.2 Detrimental

Invasive species produce adverse socioeco­ nomic, environmental (ecological), and health effects. The problem can be viewed as involving economic as much as ecological issues (Evans 2003). In fact, ecological and economic impacts of invasive species probably are “highly corre­ lated” (Vilà et al. 2010). Economic costs can be direct, involving exclusion, eradication, control, and mitigation; or indirect, involving human health or alteration of communities and ecosys­ tems (Perrings et  al. 2005, McNeely 2001a). Indirect economic costs, which include ecosys­ tem services (Charles and Dukes 2007), are more difficult to calculate, often are not consid­ ered, and can overwhelm direct costs (Ranjan 2006). Seldom considered are both the eco­ nomic and environmental costs of using pesti­ cides to control (or manage) immigrant pests. Invasive species can act synergistically, their collective effects being greater than those of the species considered individually (Howarth 1985, Simberloff 1997). The red imported fire ant might facilitate the success of an immigrant mealybug (Antonina graminis) that uses the ant’s honeydew (Helms and Vinson 2002, 2003). Synergistic effects can facilitate the invasion itself, a community‐level process known as “invasional meltdown” (Simberloff and Von Holle 1999, Simberloff 2006). In the north‐­ central United States, European buckthorn (Rhamnus cathartica) and the soybean aphid (Aphis glycines) are key taxa in a meltdown that is proposed to involve multiple adventives, including an earthworm, a flatworm, other insects and plants, a phytopathogen, and a bird (Heimpel et al. 2010). Detecting ecological impacts of invasive spe­ cies and quantifying their effects on population dynamics of native species can be difficult, per­ haps more so in the case of insects because of their small size and complex, subtle, indirect effects (those involving more than two species) (Strauss 1991, White et al. 2006). Indirect effects of adventive insects can include unintended cascading effects that are unlikely to be

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predicted by risk analysis or revealed during pre‐release screening of biocontrol agents. Quantitative estimates of the probability of indirect effects cannot be made (Simberloff and Alexander 1998). Unintended consequences that affect biodiversity fall within the “externali­ ties” of economists (McNeely 1999, Perrings et al. 2000).

21.7 ­Economic Considerations: Agriculture, Forestry, and Horticulture Harm from invasive insects sometimes is con­ sidered only in terms of economic losses to agri­ culture, forestry, or horticulture: crop damage plus control costs. Costs of control may include only those borne by governments, with costs of private control omitted (US Congress 1993). The calculation of losses may fail to consider that they are dynamic, changing from year to year and by region (Schwartz and Klassen 1981). Crop losses, coupled with far‐reaching societal impacts, can be severe when an invasive insect threatens an industry: for example, grape phyl­ loxera (D. vitifoliae) and wine production in Europe (Pouget 1990, Campbell 2005), San Jose scale (Q. perniciosus) and deciduous fruit cul­ ture in California (Iranzo et al. 2003), and sugar­ cane delphacid (Perkinsiella saccharicida) and sugar production in Hawaii (DeBach 1974). Economics in relation to invasive insects encompasses more than is treated in many ento­ mological publications, for example, research and management costs (McLeod 2004). Consideration of the consequences of immi­ grant insects in the United States also should include the federal government’s procedures for their exclusion, which can entail substantial annual costs within the country and in the coun­ tries of origin (Wallner 1996). How the costs of preventing the introduction of an immigrant species compare with those that would have been caused by that species had it become estab­ lished represent a “great unknown” (Cox 1999).

21.7.1  Crop Losses

Aggregate costs of invasive species, including insects, seldom have been estimated on a national scale (Reinhardt et  al. 2003, Essl and Rabitsch 2004, Colautti et  al. 2006). The costs estimated by US Congress (1993) and Pimentel et al. (2001, 2005) are cited frequently. The cost of annual damage to US crops by invasive insects comes to nearly $16 billion (Pimentel et  al. 2001). Because Pimentel et al. (2000, 2001) dealt only with a subset of effects from invasive spe­ cies, they might have understated the problem (Lodge and Shrader‐Frechette 2003; cf. Theo­ doropoulos 2003: 116). Historical data on crop losses from insects in the United States include Walsh’s (1868) esti­ mate of $300 million. If, like Pimentel et  al. (2001), we assume that immigrant insects caused 40% of the losses in 1868, the damage would have amounted to about $120 million (~$4 billion in 2005 dollars based on Consumer Price Index). Sasscer (1940) estimated annual losses from insects (including costs for main­ taining research and quarantine facilities, loss of markets due to quarantines, and processing costs from insect damage) to be about $3 billion annually, with at least half resulting from immi­ grant species (~$20 billion in 2005 dollars). Estimated annual costs of invasive insects in agroecosystems of the Canadian Prairie prov­ inces are about $650 million (Dosdall et al. 2011). In Australia, immigrant insects cost an esti­ mated AU$4.7 billion between 1971 and 1995. In the United Kingdom, $960 million is lost annually due to arthropods. In New Zealand, crop damage and control costs for invertebrates, mainly insects, amount to NZ$437 million annually. And in South Africa, crop damage and control costs for arthropods add up to $1 billion each year (Pimentel 2002). Economic losses from individual species can be huge (Table 21.6). In 1927, the US Congress appropriated an unprecedented $10 million to conduct a clean‐up campaign to check further spread of the European corn borer (Ostrinia nubilalis) (Worthley 1928). For pests not as well

21  Adventive (Non-Native) Insects

Table 21.6  Some economic losses from invasive insects. Species

Description of loss*

Locality

Reference

Alfalfa weevil (Hypera postica)

$500 million, 1990

USA

Simberloff 2003b

Asian papaya fruit fly (Bactrocera papayae)

AU$100 million, 1990s

Queensland, Australia

Clarke et al. 2005

Boll weevil (Anthonomus grandis)

$15 billion, cumulatively since 1893

USA

Cox 1999, Myers and Hosking 2002

Codling moth (Cydia pomonella)

$10 million–15 million annually

USA

Gossard 1909

European corn borer (Ostrinia nubilalis)

$350 million, 1949

USA

Haeussler 1952

Formosan subterranean termite (Coptotermes formosanus)

$1 billion annually

USA

Pimentel et al. 2000

Hessian fly (Mayetiola destructor)

$40 million annually

USA

Gossard 1909

Mediterranean fruit fly (Ceratitis capitata)

$100 million, eradication 1982–3; losses to economy exceed projected $1.4 billion

California, USA

Kim 1983, Kiritani 2001

Melon fly, Oriental fruit fly (Bactrocera cucurbitae, Bactrocera dorsalis)

$250 million, eradication

Japan

Kiritani 2001

Mole crickets, Scapteriscus spp.

> $77 million annually, including control costs

Southeastern USA

Frank 1998

Pink hibiscus mealybug (Maconellicoccus hirsutus)

$125 million annually

Trinidad and Tobago

Ranjan 2006

Russian wheat aphid (Diuraphis noxia)

$500 million–900 million, through 1990s

USA

Foottit et al. 2006

Sheep blowfly (Lucilia cuprina)

AU$100 million annually

Australia

New 1994

Small hive beetle (Aethina tumida)

$3 million, 1998

USA

Hood 2004

*All losses are in US dollars unless otherwise noted; costs have not necessarily been documented by economists.

established as the corn borer, actual and pre­ dicted costs of eradication, as well as predicted losses, are impressive. Unsuccessful campaigns to eradicate the red imported fire ant from the southeastern United States cost more than $200 million (Buhs 2004).When the ant was detected in California in 1997, eradication costs were estimated at between about $4 billion and almost $10 billion (Jetter et al. 2002). Eradication programs often are controversial and unsuc­ cessful (e.g., Tschinkel 2006, Carey and Harder 2013), with costs underestimated and benefits overestimated (Myers et  al. 1998). Undesirable

consequences can include adverse effects on human health, death of wildlife, and reduction of arthropod natural enemies, leading to sec­ ondary‐pest outbreaks (Dreistadt et  al. 1990, Buhs 2004). Eradication, however, can be suc­ cessful (Simberloff 2003c) and provide great financial benefits (Klassen 1989, LeVeen 1989, Myers and Hosking 2002). Annual costs associ­ ated with the anticipated arrival of the Russian wheat aphid (Diuraphis noxia) in Australia might be as high as several million dollars (New 1994). Full costs to the US bee industry from invasion by the African honeybee (Apis mellifera

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scutellata) are not yet known (Schneider et  al. 2004), but prior to its arrival, they were esti­ mated at $26 million to $58 million for beekeep­ ing and another $93 million for crop losses due to reduced pollination (Winston 1992). Adventive phloem and wood borers account for greater economic losses than forest pests that are sap and foliage feeders (Aukema et al. 2011). Losses from the Asian long‐horned borer (A. glabripennis) in nine at‐risk US cities could range from $72 million to $2.3 billion and, if every urban area in the conterminous states became totally infested, might reach nearly $670 billion (Nowak et  al. 2001). The emerald ash borer (Agrilus planipennis), which is thought to pose nearly a $300 billion threat to US timberlands (Muirhead et al. 2006), already has killed tens of millions of ash trees and become the most economically important invader of US forests (Aukema et  al. 2011, Herms and McCullough 2014, Klooster et  al. 2014). Canada could be severely affected by the Asian long‐horned borer, as well as the brown spruce longhorn beetle (Tetropium fuscum) (Colautti et al. 2006). An analysis indicating that the Asian long‐horned borer’s introduction into Europe would pose a significant threat was in press (MacLeod et al. 2002) when the beetle was detected in Austria (Tomiczek and Krehan 2001). In Italy, the recent establishment of a congener, Anoplophora chinensis, has resulted in annual control costs (2004–8) of €0.53 mil­ lion (€1 = ~US$1.21) (Vilà et al. 2010). 21.7.2  Plant Diseases and Transmission of Pathogens

Immigrant herbivores become problematic by feeding on economically important plants, but they also have indirect effects, such as the trans­ mission of viruses and other phytopathogens. The role of the European elm bark beetle (Scolytus multistriatus) in spreading Dutch elm disease in North America is well known (Sinclair and Lyon 2005). With millions of disease‐­ susceptible American elms (Ulmus americana) having been planted and a competent immigrant

vector already established (a native bark beetle is a less efficient vector; Sinclair 1978b), condi­ tions were favorable for disease outbreak when the fungal pathogen arrived from Europe. By the mid‐1970s, about 56% of urban American elms had died (Owen and Lownsbery 1989). Dutch elm disease has had the greatest societal impact of all insect‐related tree diseases of urban areas (Campana 1983); cumulative economic losses have amounted to billions of dollars (Sinclair 1978a). Although often considered an urban problem, this disease also affects plant and ani­ mal composition in forests (Sinclair 1978a, Campana 1983). The banded elm bark beetle (Scolytus schevyrewi), which was detected recently in western states, might exacerbate problems from Dutch elm disease in North America (Negrón et  al. 2005). A serious prob­ lem of eastern North American forests is beech bark disease, involving American beech (Fagus grandifolia), a Palearctic scale insect (Crypto­ coccus fagisuga) detected in Nova Scotia in about 1890 (Ehrlich 1934), and nectria fungi (formerly Nectria spp. but now placed in other genera; Rossman et  al. 1999). Feeding by the scale insect allows fungi that are unable to infect intact bark to invade injured areas. The disease not only kills beech trees, thereby altering the composition of eastern forests and reducing their commercial and recreational use, but is also likely to have cascading, adverse effects on other members of the forest ecosystem (Sinclair and Lyon 2005, Storer et  al. 2005, Cale et al. 2013). Other immigrant insects that transmit phy­ topathogens are agriculturally and horticultur­ ally important. A Nearctic leafhopper (Scaphoideus titanus) that apparently was shipped with grapevine material to the Palearctic Region serves as the principal vector of a phyto­ plasma disease (flavescence dorée) of cultivated grapes in Europe (Lessio and Alma 2004, Bressan et al. 2005). A recent (2000) immigrant, the soybean aphid (A. glycines), quickly became the most important insect pest of US soybean production (Rodas and O’Neil 2006); this Asian native transmits (or is suspected to transmit)

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several plant viruses in North America (Heimpel et al. 2004, Damsteegt et al. 2005). Another Old World aphid (Toxoptera citricida) transmits the virus that causes citrus tristeza. The disease, although present in Venezuela by 1960, did not threaten the citrus industry until the aphid arrived. By the mid‐1980s, the disease had dev­ astated the country’s citrus culture (Lee and Rocha‐Peña 1992). Whiteflies of the Bemisia tabaci species complex, which are transported with commerce throughout much of the world (Oliveira et  al. 2001, Perring 2001), transmit several geminiviruses (Czosnek et  al. 2001). In  the 1980s, the western flower thrips (Frankliniella occidentalis), which is native to the southwestern United States, assumed near cosmopolitan distribution due to global trade in greenhouse plants. By emerging as the main vector of the tospovirus that causes tomato spotted wilt, it induced disease epidemics (Ullman et al. 1997, Morse and Hoddle 2006). Immigrant insects also transmit pathogens to native plants of ecological value but little or no economic importance. A recently detected Asian ambrosia beetle (Xyleborus glabratus) transmits a fungal pathogen that is responsible for extensive mortality of native redbay (Persea borbonia), thus threatening to extirpate this tree from coastal forest ecosystems of the southeast­ ern United States (Evans et al. 2014). Immigrant aphids may vector viruses of native Hawaiian plants, including precinctive species (Messing et al. 2007).

21.8 ­Implications for Animal and Human Health Immigrant insects of veterinary importance serve as vectors of disease organisms and other­ wise affect productivity or harm domestic and companion animals. Annual losses from long‐ established species affecting US livestock include nearly $1 billion (Castiglioni and Bicudo 2005) for the horn fly (Haematobia irritans) (losses are nearly Can$70 million in Canada; Colautti et  al. 2006). The stable fly (Stomoxys

calcitrans), which has long been a pest of cattle in midwestern US feedlots, now affects range cattle. When pest numbers are high, daily decreases in weight gain can be nearly 0.23 kg per head (Hogsette 2003, Campbell 2006). The stable fly and other synanthropic Diptera are nuisance insects that affect the US tourist indus­ try (Merritt et  al. 1983). In Australia, annual production losses and treatment costs due to the sheep blowfly (Lucilia cuprina), an immi­ grant ectoparasite that is responsible for cuta­ neous myiasis (flystrike) in sheep (Levot 1995), amount to more than AU$160 million (McLeod 1995). Costs associated with the loss of wildlife as the result of immigrant insects are more diffi­ cult to express monetarily than those for domes­ tic animals. Avian malaria, although present in Hawaii, did not seriously affect the native avi­ fauna until a competent vector was in place. Following the establishment of a mosquito (Culex quinquefasciatus) in lowland areas of Maui by the early 19th century, malaria and avian pox became epidemic, which led to many native birds, especially honeycreepers, becom­ ing endangered or extinct (Warner 1968, Jarvi et  al. 2001; cf. van Riper et  al. 1986). Disease resistance, however, might be evolving in cer­ tain Hawaiian forest birds (Woodworth et  al. 2005, Strauss et al. 2006). An immigrant muscid fly (Philornis downsi) recently was detected on the Galápagos archipelago. This obligate ectoparasite of birds apparently has killed nest­ lings on the islands and could threaten Darwin’s finches (Fessl and Tebbich 2002). Costs associated with human diseases trans­ mitted by immigrant insects can be estimated (Gratz et al. 2000), as was done in Australia for dengue infections after the yellow fever mos­ quito (Aedes aegypti) became established (Canyon et  al. 2002). The impact of invasive insects on human health, however, cannot be expressed adequately in monetary terms. At least five immigrant insects associated with vec­ tor‐borne diseases helped to shape South Carolina’s culture and history (Adler and Wills 2003).

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Medical effects from invasive insects include mild skin reactions (pruritus and urticaria) from contact with brown‐tail moth or gypsy moth lar­ vae (Allen et  al. 1991, Mullen 2002), reactions from exposure to allergens of immigrant cock­ roaches (Peterson and Shurdut 1999), and life‐ threatening envenomation and hypersensitive reactions from adventive hymenopterans such as the honeybee, red imported fire ant, and other ant species (Akre and Reed 2002, Klotz et  al. 2005, Nelder et al. 2006). Effects on humans are catastrophic when immigrant insects serve as vectors of diseases that cause widespread mor­ tality (Cartwright 1972, Vitousek et al. 1997). In 14th‐century Europe, following introductions of the black rat (Rattus rattus) and oriental rat flea (Xenopsylla chaeopis), about 25 million people were killed by plague in a pandemic often called the Black Death (Cartwright 1972, Cloudsley‐ Thompson 1976, Laird 1989). A mid‐17th‐­ century immigrant to the western hemisphere was the yellow fever mosquito (A. aegypti), which arrived in the Caribbean with ships bear­ ing Africans for the slave trade and became a notorious vector of viruses that cause dengue and yellow fever (Bryan 1999). Throughout human history, immigrant insects have trans­ mitted agents responsible for major diseases (Cloudsley‐Thompson 1976, Lounibos 2002). With the advent of air travel in the 1920s, air­ planes became important transporters of mos­ quitoes, which could serve as disease vectors in new areas (Gratz et al. 2000). Disease outbreaks most often result from independent introduc­ tions of vector species and pathogens (Juliano and Lounibos 2005). Mosquito species arriving by ship are more likely to become established than those moved by aircraft (Lounibos 2002). The establishment of an immigrant mosquito (Anopheles gambiae s.l.) in Brazil during the 1930s led to epidemic malaria, imposing great socioeconomic burden on the country (Killeen et al. 2002, Levine et al. 2004). Eradication of the mosquito from northeastern Brazil, which was rapid and unexpected, ended the severe epi­ demics (Davis and Garcia 1989). A relatively recent global invader, the Asian tiger mosquito

(Aedes albopictus) can transmit arboviruses such as dengue and chikungunya (Gratz 2004). This mosquito has become established on five continents since the late 1970s (Adler and Wills 2003, Aranda et al. 2006). In some regions, the Asian tiger mosquito has displaced an immi­ grant congener, A. aegypti (Juliano 1998, Reitz and Trumble 2002, Juliano et  al. 2004, Bagny Beilhe et  al. 2012), although continental US populations of the latter species had been declining prior to the arrival of A. albopictus (Rai 1991). In New Jersey, A. albopictus has par­ tially displaced a native congener, Aedes seriatus (Rochlin et al. 2013), which is the main vector of La Crosse virus (Jackson et  al. 2012). An East Asian mosquito (Ochlerotatus japonicus) was first collected in the Western Hemisphere in 1998 in the northeastern United States (Peyton et al. 1999). This public‐health threat has spread to the southeastern states (Reeves and Korecki 2004), west coast (Sames and Pehling 2005), and  southern Canada (Darsie and Ward 2005),  and has become established in Hawaii (Larish and Savage 2005) and continental Europe (Medlock et al. 2005). It is a competent laboratory vector of West Nile virus (and a potential vector of others), and the virus has been detected in field‐collected specimens (Andreadis et al. 2001, Turell et al. 2001). The world might be entering another (fourth) transition in the history of human diseases, one characterized by ecological change rather than contact among human populations (Baskin 1999). Insects moved in commerce promise to have crucial roles in additional changes in the patterns of vector‐borne diseases, with global climate change likely to affect disease incidence and distribution (Greer and Fisman, 2008). The toll of vector‐borne diseases, in addition to loss of life, impaired health, and socioeco­ nomic consequences, includes environmental effects such as the draining and oiling of US wetlands to reduce mosquito populations and malaria (Adler and Wills 2003). Similarly, wet­ lands in other countries long have been drained, but the restoration of wetlands or construction of new ones has become more common with

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realization of the need to conserve biodiversity (Schäfer et al. 2004).

21.9 ­Ecological Impacts Whereas there has been a long‐standing interest in calculating economic losses due to invasive species, only recently have ecological costs begun to be assessed (With 2002). Environmental effects of immigrant insects are difficult to dis­ cern and estimate (Simberloff 1996, Binggeli 2003, Vilà et  al. 2010), and perhaps are being overlooked (Kenis 2005), due, in part, to an overemphasis on extinction in the popular press (US Congress 1993). However, only a “small minority” of adventive species seems to be affecting native species (Simberloff and Von Holle 1999). Of 81 adventive heteropterans recorded from Canada, only one species might be causing environmental harm (Scudder and Foottit 2006). Despite their diversity, insects are said not to show “high potential” for causing environmental harm (Wittenberg 2005). Although adventive insects probably damage the environment less than pathogens, plants, and mammals do (Simberloff 2003b), the direct and indirect ecological effects of immigrant insects on eastern North American forests (Liebhold et  al. 1995, Cox 1999, Gandhi and Herms 2010a, Herms and McCullough 2014) alone seem sufficient to negate Wittenberg’s (2005) statement. Moreover, immigrant oak‐ associated herbivores, although not economi­ cally important, could adversely affect western oak (Quercus garryana) meadows in British Columbia (Gillespie 2001). Simberloff’s (2003b) comment, therefore, seems more appropriate: “Relative to the numbers of species introduced, insects rarely cause enormous ecological (as opposed to economic) damage.” A broadening of the definition of “ecosystem impact” to include not only effects on nutrient cycling and energy flow but also substantial changes in species abundance and composition, processes such as disturbance cycles, and various structural habi­ tat changes might reveal that ecosystem impacts

exceed the level that generally is recognized (Simberloff 2011a). As underlying mechanisms for adverse effects, ranging from individual to ecosystem levels, competition and predation generally are considered more important in insects than hybridization (Rhymer and Simberloff 1996, National Research Council 2002), with interfer­ ence competition more easily demonstrated than resource competition (Simberloff 1997, 2000a). Hybridization and introgression, though apparently uncommon in insects (Dowling and Secor 1997), occur in certain species of Drosophila (Mallet 2005), subspecies of the honeybee (Sheppard 1989, Schneider et  al. 2006, Kenis et  al. 2009), between the red imported fire ant (S. invicta) and an immigrant congener (Solenopsis richteri) in a portion of their US range (Tschinkel 2006), and occasion­ ally between the European winter moth (O. bru­ mata) and the native Operophthera bruceata (Elkinton et  al. 2014). Establishment of the Asian gypsy moth in North America and its possible hybridization with the European form are causes for concern (Cox 2004). Hybridization and genetic disruption between an immigrant and an endemic tiger beetle (Cicindela spp.) might be taking place in the Galápagos Islands (Causton et al. 2006). Moreover, multiple immi­ grations of pest insects enhance genetic diver­ sity (Tschinkel 2006) and potentially create more virulent biotypes (Lattin and Oman 1983, Whitehead and Wheeler 1990). Further use of molecular techniques to quantify gene flow between adventive and native insects is a press­ ing need (Kenis et al. 2009). Environmental effects suggested for invasive insects often are based on anecdotal rather than quantified data. For example, scarab beetles released to help remove cattle dung might com­ pete with native beetles (Thomas 2002). In Hawaii, the beetles are eaten by mongooses (Herpestes javanicus), perhaps allowing these generalist carnivores to maintain larger‐than‐ normal densities (Howarth 1985). The ill‐ advised biocontrol release of the mongoose to suppress rat populations in Hawaii, and this

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carnivore’s adverse effects on native birds, is well documented (van Riper and Scott 2001). Insects seem not to alter fire regimes as do some invasive plants (D’Antonio and Vitousek 1992, D’Antonio 2000), although an immigrant cer­ ambycid (Phoracantha semipunctata) might create a fire hazard in California by killing euca­ lyptus trees (Dowell and Gill 1989). Inferences on species interactions may fail to consider alternative hypotheses for explaining putative effects (Simberloff 1981); correlation does not establish causation (Williamson 1996, Simberloff 1997). Evidence, however, increases for a causal relationship between the North American establishment of adventive lady beetles, such as Coccinella septempunctata and Harmonia axyridis (e.g., Wheeler and Hoebeke 1995, Michaud 2002, Turnock et  al. 2003, Alyokhin and Sewell 2004, Evans 2004, Day and Tatman 2006, Harmon et  al. 2007), and the decline of native coccinellids. Moreover, the use of defensive compounds (exogenous alkaloids) in larvae of H. axyridis to track intraguild pre­ dation supports the hypothesis that this coc­ cinellid’s establishment in Europe has led to the decline of native aphidophagous coccinellids (Hautier et al. 2011), as do systematic surveys of lady‐beetle abundance in Belgium, the United Kingdom, and Switzerland (Roy et al. 2012). Assessing the proximate and ultimate causes of declines in imperiled native species, which likely are subject to multiple threats, is difficult, as is evaluating the threats and their relative importance (Gurevitch and Padilla 2004). As Tschinkel (2006) emphasized for immigrant ants, few studies in which competitive displace­ ment is claimed actually were designed to meas­ ure such an effect. The examples of the environmental effects of adventive insects pre­ sented below vary in scientific rigor. Eurasian phytophagous insects in North America tend to colonize the same genera (and often the same species) that they do in the Old World and might not have been able to become established without the presence of their native (or closely related) hosts in the New World (Mattson et al. 1994, Niemalä and Mattson 1996,

Frank 2002, Langor et  al. 2009). Species of Eucalyptus, planted in North America since the 1800s, were available for late 20th century coloni­ zation by specialized immigrant herbivores (Paine and Millar 2002). Certain immigrants have been found in the Nearctic Region only on Palearctic hosts. Examples include plant bugs (Miridae) and jumping plant lice (Psyllidae) on European ash (Fraxinus excelsior) (Wheeler and Henry 1992, Wheeler and Hoebeke 2004) and a psyllid (Livilla variegata) on ornamental laburnums (Laburnum spp.) (Wheeler and Hoebeke 2005). Two Pal­ earctic seed bugs are restricted in North America to cosmopolitan and pantropical cattails (Typha spp.) (Wheeler 2002). Even if these specialized phytophages expand their host ranges in North America, they are unlikely to cause environmen­ tal harm. In other cases, Eurasian plants serve as alternative hosts of recently established immi­ grant insects that become crop pests, for instance, the Russian wheat aphid (D. noxia) (Kindler and Springer 1989). Other immigrant phytophages also are not benign faunal additions. Direct feeding by immigrant insects in Hawaii imperils plants of  special concern (Howarth 1985). In the Galápagos Islands, the cottony cushion scale (Icerya purchasi) killed endangered plants and, in turn, apparently caused local extirpation of certain host‐specific lepidopterans (Causton et al. 2006). A Mexican weevil (Metamasius cal­ lizona) detected in Florida in 1989 feeds on introduced ornamental bromeliads and kills native epiphytic bromeliads (Tillandsia spp.) that are protected by law. Destruction of native bromeliads also destroys the invertebrate inhab­ itants of water impounded in leaf axils (phy­ totelmata) on the plants (Frank and Thomas 1994, Frank and Fish 2008). Immigrant phytophages can threaten not only novel host plants but also their naive natural enemies. The glassy‐winged sharpshooter (Homalodisca coagulata), which was detected in French Polynesia in 1999, developed atypi­ cally large populations but did not adversely affect the new hosts on which it fed or affect them indirectly by transmitting the bacterium

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Xylella fastidiosa. Instead, the effects of the leafhopper’s arrival were seen at higher trophic levels: a lethal intoxication of its spider preda­ tors. The cause of mortality is unknown but might involve the leafhopper’s bacterial endo­ symbionts. By using lethal allelochemicals against spiders, H. coagulata might alter the structure and species composition of food webs in the South Pacific (Suttle and Hoddle 2006). Adventive insects also can serve as “evolution­ ary traps” for natural enemies when native para­ sitoids accept hosts that are unsuitable for their development (Abram et  al. 2014). Indirect effects of insect invaders of North American forests, such as the gypsy moth, might lower parasitoid diversity (and alter forest insect food webs), but substantial indirect effects have not been demonstrated (Timms et al. 2012). 21.9.1 Ants

Ants are among the more spectacular of inva­ sive organisms (Moller 1996); several hundred species have been or are being moved in global trade (McGlynn 1999, Suarez et al. 2005, Ward et al. 2006). The species most readily moved in commerce  –  “tramp species” (Passera 1994)  – afford opportunities for behavioral, ecological, and evolutionary studies relevant to conserva­ tion and agriculture. Immigrant ants not only reduce biodiversity but also can disrupt the bio­ logical control of plant pests (Coppler et  al. 2007) and disassemble native ant communities (Sanders et al. 2003). Immigrant ants’ competi­ tive displacement of native species often is reported, but, at best, is hard to document (e.g., Krushelnycky et al. 2005). The effects of immi­ grant ants on ant–plant mutualisms warrant more study (Holway et  al. 2002, Ness and Bronstein 2004). Ants’ mutualistic tending of aphids and scale insects can protect pest spe­ cies, increasing their densities and damage, and deterring predation by natural enemies (Kaplan and Eubanks 2002, Hill et  al. 2003, Jahn et  al. 2003). Immigrant ants, in turn, sometimes are replaced by later‐arriving ant species (Simberloff 1981, Moller 1996, LeBrun et  al. 2013), a

phenomenon seen among immigrants in other insect groups and biocontrol agents (Ehler and Hall 1982, Reitz and Trumble 2002, Snyder and Evans 2006; cf. Keller 1984). The red imported fire ant (S. invicta) adversely affects various invertebrate and vertebrate groups (Porter and Savignano 1990; Vinson 1994, 1997). Recent reviews of the causes and consequences of ant invasions (Holway et  al. 2002) and various detrimental effects of the red imported fire ant (Tschinkel 2006, Vinson 2013) provide information and references beyond those we mention here. Immigrant ants can affect seed dispersal and pollination, processes that are crucial to plant reproductive success. By removing seeds, red imported fire ants are potential threats to spring herbs (e.g., Trillium spp.) in deciduous forests of the southeastern United States (Zettler et  al. 2001), but in some cases fire ants might facili­ tate seed dispersal of native plants (Stuble et al. 2010). In the Cape fynbos flora of South Africa, the Argentine ant (Linepithema humile) has dis­ placed native ants associated with certain pre­ cinctive proteaceous plants (myrmecochores) whose seeds are ant dispersed. Argentine ants are slower to discover the seeds, move them only short distances, and eat the elaiosomes without burying the seeds in subterranean nests, as native ants do. Exposed seeds are vul­ nerable to predation and desiccation. Plant community composition might change as a result of reduced seedling recruitment (Bond and Slingsby 1984, Giliomee 1986). Because the two native ant species displaced by Argentine ants are more effective dispersers of large‐ seeded Proteaceae than are the two coexisting native species, the fynbos shrubland commu­ nity might shift toward smaller‐seeded species (Christian 2001). Displacement of native ants in Australia involves interference competition by Argentine ants (Rowles and O’Dowd 2007). Argentine ants also deter insect visitation to flowers of certain fynbos proteas (Protea nitida) (Visser et al. 1996), reduce the fruit‐ and seed‐ set of a euphorbiaceous shrub (Euphorbia char­ acias) in Spain (Blancafort and Gómez 2005)

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and generally threaten myrmecochory in the Mediterranean biome (Gómez and Oliveras 2003), pose a threat to precinctive plants in Hawaii by reducing their pollinators and plant reproduction (Loope and Medeiros 1994, 1995; Cox 1999), and might be reducing prey (e.g., caterpillars) available to insectivorous birds in Spain (Estany‐Tigerström et al. 2010). The long‐ legged or yellow crazy ant (Anoplolepis gracili­ pes) has had severe direct and indirect effects on Christmas Island, killing an estimated 10 mil­ lion to 15 million red crabs (Gecarcoidea nata­ lis) and eliminating populations of this keystone species, which regulates seedling recruitment, composition of seedling species, litter break­ down, and density of litter invertebrates. The crab’s elimination has long‐term implications for forest composition and structure. The ant’s mutualism with honeydew‐producing homop­ terans further disrupts the rainforest ecosystem (O’Dowd et  al. 2003, Green et  al. 2004). Anoplolepis gracilipes was first detected in the Seychelles in the 1960s, and has begun to affect biodiversity on the archipelago’s Bird Island since being discovered there in the 1980s (Gerlach 2004). Other immigrant ants (Williams 1994) can cause adverse environmental effects, including the bigheaded ant (Pheidole mega­ cephala) in Hawaii (Jahn and Beardsley 1994, Asquith 1995) and other Pacific islands (Wetterer 2007), the little fire ant (Wasmannia auropunctata) in the Galápagos Islands (Lubin 1984), and the Asian needle ant (Pachycondyla chinensis) in the southeastern United States (Rodriguez‐Cabal et al. 2012). 21.9.2  Bees and Wasps

Non‐social bees that are immigrants in North America have not adversely affected native bees (Cane 2003), but the recent establishment in Florida of an oil bee (Centris nitida), a special­ ized pollinator (oligolege) of a threatened native oil plant, might disrupt the plant’s mutualism with a native congeneric bee (Downing and Liu 2012). Another solitary bee, the Old World Anthidium manicatum, is now established in

North America, South America, New Zealand, and the Canary Islands. This aggressive mega­ chilid tends to be synanthropic but could have adverse effects on native bees if it spreads to novel environments (Strange et al. 2011). The introduced honeybee, a social and poly­ lectic (generalist pollinator) species, might affect native ecosystems by competing for floral resources with native bees and disrupting the pollination of native plants (e.g., Gross and Mackay 1998, Spira 2001, Dupont et  al. 2004). Although harmful effects on native flower visi­ tors have been attributed to honeybees, particu­ larly those of the Africanized honeybee on native pollination systems (Santos et  al. 2012), better experimental data and longer studies generally are needed to support the claims (Butz Huryn 1997, Kearns et al. 1998, Goulson 2003, Moritz et  al. 2005). As principal pollinators of invasive plants, honeybees also can enhance the fruit set, thus facilitating invasiveness (Goulson and Derwent 2004). Caution should be exer­ cised before introducing social bees that have become invasive elsewhere: for example, the introduction of a bumblebee (Bombus terrestris) into mainland Australia, when it is highly invasive on the Australian island of Tasmania (Hingston 2006). Immigrant wasps and yellowjackets have been implicated in detrimental ecological effects. One example is the western yellowjacket (Vespula pensylvanica) in Hawaii, which preys on native arthropods, reducing their densities and threatening arthropods of Maui’s native ecosystems (Gambino et  al. 1990, Asquith 1995). In New Zealand beech (Nothofagus) for­ ests, two yellowjackets (Vespula germanica and Vespula vulgaris) restructure invertebrate com­ munities through predation and competition, and compete with the precinctive kaka parrot (Nestor meridionalis) by harvesting honeydew from margarodid scale insects (Ultracoelostoma spp.), thereby limiting the birds’ reproductive success (Beggs and Wilson 1991, Beggs et  al. 1998, Beggs and Rees 1999). Another example is the paper wasp Polistes versicolor, which feeds mainly on lepidopteran larvae in the Galápagos

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Islands and competes for food with native verte­ brates such as finches (Causton et al. 2006). 21.9.3  Forest Pests

Forest insects were moved to distant lands via steamships in the mid‐19th century (Sailer 1983, Wheeler and Hoebeke 2001) and are being transported to all major continents (Ciesla 1993, Britton and Sun 2002, Kenis et al. 2007) in the current era of containerized shipping (Aukema et  al. 2010, Liebhold et  al. 2012). Adventive insects that alter forest ecosystems in eastern North America are immigrants except for the European gypsy moth, which was introduced into Massachusetts in the hope of crossing the moth with native silkworms to produce a disease‐­resistant strain for the US silk industry (Spear 2005). Gypsy moth defoliation of oaks (Quercus spp.) and its suppression by applica­ tions of the insecticide Bacillus thuringiensis have changed forest stand composition; increased nest predation of songbirds; decreased mast (acorn) production, resulting in declines of small mammals and changes in foraging pat­ terns of bear and deer; and decreased lepidop­ teran populations (Liebhold et al. 1995, Wallner 1996). Cascading effects of this eruptive pest encompass interactions among mast produc­ tion, mice, deer, and ticks that, in turn, affect the incidence of Lyme disease (Elkington et al. 1996, Jones et  al. 1998, Liebhold et  al. 2000). The gypsy moth’s sociological impact – on environ­ mental aesthetic quality and recreational and residential values – might be even greater than its environmental effects (Liebhold et al. 1995). An immigrant aphidoid, the balsam woolly adelgid (Adelges piceae), affects balsam fir (Abies balsamea) forests in the northeastern United States and has nearly eliminated old‐growth Fraser fir (Abies fraseri) in the spruce‐fir ecosys­ tem of the southern Appalachians (Jenkins 2003, Potter et  al. 2005). The hemlock woolly adelgid (Adelges tsugae) spread from landscape plantings to native stands of eastern hemlock (Tsuga canadensis) in the late 1980s (Hain 2005). This immigrant has caused significant mortality

in New England forests, shifting nutrient cycling, composition and structure, and imper­ iling species that are important culturally, eco­ nomically, and ecologically (Jenkins et al. 1999, Small et al. 2005, Stadler et al. 2005). The effects of hemlock’s decline might extend to long‐term effects in headwater stream ecosystems (Snyder et al. 2005). A. tsugae threatens eastern hemlock and Carolina hemlock (Tsuga caroliniana) in the southern Appalachians (Graham et al. 2005); adelgid‐induced mortality in the central and southern Appalachians might allow hardwood communities to replace hemlock forests (Spaulding and Rieske 2010). Widespread mor­ tality of ash trees caused by the emerald ash borer (A. planipennis) would have detrimental effects on Fraxinus‐specialist herbivores equiv­ alent to those on insects that depended on chestnut (Castanea dentata) before the demise of that tree species in North America (Gandhi and Herms 2010b). This immigrant buprestid beetle already has had substantial indirect effects on ecosystem processes in North American forests (Flower et al. 2013, Herms and McCullough 2014) and might have similar effects in Europe as it spreads west from European Russia (Orlova‐Bienkowskaja 2014).

21.10 ­Biological Control That invasion biology and classical biological control are linked has been pointed out by numerous workers (e.g., Ehler 1998, Strong and Pemberton 2000, Fagan et  al. 2002). Biological control once was considered to lack environ­ mental risk (DeBach 1974), and as recently as  the early 1980s was not discussed among numerous causes of declines in insect popula­ tions (Pyle et  al. 1981). Evidence for adverse effects of natural enemies, however, had long been available (Howarth 2000), and concern over their unforeseen effects had been expressed at least since the 1980s (Perkins 1987, Spear 2005: 260). During the 1980s, biocontrol began to be crit­ icized by conservationists for its irreversibility

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and possible adverse effects on non‐target plants and insects (Howarth 1983, 1985). Adverse effects in some cases had been antici­ pated but considered unimportant because the most vulnerable native plants lacked economic value (McFadyen 1998, Seier 2005). A concern for organisms of no immediate or known human benefit “provoked a revolution in the field of biological control that has continued … and has yet to be resolved” (Lockwood 2000). Follett and Duan (2000) reviewed the problem of unintended effects from both biocontrol and conservationist perspectives. Indirect ecologi­ cal effects of biocontrol were the focus of Wajnberg et al. (2001). Louda et al. (2003) dis­ cussed case histories of problematic biocontrol projects: three involving herbivores used to sup­ press weeds and seven with parasitoids or pred­ ators used against other insects. Negative ecological effects of parasitoids generally have been less than for predators (Onstad and McManus 1996). Among the conclusions of Louda et  al. (2003) was that North American redistribution of an inadvertently established (immigrant) weevil (Larinus planus) to control Canada thistle (Cirsium arvense) is having major non‐target impact on a native thistle (Cirsium undulatum var. tracyi). Effects from releases of a flower‐head weevil (Rhinocyllus conicus) against carduine thistles were consid­ ered severe in western states, especially in rela­ tion to densities of the native Platte thistle (Cirsium canescens). More recently, R. conicus has been shown to have detrimental, non‐target effects on a native herbivore, the tephritid fly Paracantha culta, on flower heads of Platte this­ tle (Louda et al. 2011). Cactoblastis cactorum, a pyralid moth released against prickly pear (Opuntia spp.) in the West Indies, might enhance the risk of extinction of a rare cactus (O. corallicola) in Florida. The moth arrived in Florida via immigration or introduction (Frank et al.1997, Johnson and Stiling 1998), eventually threatening cacti native to the southwestern states and Mexico (Bloem et al. 2005). A tachi­ nid (Compsilura concinnata) used against the gypsy moth could have long‐term effects on

Nearctic silk moths and might cause local extir­ pation. And parasitoids released to control the southern green stink bug (Nezara viridula) in Hawaii might be accelerating a decline of koa bug (Coleotichus blackburniae) populations, and could cause its extinction (Louda et al. 2003). Certain non‐target effects from well‐screened insects used in biocontrol can be considered trivial from a population perspective (Messing and Wright 2006). “Spillovers” onto nearby non‐ target plants that are associated with weed bio­ control agents at high population densities do not represent host shifts (Blossey et  al. 2001); the injury can be considered non‐target feeding rather than impact (van Lenteren et  al. 2006). The slight foliar injury on a native willow (Salix interior) by adult leaf beetles (Galerucella spp.) used against purple loosestrife (Lythrum sali­ caria) in North America actually had been pre­ dicted during pre‐release testing and should be regarded as “verification of science done well” (Wiedenmann 2005). Most biocontrol projects for insect (Lynch and Thomas 2000, van Lenteren 2006) and weed (Fowler et  al. 2000, Gould and DeLoach 2002) suppression are thought to produce slight or inconsequential effects on non‐target organ­ isms, although post‐release monitoring for adverse effects typically has not been done or has been minimal (McFadyen 1998, Hajek 2004). Host‐specific species traditionally have been chosen for weed control because of the threat that released herbivores pose to crop plants (Waage 2001, Hajek 2004). Host‐range testing of biocontrol agents used against insects has been less rigorous than for weeds (Van Driesche and Hoddle 2000, van Lenteren et al. 2006) and can be constrained by an inadequate ecological and taxonomic knowledge of native insects (Barratt et  al. 2003). Behavioral factors can complicate tests for non‐target hosts among insects used in arthropod biocontrol (Messing and Wright 2006), and the complex effects of generalist predators on other species of a com­ munity – beneficial or detrimental – are unpre­ dictable (Snyder and Evans 2006). Predators and parasitoids once were not subject to as thorough

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host‐range testing as weed agents, but the use of generalist natural enemies now is less common (Sands and Van Driesche 2003, Hajek 2004). Inundative biological control, involving the mass rearing and release of natural enemies, has shown fewer adverse ecological effects than classical biocontrol. Permanent establishment of natural enemies to achieve long‐term pest management is not the goal of inundation. Even though inundative biocontrol lacks the irrevers­ ibility of classical biocontrol, its use still can produce negative effects on non‐target species and ecosystems. Guidelines have been devel­ oped to minimize such risks (van Lenteren et al. 2003). Biological control, properly conducted and carefully regulated, can be an ally of agriculture and conservation (Hoddle 2004, Hajek 2004, Messing and Wright 2006; cf. Louda and Stiling 2004). Adventive organisms used in classical biological control still add to biotic homogeni­ zation (e.g., Louda et al. 1997) and can be con­ sidered intentional biotic contaminants (Samways 1988, 1997) whose release has moral implications (Lockwood 2001). Released agents can spread to adjacent regions and neighboring countries (Fowler et  al. 2000, Henneman and Memmott 2001, Louda and Stiling 2004). Predicting the impact of candidate biocontrol agents on target species remains problematic (Hopper 2001, Lonsdale et  al. 2001). Roitberg (2000) suggested that biocontrol practitioners incorporate concepts of evolutionary ecology, advocating collaboration with evolutionary biologists who study behavioral plasticity so that the variables most likely to determine whether candidate natural enemies would harm non‐target hosts can be identified. Even rigor­ ous host‐specificity tests of biocontrol agents (and pest‐risk analyses of adventive species) cannot be expected to predict all unintended effects that might disrupt communities and eco­ systems (Pemberton 2000, Hoddle 2003). Almost nothing is known about the micro­ sporidia that biocontrol agents of weeds might carry and their potential adverse effects (Samways 1997). Indirect effects essentially are

unavoidable in multispecies communities (Holt and Hochberg 2001). Because of documented direct and indirect (including cascading) effects on non‐target organisms, a cautious approach to biocontrol is warranted (Howarth 1991, Follett and Duan 2000, Wajnberg et  al. 2001). Classical biological control is a complex disci­ pline that evokes controversy (Osborne and Cuda 2003). Even careful consideration of per­ ceived benefits and risks of a proposed project will not satisfy all who might be affected: bio­ control specialists, conservationists, regulatory officials, policymakers, and the general public. The stochastic nature of biological systems is exemplified by the recent discovery of human‐ health implications arising from a seemingly straightforward biocontrol project: release of seed‐head flies (Urophora spp.) to suppress spotted knapweed (Centaurea stoebe ssp. micranthos [= biebersteinii, maculosa of authors]) in rangelands of western North America. The flies, released in the 1970s, prolif­ erated but did not curtail spread of the weed. Ineffective biocontrol agents such as Urophora (Myers 2000) can become abundant and pose greater risks of non‐target effects than agents that effectively control target organisms (Holt and Hochberg 2001). Although the tephritids have not directly harmed non‐target plants (the host‐specific flies have remained on target), their larvae provide a winter food source for deer mice (Peromyscus maniculus) when little other food is available. The mice climb knap­ weed stalks to forage above the snow cover. Food subsidies thus have allowed densities of deer mice, the primary reservoirs of Sin Nombre hantavirus, to increase by as much as threefold. Blood samples from mice showed that seroposi­ tive individuals were three times more numer­ ous when flies were present. Increased densities of seropositive mice might alter hantavirus ecol­ ogy, increasing the risk of virus infections in humans (Pearson and Callaway 2006). Spectacular early successes in biological control, such as the suppression of cottony cushion scale in California through importation of the vedalia beetle (Rodolia cardinalis) from

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Australia (Caltagirone and Doutt 1989), and the suppression of prickly‐pear cactus (Opuntia spp.) by various insects (DeLoach 1997), gave way to realism: that similar successes would not come as easily. Dunlap (1980) noted that L. O. Howard referred to introducing insects into a new environment as being “infinitely more complicated than we supposed 20 years ago” (Howard 1930). Some 85 years later, Howard’s comment, referring specifically to parasitoids, applies generally to the uncertain behavior of adventive insects in novel environments (e.g., Henry and Wells 2007).

21.11 ­Biological Invasions and Global Climate Change Ecologists have been aware that biological inva­ sions and climate change can affect biodiversity, but only recently have they begun to consider the interplay between the two factors (Ward and Masters 2007, Walther et  al. 2009). The complexity, context dependency, subtlety, and uncertainty that typify invasion ecology are compounded when considering invasive spe­ cies’ responses to the three major variables of global climate change: increasing temperature, altered precipitation patterns, and elevated CO2 levels (Pritchard et al. 2007). Climate change is expected to affect ecosys­ tem functions and threaten global biodiversity by causing extinction of species (e.g., Thomas et  al. 2004, Rinawati et  al. 2013), with habitat specialists more at risk because of previous hab­ itat destruction (Travis 2003). Shifts in range, typically toward the poles, are more readily detected responses to climate change than are extinctions. Ranges often expand latitudinally and elevationally at the cool margins of popula­ tions, whereas contractions at warm, lower lim­ its of latitude and elevation are less common (Wilson et al. 2005). An example of northward range expansion in Japan is that by a North American immigrant webworm (Hyphantria cunea), which not only has undergone

northward range expansion in temperate areas, but also has added a generation and is trivoltine in a portion of its Japanese range (Walther et al. 2009). A detailed eco‐physiological knowledge of the adventive stink bug N. viridula (Musolin 2007) was crucial to understanding its similar response to warming in Japan. Range shifts, however, are not without ecological costs, such as the phenological maladaptation of N. viridula to its novel environment in Japan (Musolin 2007). Even with the inexactness of climate projec­ tions (Dukes 2011), predictions of a range shift by an insect species in response to a climatic variable (e.g., warming) can be accurate, espe­ cially when extensive information on an insect’s phenology, voltinism, behavior, and physiology are available (Simberloff 2000b, Musolin 2007). In terrestrial ecosystems, extensive effects on biodiversity can be expected for insect–plant communities because of the dominance of these organisms (Nooten et  al. 2014). Model‐based predictions, however, become less precise with increasing complexity, uncertainty, and variabil­ ity (e.g., Pincebourde and Woods 2012). An accuracy equivalent to that of predicting the effects of warming on an insect species should not be expected for predicting the overall effects of climate change on community structure and ecosystem processes (Andrew and Hughes 2005, Nooten et al. 2014). Predictions involving communities and ecosystems are complicated by climatic variables that directly and indirectly affect a multitude of insect species, the lack of key bionomic data for insects of all trophic lev­ els, and incomplete biological data on plants, such as climate change’s effects at the cellu­ lar level. Given our inability to predict the effects of invasive species (Simberloff 2000b), we should not be surprised by unforeseen consequences of interactions between global climate change and invasive species. In a changing climate, adven­ tive species now considered invasive might some day be looked upon as desirable (Walther et al. 2009). Researchers who study interactions between invasive species and climate change continue to document effects of climate on

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numerous insect species and reveal the physio­ logical plasticity and genetic variability that enable insects to adapt and evolve in response to climatic instability. Climate’s direct and indi­ rect effects, positive and negative, on invasive insects are likely to be species specific, thus complicating attempts to assess climatic effects at community and ecosystem levels.

21.12 ­Systematics, Biodiversity, and Adventive Species Systematics and taxonomy are fundamental to the study, communication, and identification of agriculturally important pest species (Miller and Rossman 1995). Misidentifications can result in serious miscalculations concerning life‐history studies, pest‐risk assessments, and biocontrol strategies, as evidenced by species of the moth genus Copitarsia (Simmonds and Pogue 2004, Venette and Gould 2006). Numerous pest prob­ lems have been solved through a systematic knowledge of organisms that affect agricultural and forest ecosystems (Miller and Rossman 1995, Rossman and Miller 1996). The elucida­ tion of the biology of a pest species for control purposes can be achieved only through accurate identification (Wilson 2000). The availability of an adequate “biosystematic service” (Knutson 1989) is needed to deal with the problem of immigrant insects (Dick 1966, Oman 1968). Relatively few nations have biosys­ tematic service centers, and those that do often lack specialists to identify species of certain economically important groups. Such gaps in taxonomic coverage (Oman 1968, Wheeler and Nixon 1979) impede the execution of plant‐reg­ ulatory functions and the enforcement of quar­ antine laws (Knutson 1989, New 1994), although the availability of port identifiers (Shannon 1983) helps to compensate for a lack of special­ ists in particular taxa. A limited understanding of taxonomy and lack of specialists can lead to catastrophic socioeconomic losses, as happened with Dutch elm disease in North America (Britton and Sun 2002). Accurate identification

facilitates determination of an invader’s origin, allowing appropriate areas to be searched for natural enemies that might suppress pest densi­ ties by classical biological control (Sabrosky 1955, Delucchi et  al. 1976, Danks 1988). Thorough systematic knowledge also is crucial to assure accurate identification of natural ene­ mies released by researchers and those sold commercially (e.g., Henry and Wells 2007). Better support for taxonomy and systematics (Knutson 1989, New 1994) would enhance our ability to identify newly established species that threaten agriculture, forestry, human health, and the environment and to determine their areas of origin. It also would enhance our ability to identify insects intercepted in commerce and assist regulatory agencies in determining whether the species are likely to be harmful or innocuous.

21.13 ­Concluding Thoughts Invasive species might soon supplant habitat loss and fragmentation as the principal threat to native biodiversity (Crooks and Soulé 1999) and undoubtedly will continue to provide “wonder and surprise” (Simberloff 1981) for ecologists who study them. Adventive insects will con­ tinue to be redistributed globally given the development of new transportation technolo­ gies and emphasis on free trade, coupled with inevitable increases in human migration and tourism. Programs of regulatory enforcement are unlikely to keep pace with increases in global commerce due to liberalization of trade (Jenkins 1996). The public will remain generally unaware that losses in invertebrate diversity can be detri­ mental to human well‐being (Kellert 1995). Even though it is generally acknowledged that invading insects can affect ecosystem structure and function, more rigorous scientific data are needed to assess their detrimental effects on native biodiversity, as is the case for invasive species in general (Brown and Sax 2007). As the numbers of immigrant insects con­ tinue  to increase, so too will opportunities for

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introducing parasitoids and predators to help suppress insect pests among the newly estab­ lished invaders. Formal risk assessments continue to be refined for different taxa (Kumschick and Richardson 2013), including insects (e.g., ants; Ward et  al. 2008). Because of the idiosyncratic nature of adventive insects (including biocontrol agents) in new environments, risk assessments are useful in determining the probability that a species will invade but cannot be expected to pre­ dict with certainty where adventive species might become established or their economic effects, let alone their complex and subtle environmental interactions and consequences. A guilty‐until‐ proven‐innocent approach to pest exclusion and the use of “white lists” (e.g., McNeely et al. 2001), however, would represent a useful change from current regulatory policy (Ruesink et  al. 1995; Simberloff et al. 1997; Simberloff 2003a, 2005b). Messing and Wright (2006) recommended that US policies regulating the introduction of bio­ control agents be made similar to those employed by Australia and New Zealand. Changes to our first line of defense – attempts at exclusion or prevention of ­establishment – are likely to come slowly. As Van Driesche and Van Driesche (2001) pointed out, Americans tend to view prevention as an unpalatable concept. Attempts to exclude immigrant species conflict with society’s emphasis on free trade and travel (Kiritani 2001, Low 2001). Not only will addi­ tional immigrant insects continue to become established in the United States and elsewhere, but some species once considered innocuous faunal additions will be revealed as harmful. This prediction follows from the realization that relatively few immigrant insects have received attention from researchers, and with lag times sometimes being protracted, adverse ecological effects can take years to develop and even longer to be detected. Immigrants infused with new genetic material via subsequent introductions may continue to adapt to new environments. Pestiferous immigrants no longer thought to represent a threat might resurge as a result of changes in agricultural practices, climate, and environment.

The invasive species problem is “a complex social and ethical quandary rather than solely a biological one” (Larson 2007). Invasive species cannot be prevented, but the problem can be minified if attempts at amelioration are viewed as the “art and science of managing people” (Reaser 2001). We agree that human dimen­ sions of the problem deserve more attention and that effective solutions depend heavily on policymakers appreciating connections between invasive species and global trade, transport, and tourism (McNeely 2001b, 2006). Policymakers also need to realize that climate change can exacerbate the impacts of invasive species. Numerous suggestions for alleviating the invasive‐species problem have been made (e.g.,  Lodge et  al. 2006, Nentwig 2007a). Recommendations include an obvious need to develop reliable predictive theories of biological invasions; to be more aware of species that have become invasive elsewhere; and to foster greater international collaboration and cooperation (Clout and De Poorter 2005, Bateman et  al. 2007), with continued development of online information networks and less emphasis on political boundaries (McNeely 2001c, McNeely et al. 2001, De Poorter and Clout 2005, Simpson et al. 2006). Greater collaboration among biolo­ gists, economists, geographers, psychologists, and sociologists will be particularly crucial in addressing problems (McNeely 2006). Among more innovative suggestions is the development of approaches that would subsidize native spe­ cies until they are able to adapt to altered envi­ ronments and coexist with invaders (Schlaepfer et al. 2005). As is the case for most other aspects of invasion biology, researchers, conservation­ ists, policymakers, and the public disagree on how best to deal with adventive organisms. Disparate views have long characterized discus­ sions of adventive species. Before the United States enacted plant‐regulatory legislation, a leading federal official once advocated a laissez‐ faire approach to immigrant insects (Marlatt 1899), which elicited a storm of protest (Wheeler and Nixon 1979). More recently, “blanket opposition” to adventive organisms has been

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predicted to become “more expensive, more irrational, and finally counterproductive as the trickle becomes a flood” (Soulé 1990). Progress toward documenting the extent of the invasive‐species problem and devising solutions has been made in recent years. The Scientific Committee on Problems of the Environment (SCOPE) was a founding partner in the Global Invasive Species Program (GISP). Created in 1997, GISP seeks solutions through new approaches and tools (Mooney 1999, McNeely et al. 2001, Barnard and Waage 2004). Noteworthy US initiatives include the creation in 1999 of a National Invasive Species Council. Historical data such as interception records of  regulatory agencies (e.g., Worner 2002, McCullough et  al. 2006, Ward et  al. 2006) are being evaluated to address the lack of informa­ tion on failed introductions (other than biocon­ trol agents), a deficiency that Simberloff (1986) pointed out. Other positive signs are increased emphasis on the role of taxonomy in the early detection of immigrants, such as regional work­ shops for enhancing the identification skills of diagnosticians at land‐grant universities and identifiers at US ports of entry (Hodges and Wisler 2005). We also note a recent collabora­ tion of the Carnegie Museum of Natural History, traditionally a research institution, with federal and state agencies involved in detecting new pests. This linkage supplements the museum’s budget while providing timely identifications of insects found in traps or surveys in or near ports of entry. Of the principal means of dealing with inva­ sive species – exclusion, detection, and manage­ ment (e.g., containment, eradication, and mitigation) – we think that detection warrants greater attention. J. W. Beardsley regularly looked for new immigrant insects in Hawaii from 1960 to 1990 (Loope and Howarth 2003). More entomologists who are familiar with local faunas, and hence more likely to recognize insects that seem out of place (Lutz 1941: 6; Hoebeke and Wheeler 1983), are conducting detection surveys. Our own fieldwork in the vicinity of port cities in New England and the

Atlantic provinces of Canada (e.g., Hoebeke and Wheeler 1996, Wheeler and Hoebeke 2005), and fieldwork by Christopher Majka and col­ leagues in Atlantic Canada (e.g., Majka and Klimaszewski 2004), attest to the value of detec­ tive work in areas that are vulnerable to entry by immigrant insects. Early detection of immi­ grants favors a rapid response (Burgess 1959, Oman 1968, Reynolds et  al. 1982), and facili­ tates eradication (Simberloff 2003c, Pluess et al. 2012, Tobin et al. 2014) and classical biological control (Ehler 1998). The advantages of early detection in managing invasive species (Crall et  al. 2012), coupled with public involvement (Dick 1966), were demonstrated in Auckland, New Zealand, in 1996; a private citizen gave government scientists a distinctive caterpillar that proved to be the Asian white‐spotted tus­ sock moth (Orgyia thyellina). This potential pest, although apparently having been estab­ lished for more than a year, was eradicated (Clout and Lowe 2000). Contact with a local USDA office by a Chicago resident who sus­ pected he had a specimen of the Asian long‐ horned beetle (A. glabripennis) proved crucial to the city’s eradication efforts against the pest (Lingafelter and Hoebeke 2002, Antipin and Dilley 2004). The availability of the Internet has facilitated the general public’s involvement (as citizen scientists) in detection, post‐establish­ ment delimiting surveys, and other roles that aid the management of invasive species (Crall et al. 2010, Ashcroft et al. 2012). DNA barcod­ ing might also facilitate earlier detections of harmful immigrant insects (Floyd et al. 2010). A review of recent literature on immigrant insects in British Columbia revealed a trend toward reporting the first records of adventives in trade magazines and in‐house publications rather than in scientific journals. Outlets for reporting immigrants new to the province might have changed during the 1990s because of an inability to pay publication costs for papers in scientific journals; the view that with increas­ ing biotic homogenization the presence of species new to a fauna no longer warrant document­ ation in journal articles; a lack of

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taxonomic specialists who are capable of identi­ fying immigrant species; and too few entomolo­ gists remaining in British Columbia to address new threats to agriculture, forestry, and public health (Gillespie 2001). Britton and Sun (2002) acknowledged that Internet sites can omit rele­ vant references and often are ephemeral. We, therefore, encourage publishing the detection of immigrants in mainstream journals, with accompanying summaries of bionomics in the area where species are native, as well as taxo­ nomic information to facilitate recognition in their new faunas. The availability of at least the approximate time of arrival is important in understanding the long‐term effects of invaders (Strayer et al. 2006). We also feel it is useful to follow the spread of immigrants and to docu­ ment range extensions; such historical records are invaluable in allowing future workers to reconstruct immigration events. Knowledge of the new ranges of transferred species also can enhance our biological understanding of inva­ sive organisms (McGlynn 1999). A global computerized database of immigrant pests has been envisioned for more than 25 years to complement the Western Hemisphere (formerly North American) Immigrant Arthropod Database (WHIAD), administered by the USDA (Knutson et al. 1990, Kim 1991). Other world regions would benefit from a mas­ ter list of all adventive species, which would help in inventorying Earth’s biota, serve as a database for assessing biotic changes, and facili­ tate dissemination of information on invasive species (Wonham 2003). Schmitz and Simberloff (2001) proposed a US database administered by a National Center for Biological Invasions. Taking advantage of existing capacities and partnerships (WHIAD was not mentioned), the center would place the administration of rules and regulations pertaining to invasive species under a central agency linked to a major univer­ sity (perhaps the Institute for Biological Invasions, University of Tennessee, which Simberloff directs; or the Center for Invasive Species Research, University of California, Riverside). Loosely modeled after the Centers

for Disease Control and Prevention (Schmitz and Simberloff 2001), the center would be of immeasurable value in dealing promptly and effectively with invasive species. Creation of a National Center for Biological Invasions might forestall homogenization of the US biota and further erosion of quality of life. Societal effects of immigrants can include loss in the amenity value of ecosystems and reduc­ tion in ecotourism, owing to sameness among biotic communities (McLeod 2004, Olden et al. 2005). The harmful effects of immigrant insects might also include development of a biophobic public reluctant to venture outdoors (Soulé 1990) because of the possibility of inhaling small immigrant insects such as whiteflies, and threats from imported fire ants and African honeybees (Vinson 1997, Paine et  al. 2003) or mosquito‐ transmitted diseases. In the event of bioterror­ ism involving the release of pathogens or other harmful organisms in the United States (Pratt 2004), a rapid and effective response to the threat would be more likely if a national center for invasive species were in place. We feel that  congressional action on Schmitz and Simberloff ’s (2001) proposal, perhaps more than any other initiative, would increase public understanding of the problem, stimulate inter­ est in studying invasive species, improve cur­ rent programs of pest exclusion and detection, and ensure prompt responses to new invaders. A US center for bioinvasions also could serve as a model for other nations as they try to protect native biodiversity and preserve society’s “sense of place and quality of life” (Olden et al. 2005).

­Acknowledgments We appreciate the editors’ invitation to be part of the book. We are pleased to carry on the anal­ ysis of immigrant insects in North America begun by the late Reece Sailer and dedicate our review to Daniel Simberloff for his numerous seminal contributions to invasion ecology. The editors and anonymous referees offered many constructive suggestions for improving the

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manuscript. A.G.W. thanks interlibrary‐loan, reference, and remote‐storage librarians at Cooper Library, Clemson University, for their assistance; Tammy Morton and Rachel Rowe for their help with manuscript preparation; and Thomas Henry, Gary Miller, and Craig Stoops for much‐appreciated encouragement.

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aliens. Global Ecology and Biogeography 21: 305–311. Webster, F. M. 1892. Early published references to some of our injurious insects. Insect Life 4: 262–265. Webster, F. M. 1897. Biological effects of civilization on the insect fauna of Ohio. Pp. 32–46. In Fifth Annual Report of the Ohio State Academy of Science, Columbus, Ohio. Wetterer, J. K. 2007. Biology and impacts of Pacific island invasive species. 3. The African big‐headed ant, Pheidole megacephala (Hymenoptera: Formicidae). Pacific Science 61: 437–456. Whattam, M., G. Clover, M. Firko and T. Kalaris. 2014. The biosecurity continuum and trade: border operations. Pp. 149–188. In G. Gordh and S. McKirdy (eds). The Handbook of Plant Biosecurity. Springer, Dordrecht. Wheeler, A. G., Jr. 1999. Otiorhynchus ovatus, O. rugosostriatus and O. sulcatus (Coleoptera: Curculionidae): exotic weevils in natural communities, mainly mid‐Appalachian shale barrens and outcrops. Proceedings of the Entomological Society of Washington 101: 689–692. Wheeler, A. G., Jr. 2002. Chilacis typhae (Perrin) and Holcocranum saturjae (Kolenati) (Hemiptera: Lygaeoidea: Artheneidae): updated North American distributions of two Palearctic cattail bugs. Proceedings of the Entomological Society of Washington 104: 24–32. Wheeler, A. G., Jr. and T. J. Henry. 1992. A Synthesis of the Holarctic Miridae (Heteroptera): Distribution, Biology, and Origin, with Emphasis on North America. Thomas Say Foundation Monograph 25. Entomological Society of America, Lanham, Maryland. 282 pp. Wheeler, A. G., Jr. and E. R. Hoebeke. 1995. Coccinella novemnotata in northeastern North America: historical occurrence and current status (Coleoptera: Coccinellidae). Proceedings of the Entomological Society of Washington 97: 701–716. Wheeler, A. G., Jr. and E. R. Hoebeke. 2001. A history of adventive insects in North America: their pathways of entry and programs for their

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(Salix interior) in Illinois. Great Lakes Entomologist 38: 100–103. Wilcove, D. S., D. Rothstein, J. Dubow, A. Phillips and E. Losos. 1998. Quantifying threats to imperiled species in the United States. BioScience 48: 607–615. Williams, D. F. 1994. Exotic Ants: Biology, Impact, and Control of Introduced Species. Westview Press, Boulder, Colorado. 332 pp. Williamson, M. [H.]. 1996. Biological Invasions. Chapman and Hall, London. 244 pp. Williamson, M. [H.]. 1999. Invasions. Ecography 22: 5–12. Williamson, M. H. and K. C. Brown. 1986. The analysis and modelling of British invasions. Philosophical Transactions of the Royal Society of London 314B: 505–522. Williamson, M. [H.] and A. Fitter. 1996. The varying success of invaders. Ecology 77: 1661–1666. Wilson, E. O. 1992. The Diversity of Life. Harvard University Press, Cambridge, Massachusetts. 424 pp. Wilson, E. O. 1994. Naturalist. Island Press, Washington, DC; Shearwater Books, Covelo, California. 380 pp. Wilson, M. R. 2000. Loss of taxonomists is a threat to pest control. Nature 407: 559. Wilson, R. J., D. Gutiérrez, D. Martinez, R. Agudo and V. J. Monserrat. 2005. Changes to the elevational limits and extent of species ranges associated with climate change. Ecology Letters 8: 1138–1146. Wilson, S. W. and A. Lucchi. 2007. Feeding activity of the flatid planthopper Metcalfa pruinosa (Hemiptera: Fulgoroidea). Journal of the Kansas Entomological Society 80: 175–178. Winston, M. L. 1992. Killer Bees: the Africanized Honey Bee in the Americas. Harvard University Press, Cambridge, Massachusetts. 162 pp. Wirth, W. W. 1979. Siolimyia amazonica Fittkau, an aquatic midge new to Florida with nuisance potential. Florida Entomologist 62: 134–135. With, K. A. 2002. The landscape ecology of invasive spread. Conservation Biology 16: 1192–1203.

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Wittenberg, R. (ed). 2005. An Inventory of Alien Species and Their Threat to Biodiversity and Economy in Switzerland: Report to the Swiss Agency for Environment, Forests and Landscape. CABI Bioscience Switzerland Centre, Delémont. 417 pp. Wonham, M. J. 2003. Ecological gambling: expendable extinctions versus acceptable invasions. Pp. 179–205. In P. Kareiva and S. Levin (eds). The Importance of Species: Perspectives on Expendability and Triage. Princeton University Press, Princeton, New Jersey. Wood, S. L. 1975. New synonymy and new species of American bark beetles (Coleoptera: Scolytidae), Part II. Great Basin Naturalist 35: 391–401. Woods, M. and P. V. Moriarty. 2001. Strangers in a strange land: the problem of exotic species. Environmental Values 10: 163–191. Woodworth, B. L., C. T. Atkinson, D. A. LaPointe, P. J. Hart, C. S. Spiegel, E. J. Tweed, C. Henneman, J. LeBrun, T. Denette, R. DeMots, K. L. Kozar, D. Triglia, D. Lease, A. Gregor, T. Smith and D. Duffy. 2005. Host population persistence in the face of introduced vector‐ borne diseases: Hawaii amakihi and avian malaria. Proceedings of the National Academy of Sciences USA 102: 1531–1536.

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22 Biodiversity of Blood-sucking Flies: Implications for Humanity Peter H. Adler Department of Plant and Environmental Sciences, Clemson University, Clemson, South Carolina, USA

Flies are so mighty that they win battles, paralyze our minds, eat our bodies… (Blaise Pascal, 1660) The anecdotal claim that flies have been responsible for more human deaths and misery than any other group of macroorganisms in recorded history is not easily dismissed. From disseminators of disease to purveyors of famine, flies have marched in lockstep with humanity. They are found in the hieroglyphics of ancient Egypt (Greenberg 1973), and hold a high biblical profile as the fourth of the 10 plagues that Moses brought down on the house of Pharaoh (Exodus 8: 21–31). They have driven cultures, economies, land use, and the outcomes of battles (Steiner 1968, Pauly 2002, Adler and Wills 2003). Through the transmission of disease agents, they have been a driving force in human evolution. Omnipresent, prolific, and rapid in development, their sudden appearance in rotting organic matter fueled the quaint notion of spontaneous generation. They have tracked humans across the globe, many species now being cosmopolitan. Roughly 6% of immigrant insect species in the 48 contiguous United States are flies (Sailer 1983), including some of history’s most destructive species, such as the yellow fever mosquito (Aedes aegypti) and Hessian fly (Mayetiola destructor).

Only a few dipteran families  –  the Syrphidae and perhaps the Tephritidae – hold even a fraction of the aesthetic allure of butterflies, dragonflies, and tiger beetles. Much of the progress in understanding dipteran biodiversity, therefore, relies on the impetus of socioeconomic and medicoveterinary concerns. Blood-sucking flies, because they breach the host’s circulatory system, can be important in the transmission of disease agents. The evolutionary antiquity of blood-sucking flies (Borkent and Grimaldi 2004) suggests a rich and often tightly evolved system of interactions with hosts and pathogens. Because of their significance to humanity, flies that suck blood and transmit the agents of disease are among the taxonomically best-known Diptera in the world. Their well-developed taxonomy, although still markedly incomplete, suggests that they can provide insight into the biodiversity patterns and trends of other organisms. In the following treatment, I focus on the biodiversity of blood-sucking flies of vertebrate animals, and particularly those that transmit parasites and pathogens. Blood-sucking, or hematophagous, flies are defined here as species with adults that cut or puncture host skin to obtain a blood meal. Not treated are flies that take blood from invertebrates; flies with bloodfeeding larvae (e.g., Protocalliphora species); flies that scarify wounds and eyes for blood and

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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other secretions (e.g., Musca autumnalis); and non-biting vectors of disease agents or, borrowing terminology from pollination ecology, the “mess-and-soil” vectors, such as filth flies (e.g., Musca domestica). Also untreated are the dipteran vectors, all non-biting, of phytopathogens (Harrison et al. 1980). I first consider the size of the world fauna of blood-sucking flies, with a brief summary of the biodiversity and socioeconomic importance of each family. I then examine the philosophy, relevance, status, and future of biodiversity investigations on these flies in relation to the welfare of humans and domestic animals.

22.1 ­Numbers and Estimates The order Diptera, representing perhaps 10% of all life forms, comprises nearly 160,000 described species worldwide divided among 158 families, some of which are acknowledged to be unnatural, paraphyletic or polyphyletic groups (Courtney et  al., this volume). How many species of flies inhabit the planet? In the words of E. O. Wilson (1985), referring to all life forms, “We do not know, not even to the nearest order of magnitude.” Some estimates suggest that nearly half or more of the Nearctic dipteran fauna remains undescribed (Thompson 1990). Estimates of the unknown are far greater for the tropical regions. The consequences of not knowing how many species  –  or more importantly, what species  –  share our planet are disproportionately greater for some dipteran taxa than for others. The relative importance to human welfare of, for instance, the Culicidae far exceeds that of any of the multitude of more obscure families of flies such as, say, the Asteiidae. More effort and resources, therefore, have been dedicated to the taxonomy of hematophagous flies than of nonhematophagous flies. Consequently, the number of described species of hematophagous Diptera should approach the actual number more nearly than that for other flies. The efforts of more than 250 years have brought us to the point where

more than 18,200 named species have been placed in 11 families of hematophagous flies, representing approximately 11.5% of the total described species of Diptera. About one-quarter of these species have lost or modified the biting mouthparts over evolutionary time and are unable to cut or puncture flesh to obtain blood (e.g., some species of Culicidae, Simuliidae, and Tabanidae), or they feed on invertebrate blood (many Ceratopogonidae). The total number of described species that take vertebrate blood is about 13,833 (Table 22.1). Yet, counting species is akin to running in place; no sooner are the species counted than new names are added and older ones synonymized or resurrected. In the hyperactive five-year period from 2000 to 2004, for example, 179 new species of black flies were described, 28 names were synonymized, and 16 names were recovered to validity from synonymy. In a similar five-year time frame, 1999 to 2003, 242 new species of ceratopogonids (including 40 vertebrate-blood feeders) were described, increasing the number of species for the entire family by 4.6%. From 2009 to 2015, about 610 new species of flies that acquire blood from vertebrates were described. The discovery and recognition of species varies over time, often depending on significant events or revolutions in approaches, methods, and technologies. For the Simuliidae, for example, significant advancements include the first use of male genitalia (1911) and later female genitalia (1927) for taxonomic purposes, and the introduction of cytogenetic procedures (1956). Molecular techniques represent the current revolution, with DNA barcoding (2003) among the most touted methods. New species of blood-sucking flies continue to be discovered in poorly sampled, as well as more thoroughly sampled, geographic areas. For most families, the greatest potential for new species lies in untapped areas of the tropical rainforests. Seventy-one new species of black flies, for example, were described in a single year from three of the five major islands of Indonesia (Takaoka 2003), and more can be expected as the high mountains and surround-

1; 33

Glossinidae# (tsetse)

40 174

Muscidae (horn flies, stable 11; 57 flies, biting muscids)†† 9; 1,033

2; 41 26; 2,127 135; 4,434

Psychodidae (sand flies)‡,‡‡

Rhagionidae (biting snipe flies)‡,§§

Simuliidae (black flies)¶¶

Tabanidae (horse flies, deer flies)‡,##

747

216

0

135

Hippoboscidae (louse flies, 65; 786 keds, bat flies)‡,**

33

751

39; 3,445

Culicidae (mosquitoes)‡,¶

192

6

4; 1,688

Corethrellidae (frog-biting 1; 107 midges)‡

Ceratopogonidae (biting midges, no-see-ums, punkies)‡,§

13

514

255

7

50

5

147

0

730

11

142

15

326

231

29

15

3

47

0

169

7

156

3

1,217

363

0

531

6

241

0

1,031

70

316

24

955

388

0

123

14

196

0

1,000

13

429

23

675

717

6

140

14

108

0

473

3

453

7

World genera; species Afrotropical Australasian Nearctic Neotropical Oriental Palearctic

Athericidae (athericids)†,‡ 3; 82

Taxon (English common name)*

Total number of described species

(Continued)

Chainey and Oldroyd 1980, Chvala 1988, Fairchild and Burger 1994, Burger 1995, Andreeva 2004, Coscarón and Papavero 2009, Henriques et al. 2012, Species 2000 and ITIS 2015

Takaoka 2003, Adler et al. 2004, Adler and Crosskey 2015b

Turner 1974, Nagatomi and Evenhuis 1989

Lewis 1978, Young and Perkins 1984, Seccombe et al. 1993, Young and Duncan 1994, Curler and Jacobson 2012, Bates et al. 2015

Zumpt 1973, Pont 1980b, Braack and Pont 2012

Hutson and Oldroyd 1980, Maa and Peterson 1987, Peterson and Wenzel 1987, Wenzel and Peterson 1987, Maa 1989, Guerrero 1997

Pont 1980a, Jordan 1993, Krafsur 2009

Rueda 2008, Gaffigan et al. 2015, Harbach 2015

Borkent 2008

Borkent and Wirth 1997, Borkent 2014

James 1968; Nagatomi 1975; Stuckenberg 1980, 2000; Webb 1981; Nagatomi and Evenhuis 1989; Rozkošný and Nagatomi 1997

Reference

Table 22.1  World biodiversity of extant, described hematophagous flies that take blood from vertebrates, followed by the number of fly-borne diseases. Family classification follows that of Pape et al. (2011).

15

21

17

20 17

16 18

8

2,596 Table 22.2

Table 22.2

—

Reference

* Does not include families that presumably do not attack vertebrates but, nonetheless, have biting or cutting mouthparts. The family Chironomidae includes three species with mandibulate mouthparts but with unknown (if any) hosts (Cranston et al. 2002). Whether the feeding behavior of the carnid bird flies of the genus Carnus involves piercing and sucking of blood from birds remains controversial (Grimaldi 1997). The total number of species does not always equal the sum of regional faunas because some species are present in more than one region. † Includes only genera with representatives known to take vertebrate blood (Atrichops, Dasyomma, Suragina, and Suraginella). ‡ Includes species described as new, plus new synonyms and revalidated species, since the references listed here were published, based on searches of Zoological Records to August 2015. § Includes only members of the family that feed on vertebrate blood: Austroconops, Culicoides, Leptoconops, and Forcipomyia (Lasiohelea). Species numbers for each region are based on type localities given by Borkent (2014); the 257 species with China as the type locality are divided equally between the Oriental and Palearctic regions. ¶ Number of blood-feeding genera ranges from 39 (Gaffigan et al. 2015) to 110 (Harbach 2015), depending on the classification system. Includes all species of the family except 89 species of Toxorhynchites with non-cutting mouthparts and 12 species of Malaya that feed on regurgitated stomach contents of ants; the number of vertebrate blood-feeding mosquitoes, nonetheless, might be overstated because hosts, if any, of many species remain unknown. # Includes subspecies, with the view that closer scrutiny might confirm at least some as valid species. Subspecies account for about one-quarter of the total species count. ** Family Hippoboscidae sensu lato historically has been (and sometimes still is) presented as three separate families: Hippoboscidae sensu stricto (21 genera), Nycteribiidae (13 genera), and Streblidae (31 genera). †† Includes only those species with biting mouthparts (subfamily Stomoxyinae plus one species, Musca crassirostris, in subfamily Muscinae). ‡‡ Includes only taxa with biting mouthparts: subfamilies Phlebotominae (988 species; Bates et al. 2015) and Sycoracinae (three genera, 45 species; Santos et al. 2013). Consensus is building for recognition of six genera of Phlebotominae (Bates et al. 2015), although as many as 25 genera have been recognized, with most of the discrepancy in numbers being in the New World (Galati 1995); about 5% of Phlebotominae are subspecies, not including nominotypical subspecies. §§ Includes only those genera with representatives known to take vertebrate blood (Spaniopsis and Symphoromyia). ¶¶ Includes all members of the family except 50 species (25 in the Nearctic Region and at least 32 in the Palearctic Region) that do not have mouthparts adapted for cutting host tissue. ## Includes all members of the family except Goniops (one Nearctic species), Stonemyia (eight Nearctic and three Palearctic species), the subfamily Scepsidinae (six Afrotropical and one Neotropical species), and the tribe Mycteromyiini (16 Neotropical species), which do not take vertebrate blood; additional species probably do not feed on vertebrate blood, but they are poorly documented.

26

15

3,141

42

8

3,799

Diseases of domestic animals

18

986

45

Diseases of humans

1,876

296; 13,833

Totals

2,307

World genera; species Afrotropical Australasian Nearctic Neotropical Oriental Palearctic

Total number of described species

Taxon (English common name)*

Table 22.1  (Continued)

22  Biodiversity of Blood-sucking Flies

ing tropical forests of areas such as Irian Jaya reluctantly yield their species. Additional biodiversity hotspots are in politically unstable areas of the world that will prove hazardous for decades, littered with political unrest, armed insurgents, land mines, and government restrictions on free-range collecting. Some of the potentially species-rich but politically troublesome areas include Afghanistan, Cambodia, Myanmar, and northern India and Pakistan. An unknown number of species remains hidden within described morphospecies (species recognized on anatomical criteria). Prospecting in the genome, therefore, is likely to reveal a wealth of additional biodiversity. Cytogenetic and molecular studies have shown that morphologically similar species, known as cryptic species, or sibling species, are commonplace among blood-sucking flies. About one-fourth of the 255 species of black flies in North America were discovered chromosomally (Adler et al. 2004). In Latin America, the black fly Simulium metallicum is a complex of more than seven cryptic species (Conn et al. 1989). At least 40 of more than 480 species in the mosquito genus Anopheles are unnamed members of species complexes (Harbach 2004). The Anopheles punctulatus complex in Papua New Guinea, for example, consists of at least six cryptic species (Foley et al. 1993), and the New World Anopheles crucians complex includes five cryptic species (Wilkerson et al. 2004). Nearly 30 years of chromosomal studies of African vectors have shown that Anopheles gambiae consists of seven or more cryptic species (Coluzzi et al. 2002), and Simulium damnosum consists of 55 cryptic species and cytoforms (Post et al. 2007), making it the largest species complex of any blood-feeding organism. As recently as 2013, two new species were formally named and described in the An. gambiae complex (Coetzee et  al. 2013), perhaps the most-studied medically important arthropod on the planet. Hidden more deeply than cryptic species are homosequential sibling species, which have the same banding sequences in their polytene chromosomes and are almost identical morphologically (Bedo 1979). Their discovery is facilitated by ecological differences and cytological e­vidence

such as heterozygote deficiencies of polymorphic inversions. Because of the difficulty in uncovering homosequential sibling species, no statements yet can be made about their prevalence. Molecular techniques hold the potential to reveal hidden species that are reproductively isolated but lack diagnostic cytological and morphological markers. A complete biodiversity catalog for extant blood-sucking flies should include not only all species arranged phylogenetically, but also all life stages, both sexes, and ultimately a comprehensive genetic library for each species. Although the number of blood-feeding species currently stands at 13,883, the actual structural and ecological diversity is about five times greater (i.e., ca. 69,415 biodiversity units), taking into account eggs, larvae, pupae, males, and females. In many cases, however, only one or two life stages or a single sex are known. Species-level taxonomy of larvae and pupae is well developed for the Culicidae, Glossinidae, Simuliidae, and a few regional groups, but poorly known for the remaining families. The larvae and pupae of North American simuliids, for example, are described for 98% and 93% of the species, respectively (Adler et al. 2004), whereas respective figures for the larvae and pupae of the world’s Culicoides are only 13% and 17% (Borkent 2014). The eggs have been described for no more than 10% of the world’s species of blood-sucking flies, perhaps largely a matter of choice, for they often can be extracted from females that are captured gravid or that are allowed to mature their eggs after capture. The job of collecting, rearing, curating, describing, naming, and publishing the remaining biodiversity of hematophagous Diptera is daunting.

22.2 ­Overview of Blood-sucking Flies and Diseases Of the roughly 13,833 described species of flies that acquire blood from vertebrate hosts, about 2% serve as vectors of the agents of at least 45 diseases of humans, and less than 1% are known to transmit the agents of more than 40 diseases of ­domestic animals (Table 22.2). The following

717

African trypanosomiasis (sleeping sickness)

[Deer ked dermatitis]

Glossinidae

Hippoboscidae

Avian trypanosomiasis, [bartonellosis], [filariasis of canids]

Baker 1967, Dehio et al. 2004, Reeves et al. 2006, Lloyd 2009

Krinsky 2009

Harwood and James 1979, Eldridge et al. 2000, Foster and Walker 2009

Avian malaria, avian pox (e.g., fowlpox), canine dirofilariasis (dog heartworm disease), eastern equine encephalitis, Japanese encephalitis, [various onchocerciases], Rift Valley fever, Venezuelan equine encephalitis, Wesselsbron disease, western equine encephalitis, West Nile encephalitis, [additional viral diseases]

[Anthrax], bancroftian filariasis (elephantiasis), Barmah forest viral disease, brugian filariasis, [Cache Valley viral disease], [California encephalitis], chikungunya fever, dengue, dirofilariasis, eastern equine encephalitis, [Ilheus fever], [Jamestown Canyon viral disease], Japanese encephalitis, La Crosse encephalitis, malaria, Mayaro fever, Murray Valley encephalitis, O’nyong-nyong fever, Rift Valley fever, [Rocio encephalitis], Ross River fever, Semliki Forest encephalitis, Sindbis fever, [showshoe hare viral disease], St Louis encephalitis, Tahyna fever, [tularemia], Venezuelan equine encephalitis, Wesselsbron disease, western equine encephalitis, West Nile encephalitis, yellow fever, Zika, [additional viral diseases]

Culicidae

Nagana

—

None known

None known

Mellor et al. 2000, Mullen 2009, Rasmussen et al. 2012, Carpenter et al. 2013

—

Corethrellidae

None known

Reference

African horse sickness, Akabane viral disease?, avian trypanosomiasis, bluetongue disease, [bovine ephemeral fever?], bovine onchocerciasis, [epizootic hemorrhagic disease], [equine encephalosis], equine onchocerciasis, leucocytozoonosis, [Palyam viral disease?], Schmallenberg viral disease, [additional viral diseases]

None known

Athericidae

Domestic animals†

Ceratopogonidae Mansonelliasis, Oropouche fever

Humans

Taxon

Diseases*

Table 22.2  Hematophagous fly-borne diseases of humans and domestic animals of the world; dipteran families and diseases within each family are listed alphabetically.

None known

Mansonelliasis, onchocerciasis (river blindness), [tularemia]

[Anthrax], loiasis, tularemia

Rhagionidae

Simuliidae

Tabanidae

—

Rutledge and Gupta 2009

Zumpt 1973, Harwood and James 1979, Moon 2009, Baldacchino et al. 2013

B. Mullens 2009, Baldacchino et al. 2014

* Diseases in square brackets indicate that the families under which they are listed probably have a minor epidemiological role; other vectors or means of transmission are more common. A disease followed by a question mark (?) indicates a suspected, but unconfirmed, vectorial connection with the particular dipteran family. Many additional disease-causing agents, particularly viruses, have been isolated from blood-sucking flies, but the role of the flies in transmission of the agents remains largely unknown. † Livestock, poultry, cats, and dogs.

Anaplasmosis, [anthrax], [besnoitiosis], [bovine leukosis], elaeophorosis, equine infectious anemia (swamp fever), [hog cholera], mal de caderas, surra, [additional bacterial and viral diseases and trypanosomiases]

Avian trypanosomiasis, bovine onchocerciasis, [canine Crosskey 1990, onchocerciasis], leucocytozoonosis, vesicular stomatitis Mead et al. 2004, Adler and McCreadie 2009, Hassan et al. 2015

None known

Leishmaniasis (canine and feline), vesicular stomatitis? Bartonellosis (Oroya fever (= Carrion’s disease) and verruga peruana), Chandipura viral disease, Changuinola fever, leishmaniasis (cutaneous and visceral forms), sand fly fever (papatasi fever), vesicular stomatitis?

Psychodidae

[African swine fever], [anthrax], [bovine besnoitiosis], [bovine herpes mammillitis], [bovine leukosis], [cutaneous streptothrichosis], [equine infectious anemia], habronemiasis (summer sores), [lumpy skin disease], [Rift Valley fever], stephanofilariasis, vesicular stomatitis?, [West Nile encephalitis], [additional bacterial diseases]

[Anthrax], [cutaneous streptothrichosis]

Muscidae

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accounts ­summarize the taxonomic status, bionomics, vector-borne diseases, and socioeconomic importance of the 11 families of flies with blood-sucking representatives (Fig. 22.1). The families are listed alphabetically; the sequence would differ if the families were arranged

(a)

(b)

(c)

(d)

(e)

(f)

according to their effect on society, with mosquitoes at the top. 22.2.1 Athericidae

The athericids have one of the lowest profiles of the families with species that feed on vertebrate

Figure 22.1  Representative females of major groups of blood-sucking flies. (a) No-see-um (Ceratopogonidae). (b) Mosquito (Culicidae). (c) Louse fly (Hippoboscidae). (d) Biting snipe fly (Rhagionidae). (e) Black fly (Simuliidae). (f ) Horse fly (Tabanidae). (a–d) and (f ) from Agriculture and Agri-Food Canada with permission under terms of the Government of Canada’s Open Government License; (e) from Adler et al. (2004), © with permission of Cornell University Press.

22  Biodiversity of Blood-sucking Flies

blood. The larvae are predaceous, inhabit streams, and are poorly known taxonomically (Webb 1995). The females of four genera take vertebrate blood. Those of Atrichops feed on frogs and those of Dasyomma and Suragina on mammals, including humans, cattle, and horses, with one record from an owl (Nagatomi and Soroida 1985). Hosts of Suraginella are unknown (Stuckenberg 2000). The athericids have not earned pest status, and are not yet known to transmit pathogens or parasites. 22.2.2 Ceratopogonidae

The family Ceratopogonidae consists of more than 6000 described, extant species in about 110 genera (Borkent 2014). It is the most species-rich family of blood-sucking flies, a status related to the small body size, diverse larval habitats, breadth of larval and adult feeding behaviors, worldwide distribution, and evolutionary age, the oldest fossils being from the Lower Cretaceous. Females of some small genera do not bite, whereas those in the vast majority of genera feed on invertebrates (Downes and Wirth 1981). Only three genera (Austroconops, Culicoides, and Leptoconops) and the subgenus Forcipomyia (Lasiohelea), comprising about 1699 species (Borkent 2014), take the blood of vertebrates including amphibians, birds, fish, mammals, and reptiles. Larvae develop in an impressive range of habitats including coastal marshes, streams, ponds, rotting plants, manure, and phytotelmata (water held by plants). They feed on algae, bacteria, detritus, and small invertebrates. The taxonomy of the immature stages, with a few regional exceptions (e.g., Murphree and Mullen 1991), is poorly developed. In addition to causing nuisance problems by biting, female ceratopogonids transmit at least 66 viruses, 15 species of protozoans, and 26 species of filarial nematodes (Borkent 2005). More than 50 viruses have been isolated from females of the genus Culicoides (Mellor et al. 2000). Two significant human diseases are caused by ceratopogonid-borne agents. Mansonelliasis is caused by three species of filarial nematodes transmitted by biting midges in the Caribbean, northern South

America, and Africa. Oropouche fever, caused by a virus, strikes in the Caribbean and the Amazon region. The most prominent ceratopogonidborne disease of domestic animals is bluetongue, an economically costly, international disease of livestock. African horse sickness, one of the most lethal infectious diseases of horses, is a ceratopogonid-borne viral disease that can cause equid mortality rates in excess of 90% (Mellor et  al. 2000). A recently identified disease of economic consequence is caused by Schmallenberg virus, which manifested suddenly among ruminants in Europe in 2011 (Rasmussen et al. 2012). 22.2.3 Corethrellidae

More than 100 species of frog-biting midges are currently recognized in the world, and nearly 65% of them are in the Neotropical Region (Borkent 2008). Larvae are predators and live in lentic habitats such as pools alongside streams and in phytotelmata. Females feed on the blood of male frogs that they locate by following their calls (Bernal et al. 2006). Some species transmit trypanosomes to frogs (Johnson et al. 1993). 22.2.4 Culicidae

The medicoveterinary importance of the Culicidae has made them one of the taxonomically best known families of arthropods at the species level, with 3546 species of which 97.2% feed on vertebrate blood (Harbach 2015). Higher classification of the Culicidae, however, has proved challenging. It has undergone significant, at times controversial, transformations. Classification systems with as few as 41 genera and as many as 112 are currently in use (Reinert et al. 2008, Gaffigan et al. 2015, Harbach 2015, Wilkerson et  al. 2015). The Culicidae is the only family of insects for which two international journals have been devoted (Journal of the American Mosquito Control Association and the now defunct Mosquito Systematics). The larvae and pupae are known for most species, and the eggs have been described for a greater percentage of species than for any other group of bloodsucking flies.

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Mosquitoes inhabit all regions of the world except Antarctica, and are among the most abundant and conspicuous organisms in areas such as the tundra and boreal forest, although species richness is greatest in the tropics. The larvae and pupae are found in nearly all stillwater habitats, the most common including salt marshes, rain pools, tree holes, artificial containers, pitcher plants, lakes, and swamps. Larvae use a variety of modes, such as filtering, to feed on microorganisms, small macroinvertebrates, and detritus. Females of most species take blood, principally from birds and mammals, but also from amphibians, reptiles, fish, and insects (Rueda 2008). Mosquitoes can become such a nuisance that they disrupt outdoor activity, destroy personal composure, and impede economic development (Laird et  al. 1982). Nuisance problems drive mosquito abatement programs in the United States, involving hundreds of millions of dollars annually. Threats from mosquito-borne diseases, such as West Nile encephalitis, further swell these budgets. Mosquitoes are the terrorists of the arthropodan world. The legions of protozoans, viruses, and other disease agents that they transmit make them the greatest global threat to humanity of any group of organisms other than humans and microbes. They transmit a disproportionate number of pathogens. About half of the more than 500 known arboviruses have been isolated from mosquitoes, and more than 100 infect humans (Karabatsos 1985). New arboviruses continue to be discovered through molecular exploration (Wang et al. 2009). The principal mosquito-borne diseases of humans include arboviral encephalitis, dengue, lymphatic filariasis, malaria, and yellow fever. Human malaria, caused by any of four species of Plasmodium protists transmitted by about 70 species of anopheline mosquitoes, is a devastating disease, with up to half a billion new cases annually in tropical and subtropical regions (Foster and Walker 2009). Although death rates from malaria decreased 47% worldwide from 2000 to 2014, the specter of drug resistance

looms large (ProMED 2014a). Yellow fever, an acute hemorrhagic disease, kills about 30,000 people annually despite the availability of a vaccine since the late 1930s (World Health Organization 2014). Human lymphatic filariasis, caused by three species of nematodes transmitted by more than 60 species of mosquitoes, accounts for more than 120 million active infections (World Health Organization 2015a). Some of the worst-ever epidemics of Aedes-borne dengue, the world’s most rapidly spreading tropical disease, occurred recently. Brazil, for instance, saw nearly 588,000 cases in 2014, while Malaysia’s case load tripled and Taiwan’s increased nearly 17-fold compared with 2013 (ProMED 2014b, 2015a). Also spreading with troubling rapidity is chikungunya fever, another Aedes-borne viral disease (Coffey et  al. 2014). French Polynesia, for example, had about 40,000 cases in 2014, and the tiny Caribbean islands of Guadeloupe and Martinique had well over 50,000 cases (ProMED 2014c, 2014d). These statistics belie the immeasurable socioeconomic burden and losses to future generations through the winnowing of human potential. Many of the mosquito-borne human-disease agents, such as the encephalitides, afflict domestic animals, which also suffer their own unique complement of mosquito-borne diseases. 22.2.5 Glossinidae

Of the 33 species and subspecies of tsetse, 31 are restricted to Africa south of the Sahara, and two are in southwestern Saudi Arabia. Four Oligocene fossil species from the Florissant shales of Colorado suggest that tsetse vexed the American megafauna during the Age of Great Mammals. The family is well known taxonomically. The last new species was named more than 20 years ago, and the adults and about half of the puparia of all species and subspecies have been described (Jordan 1993). The taxonomic status of a number of taxa, however, remains unresolved, and morphological and molecular data do not always produce reciprocally monophyletic groups (Dyer et al. 2011).

22  Biodiversity of Blood-sucking Flies

Females have a low lifetime fecundity, maturing one egg at a time and nurturing the larva in the uterus. The final (third) instar is deposited on the ground and within a few hours transforms into a puparium in the soil. Both males and females take blood. Hosts include reptiles (e.g., crocodiles), large mammals (e.g., buffalos, giraffes, humans, rhinoceroses, and suids), and occasionally birds (e.g., ostriches). Despite transmitting only about seven recognized species of trypanosomes to mammals (Jones 2001), tsetse have had a powerful influence in Africa. The trypanosomiases – sleeping sickness in humans and nagana in livestock  –  have caused enormous human suffering, inhibited economic development, and restricted animal agriculture, while also serving as the single greatest conservator of the African savannah by restricting the encroachment of humans and livestock (Harwood and James 1979, Krinsky 2009). 22.2.6 Hippoboscidae

The 780-plus species of the worldwide family Hippoboscidae sensu lato sometimes are divided among three discrete families, the Hippoboscidae sensu stricto, Nycteribiidae, and Streblidae. The latter two taxa, comprising more than 70% of the Hippoboscidae sensu lato, are obligate ectoparasites of bats and have little known relevance to the health and welfare of humans or domestic animals. About 75% of the Hippoboscidae sensu stricto are ectoparasites of birds, with the remainder on mammals other than bats. Species richness is greatest in the Neotropics. All known species of the Hippoboscidae sensu lato are larviparous, nourishing a single larva, which forms a puparium upon deposition. Both sexes are obligate blood feeders. Among the bird and mammal feeders, each species is exclusively mammalophilic or ornithophilic. No species habitually feeds on humans, but some attack domestic animals. Premier among them is the sheep ked (Melophagus ovinus), an economically important pest of sheep that causes

damage to pelts. A few species of hippoboscids transmit trypanosomes and apicomplexan parasites to domestic pigeons, and some transmit parasites and pathogens to wildlife (Lloyd 2009). Hippoboscids are probable vectors of Bartonella and other pathogenic bacteria among bats (Billeter et al. 2012). The role of hippoboscids in transmitting disease agents is probably grossly underappreciated. 22.2.7 Muscidae

The biting muscids include members of the subfamily Stomoxyinae and one species (Musca crassirostris) in the subfamily Muscinae. The number of described morphospecies has plateaued at 57; only two new species have been described in the past 35 years (Braack and Pont 2012). About 70% of the species are in the Afrotropical region. The larvae and puparia of about 15% and 6%, respectively, of the biting species are described. The larvae typically develop in dung associated with hosts of the adult flies. Larvae of the stable fly (Stomoxys calcitrans) also develop in decomposing vegetation, especially grass cuttings. The males and females of all biting muscids feed on mammalian blood, although some probably feed from sores and host exudates rather than pierce the hide (Zumpt 1973). Humans can be annoyed by some species, especially the stable fly. Ungulates are hosts of most species. The two principal livestock pests are the widely distributed horn fly (Haematobia irritans) and the cosmopolitan stable fly. Both species cause anxiety, decreased immunological response, reduced milk production, and weight loss (Moon 2009). The stable fly is responsible for about US$2 billion in economic losses each year in the United States (Taylor et al. 2012). The stomoxyines, at least under laboratory conditions, are capable of transmitting a number of pathogens, some by mechanical means: that is, by contamination of the mouthparts (Baldacchino et al. 2013). The horn fly and stable fly transmit spirurid nematodes that cause cutaneous diseases known as habronemiasis in horses and stephanofilariasis in cattle.

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22.2.8 Psychodidae

The 1000-plus species of biting psychodids, or sand flies, are restricted to two subfamilies: the Phlebotominae (sometimes considered a separate family) and the Sycoracinae. These subfamilies are widespread on all continents except Antarctica, although more than half of the species are Neotropical. Taxonomic knowledge of the immature stages, with some exceptions (Hanson 1968), is restricted to species of concern to human health. Sand flies develop in damp terrestrial environments, where the larvae feed on decaying organic matter. Female phlebotomines feed on amphibians (toads), birds, mammals, and reptiles, and include the major vectors (Lutzomyia and Phlebotomus) of human-disease agents. Females of the seldom-encountered sycoracines feed on frogs. Most sand flies have broad host ranges (Rutledge and Gupta 2009), which might reflect undiscovered cryptic species. Biting by sand flies can be annoying, but their medical importance is related to the bacterial, protozoan, and viral agents they transmit. Foremost among the human diseases are the cutaneous and visceral forms of leishmaniasis, caused by about 23 protozoan species of Leishmania transmitted by about 70 to 80 species of sand flies (Lawyer and Perkins 2000, Ready 2013). The World Health Organization (2015b) estimates that there are 1.3 million new cases annually. Phlebotomineborne viruses cause an influenza-like illness, sand fly fever, and several additional geographically local human diseases. Bartonellosis is a human disease caused by phlebotomine-borne bacteria in Colombia, Ecuador, and Peru. Sand flies have little veterinary importance, although they might be involved in transmission of the causal agents of leishmaniasis to dogs, the latter serving as a reservoir for human infection (Ostfeld et al. 2004). 22.2.9 Rhagionidae

Of the 21 genera of Rhagionidae, only the Australian Spaniopsis and the Holarctic Symphoromyia include species that feed on ver-

tebrate blood. The poorly known immature stages live in moist soil. Larval feeding habits are sketchy but apparently involve detrital feeding and possibly facultative predation. The actual number of species of Symphoromyia is considered to be greater than the 32 currently recognized (Turner 1974). Molecular work is needed to resolve existing species issues and reveal cryptic species. The females of Spaniopsis feed on humans and probably other mammals. Those of Symphoromyia acquire blood from a wide range of hosts, including cattle, deer, horses, and humans, and are significant pests in some areas of western North America and Central Asia (Turner 1974). No animal pathogens or parasites are known to be transmitted by the females of Spaniopsis or Symphoromyia. 22.2.10 Simuliidae

Black flies are distributed worldwide between 55 °S and 73 °N, but are absent from some oceanic islands and areas without flowing water. Species richness is greatest in the Palearctic region based on current numbers, although this status is likely to change as the Neotropical and Oriental Regions are further explored. The larvae require flowing water and are often the numerically dominant macroinvertebrates in lotic habitats (Adler and McCreadie 1997, Malmqvist et al. 2004). The family is one of the more completely known among hematophagous flies, largely because of the routine practice of describing the larva, pupa, male, and female of new species; the extensive use of cytotaxonomy (Adler and Crosskey 2015a); and the well-defined habitat of the larvae and pupae, which facilitates the collection of immatures and association of life stages. The females of all but about 2.5% of the world’s 2177 species take blood (Adler and Crosskey 2015b). Hosts are restricted to birds and mammals. Black flies are major biting and nuisance pests and are the only insects that have routinely killed animals by exsanguination and toxic shock from injected salivary components (Crosskey

22  Biodiversity of Blood-sucking Flies

1990). No species is strictly anthropophilic, but many take blood from humans (Adler et al. 2004, Adler and McCreadie 2009). Two species of filarial nematodes cause diseases in humans. Onchocerca volvulus causes human onchocerciasis in equatorial Africa, southern Yemen, and localized areas of Central and South America (Adler et al. 2010). Although the World Health Organization estimated that about 18 million people were afflicted in 1995, subsequent evidence suggested that the figure should have been 37 million heavily infected people (Remme et al. 2006). Landmark achievements have come in the fight against onchocerciasis. Transmission has been interrupted or eliminated in 11 of the 13 New World foci, with only the Yanomami people requiring continued treatment with the human formulation of ivermectin in Brazil and Venezuela (World Health Organization 2015c). Colombia was declared onchocerciasis-free in 2013 and Ecuador in 2014; Guatemala and Mexico are expected to follow. Mansonella ozzardi causes mansonelliasis, a marginally pathogenic disease in the rainforests of Brazil, Colombia, Guyana, Venezuela, and southern Panama (Adler and McCreadie 2009). Domestic fowl are plagued by simuliidborne Leucocytozoon protists, cattle are infected by the more benign filarial worm Onchocerca lienalis, and dogs occasionally are infected with Onchocerca lupi (Crosskey 1990, Hassan et al. 2015). 22.2.11 Tabanidae

The large size of tabanids, often eliminating the need for a microscope in routine identification, has appealed to taxonomists and promoted the primarily morphological approach to their taxonomy, revealing more than 4400 species. Morphotaxonomy, nonetheless, sometimes suggests the presence of cryptic species, confirmed in some instances or revealed de novo by additional, typically molecular, techniques (Sakolsky et al. 1999, Banerjee et al. 2015). The larvae and pupae require diligent searching to locate and are moderately well known only in the Nearctic

Region (e.g., Burger 1977); only about 5% of the species are known as immatures in the Neotropical Region (Coscarón and Papavero 2009). Tabanids are present throughout the world, primarily below the tree line. The larvae are generalist predators and inhabit wet soil and debris in bogs, marshes, ponds, and stream margins, although some species live in drier soil and tree holes. Females feed chiefly on mammals and occasionally amphibians, birds, and reptiles. Species of Goniops, Stonemyia, the subfamily Scepsidinae, the tribe Mycteromyiini, and an unknown number of additional species do not take blood. Humans and livestock are annoyed by deer flies and horse flies. The only human disease that is consistently tabanid-borne (via Chrysops) is loiasis, caused by a filarial nematode known as the African eyeworm (Loa loa). Tabanids, along with stomoxyines, are considered the most important blood-feeding flies responsible for mechanical transmission of pathogens; a long list of pathogens and parasites has been associated with tabanids, but the epidemiological role of these flies is generally unknown (B. Mullens 2009, Baldacchino et  al. 2014). The bacterium that causes tularemia, for example, can be transmitted mechanically, although the proportion of human and livestock cases attributable to infection via tabanids is unknown.

22.3 ­Rationale for Biodiversity Studies of Blood-sucking Flies A major objective of biodiversity studies is to document all species on Earth. New biological riches (e.g., foods and medicinal compounds), aesthetics, the impending loss of species, and matters of conservation typically justify biodiversity studies of most organisms. Beyond the unifying goal of documenting species, the chief motives driving biodiversity studies of bloodsucking flies are likely to diverge from those for other organisms. Threats to human and animal welfare, such as economic losses and disease epidemics caused by pests and vectors, motivate

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biodiversity research on blood-sucking flies, with the ultimate goal of eliminating the risk. Yet, among blood-sucking flies, only one of the four life stages, and often only the female, directly creates risk. The male and pre-adult stages, particularly the larval stage, often perform key functional roles in the environment (Malmqvist et  al. 2004). Larval black flies, for example, have been termed “ecosystem engineers” because they have a vital role in processing dissolved and particulate matter into larger fecal pellets used as food by other aquatic organisms and as fertilizer for flood-plain vegetation (Wotton et  al. 1998, Malmqvist et  al. 2004). A trade-off thus exists between reducing the troublesome adult stage and conserving the beneficial immature stages. Ironically, the larval stage often is targeted for control of the adult pest or vector. Complicating matters further, adult blood-sucking flies can play an integral part in the environment as pollinators, food for predators, and regulators of wildlife populations (Malmqvist et al. 2004). One would find it difficult to argue for conservation of the yellow fever mosquito (A. aegypti), a vector not only of the virus of its namesake but also, inter alia, chikungunya virus, dengue viruses, and Ross River virus. Little attention was paid, for example, when an onchocerciasis vector in the S. damnosum complex putatively was driven to extinction as a result of control efforts (Cheke et al. 2008). The intrinsic difficulties of eradicating a vector, the unintended consequences of doing so, and the desire to maintain all life forms can be addressed by breaking the cycle of disease while conserving the vector. The transmitted causal agent can be targeted with drugs given to the vertebrate hosts, and vector populations can be suppressed to levels sufficient to disrupt the transmission cycle. Well into the 1930s, malaria was one of the major socioeconomic burdens in much of the United States, afflicting 6 million to 7 million people annually and reducing the South’s industrial potential by about one-third (Russell 1959, Desowitz 1998). Dichlorodiphenyltrichloroethane (DDT), antimalarial drugs, habitat alteration (e.g., oiling and

draining of wetlands), and improved standards of living eventually broke the cycle (Adler and Wills 2003). The principal vectors, members of the Anopheles quadrimaculatus complex, remain common in the formerly malarious regions of the southern United States. The Plasmodium species responsible for human malaria, however, are essentially gone from the areas where they were unintentionally introduced by the slave trade. The dilemma of conserving or eliminating hematophagous flies is epitomized by the black fly Simulium ochraceum (formerly Simulium bipunctatum) in the Galápagos Islands. Simulium ochraceum was discovered in the archipelago (on San Cristóbal) in 1989 (Abedraabo et al. 1993) and has since become a serious biting pest of humans, causing some residents to abandon their farms. Because of limited breeding sites, the black flies could be eradicated from the archipelago by applying the larva-specific biopesticide Bacillus thuringiensis var. israelensis. The crucial issue is whether the species is a recent introduction, as some authors (Abedraabo et al. 1993) maintain, or has been in the archipelago for longer. The distinction is significant because if it has long been present, it might be a keystone species, serving as the basis of the food web for other aquatic invertebrates; in this scenario, its eradication could disrupt the island’s flowing-water ecosystem. Simulium ochraceum is actually a species complex of at least two cryptic species in Central and South America, one or more of which transmits the causal agent of human onchocerciasis (Hirai et al. 1994). Still unknown is which member of the complex is present in the Galápagos Islands and to what extent it has diverged from mainland populations. Cytogenetic and molecular techniques are now being used to determine the identity of the insular species, as well as its mainland source, extent of divergence, and length of time in the Galápagos Islands. Similar quandaries will continue to arise as land use changes and as the interface between civilization and raw nature expands. Persistent incursions into undeveloped areas of the tropics

22  Biodiversity of Blood-sucking Flies

expose people to new and greater risks of vector-borne diseases (Basáñez et  al. 2000), while development projects (e.g., irrigation) increase the prevalence of diseases such as leishmaniasis (Lane 1993). Regardless of the motivation for biodiversity studies of blood-sucking flies, the deep understanding that has accrued from such studies has fostered the use of hematophagous flies as research models in areas applicable to other organisms. Blood-sucking flies have provided models for studies of community ecology (McCreadie and Adler 1998), genomic mapping (Holt et  al. 2002), host–symbiont evolution (Chen et  al. 1999), filter feeding (Merritt et  al. 1996), island biogeography (Craig 2003), speciation (Rothfels 1989), transgenic arthropods (Alphey et al. 2002), and a bounty of other relevant topics.

22.4 ­Biodiversity Exploration Progress in documenting the biodiversity of blood-sucking flies has been uneven among families. This imbalance stems not only from the differential health and economic importance of the various families to society, but also from the largely independent research efforts for each family, embracing different terminologies, techniques, and philosophies. These independent trajectories are maintained by specialists who typically confine their work to a single group. Progress, however, has been made in homologizing structures and, hence, terminology across families (Sinclair et  al. 2007). The Manual of Nearctic Diptera, for instance, provides a lingua franca of morphological terms for larvae and adults, although rarefied family-specific terms persist, especially for genitalia and pupae. Tools and approaches are applied variously among families. Polytene chromosomes have played an integral part in the taxonomy of some groups but not others; yet even among the groups for which cytotaxonomy has been practiced routinely (Culicidae and Simuliidae), the terminology and the discoveries are typically

family specific. More than 110,000 specimens of blood-sucking flies have been DNA-barcoded, about half of which are mosquitoes (BOLDSYSTEMS 2014). Although barcoding, at least for the moment, is often an expected approach to biodiversity exploration and species identification – its controversial nature not withstanding (Besansky et  al. 2003, Rubinoff et  al. 2006)  –  it, and other molecular tools, is applied routinely only in certain groups of hematophagous flies, particularly those that transmit disease agents. The criteria used to define species also vary among groups (and even among methods). Morphological criteria are used to define most species, although cytological and molecular criteria also are used in the Culicidae and Simuliidae. Subspecies are recognized in some families (e.g., Culicidae and Glossinidae) but not others (e.g., Corethrellidae and Simuliidae). In some groups of flies, certain taxonomic methods have been more profitable than others. In black flies, a group in which speciation likely has been driven by chromosomal rearrangements (Rothfels 1989), cytological approaches have been instrumental in the discovery and resolution of species (Adler et  al. 2010). More than 650 papers, representing about 25% of all nominal species, have appeared on the subject – the most extensive literature on the genetics of natural populations for any group of organisms (Adler and Crosskey 2015a). The Simuliidae provide the lesson that significant biodiversity lies hidden, not only as cryptic (sibling) species, but also as homosequential sibling species (Bedo 1979). Although chromosomes currently provide the most powerful tool for revealing hidden species in the Simuliidae, they are useful, with notable exceptions (Bedo 1976), only for middle- to late-instar larvae. Molecular prospecting now occurs routinely in black flies (Krüger et  al. 2006, Pramual and Adler 2013, Hernández-Triana et  al. 2015), and has been applied successfully to resolve difficult taxonomic problems (Conflitti et al. 2015). The Ceratopogonidae, like all medically important Diptera, present a weight of challenges,

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which will be addressed most profitably through integrated morphological and molecular approaches in the context of rapidly emerging technologies (Harrup 2015). The small size of ceratopogonids seems to have put chromosomal studies beyond a willing limit of effort. Isozyme studies provided early examples that molecular techniques can provide a profitable approach to species questions, demonstrating that the ceratopogonid Culicoides variipennis is a complex of three reproductively isolated species (Holbrook et al. 2000). Molecular investigations of the economically important Ceratopogonidae are picking up pace (Mathieu et  al. 2007), simplifying identification and revealing additional cryptic biodiversity (Ander et al. 2013). Among mosquitoes, cytogenetic techniques have been invaluable in revealing cryptic species, although not all mosquitoes are readily amenable to band-by-band chromosomal analysis. The polytene chromosomes of anophelines are often workable, but those of many culicines prove difficult, although the limits of the technique can be pushed (McAbee et  al. 2007)  –  for example, by using Malpighian tubules rather than the standard tissues such as larval salivary glands (Zambetaki et  al. 1998, Campos et  al. 2003). Molecular techniques are used routinely to reveal and discriminate cryptic species of mosquitoes (Kengne et al. 2003, Benet et al. 2004, Wilkerson et al. 2004, Gómez et al. 2015) and have largely supplanted cytogenetic approaches. Molecular techniques, from DNA barcoding (Cywinska et al. 2006, Kumar et al. 2007, Linton et al. 2013, Ruiz-Lopez et  al. 2013) to whole-genome sequencing, will play an increasingly prominent part in routine mosquito taxonomy. Morphological approaches historically have dominated phlebotomine taxonomy. Chromo­ somal studies have been limited (White and Killick-Kendrick 1975, Ready 2013). Molecular techniques increasingly are being brought to bear on species problems of phlebotomines, and although about 20% of the known species have been evaluated using the tools of molecular systematics, most studies have examined evolutionary systematics rather than species-level

taxonomy (Depaquit 2014). Protein profiling (matrix-assisted laser desorption/ionization-time of flight mass spectrometry (MALDI-TOF MS)) has been introduced as an approach to the identification of sand flies (Mathis et al. 2015). Similarly to many molecular studies, most protein-profiling research on sand flies has focused on major vector complexes associated with human leishmaniasis. For several decades, the Neotropical sand fly Lutzomyia longipalpis was suspected of being a species complex. Isozymes, molecular data, and pheromonal chemistry supported this notion and revealed at least four cryptic species (Arrivillaga et  al. 2003, Hamilton et  al. 2004). Similarly, the Mediterranean Phlebotomus perniciosus complex consists of cryptic species (Pesson et al. 2004). Establishing the vectorial abilities of each of these cryptic species should help to explain observed differences in the distribution and clinical manifestations of leishmaniasis, and ultimately improve vector-management strategies (Lanzaro and Warburg 1995). Tsetse have a rich history of classic genetic studies (Gooding and Krafsur 2005), and are now frequent subjects of molecular investigation. Polytene banding patterns, although little studied, are information rich (GariouPapalexiou et  al. 2007). Evidence for cryptic species among tsetse is compelling (Krafsur 2009). Hybridization between some subspecies results in male sterility of the offspring (Gooding 1985), and heterozygote deficiencies and linkage disequilibria occur within other subspecies, indicating population substructuring (Luna et al. 2001) that might reflect cryptic species or incipient species. Of particular interest with regard to the hidden biodiversity of tsetse is the potential variation in the ability to transmit trypanosomes. For the remaining families, morphological approaches to species questions continue to dominate, despite the option of using molecular and other techniques. The few chromosomal studies on the Tabanidae have been of a simple, karyotypic nature (Altunsoy and Kiliç 2010). Early on, enzyme electrophoresis established the validity of two cryptic species of salt marsh

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greenheads, Tabanus conterminus and Tabanus nigrovittatus (Jacobson et al. 1981), and cuticular hydrocarbon analysis later corroborated their existence and revealed a probable third species (Sutton and Carlson 1997). DNA barcoding typically supports morphologically defined species of tabanids and reveals cryptic species (Cywinska et al. 2010, Banerjee et al. 2015). With time, biodiversity prospecting in bloodsucking flies will come to rely heavily – some think exclusively – on molecular techniques. This suborganismal approach might uncover the genetic basis for reproductive isolation. Molecular, chromosomal, and morphological approaches, however, reflect hierarchical scales of investigation; information at one scale might not be accessible at another scale. A pluralistic approach, zooming in and out on the biodiversity scale, although not always producing concordance (della Torre et al. 2001, 2002), is likely to be the most illuminating strategy. Despite the value of a synthetic approach, the trend is swinging toward an exclusively molecular approach, propelled by the increasing ease, speed, and accessibility of molecular techniques, whereas cytogenetic and morphological techniques remain relatively difficult and time consuming (Adler and Crosskey 2015a). Laboratory aspects of revealing and describing the biodiversity of blood-sucking flies are often corroborated, informed, or initiated when biological discrepancies (e.g., in seasonality or host usage) are observed in natural populations. Future studies of biodiversity must integrate the study of dead specimens with information from populations in nature. For a complete appreciation of hematophagous-fly biodiversity, scientists must strive for an understanding of living organisms, including habitat preferences, reproductive behaviors, and interactions with other organisms.

22.5 ­Societal Consequences of Disregarding Biodiversity Accurate identification is crucial to all scientific research and its applications, perhaps no more so than when dealing with blood-sucking pests

and vectors. Yet misidentification is rampant in the literature on blood-sucking flies, owing in part to the similarity among so many species, the dwindling numbers of specialists, and the lack of mandatory taxonomy and systematics courses. More than 600 misidentifications have been documented in the 2200 or so articles and theses on North American black flies (Adler et  al. 2004). Misidentifications can disrupt economies, waste money, and cost lives. The misidentification of Anopheles varuna, a nonvector of malarial agents, misdirected efforts to control the actual vector in central Vietnam (Van Bortel et  al. 2001). Misidentification of another non-vector, Anopheles filipinae, in the Philippines set the stage for similarly unproductive management efforts (Foley et  al. 1996). Targeting the wrong species also could exacerbate the pest or disease problem by opening habitat for development of the real villain. The success of antimalarial programs is inversely correlated with the biodiversity of the vectorial system (Coluzzi 1984). Failure to recognize all entities of the system compromises success. Efforts to manage pests and vectors biologically – for example, by introducing sterile males, genetically engineered individuals, or host-specific natural enemies – must ensure compatibility with the targeted populations. At special risk for misidentification are the morphologically similar, if not identical, cryptic (sibling) species and the more covert homosequential sibling species. Given their frequency and the difficulty in recognizing them, the chance of misidentification is considerable. The different vectorial capacities of cryptic species underscore the importance of precise identification (Adler et  al. 2010). The demonstration that the biting midge C. variipennis is actually three distinct species, only one of which (Culicoides sonorensis) is a principal vector of bluetongue virus in North American ruminants, implies that vector-competence genes have a low probability of flowing from C. sonorensis to C. variipennis sensu stricto (Holbrook et al. 2000). The significance for North American agriculture is that livestock and germplasm can be moved more freely from blue-

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tongue-free areas of the United States to bluetongue-free countries. At least half of the major vectors of human malarial agents belong to complexes of cryptic species (Krzywinski and Besansky 2003). The seven or more cryptic species in the An. gambiae complex differ in their ability to transmit human malarial agents, ranging from non-vector to highly competent vectors (Coluzzi 1984). Only a few of the 10 or more cryptic species of African biting midges in the Culicoides imicola complex have been implicated in the transmission of African horse sickness virus (Meiswinkel 1998, Mellor et  al. 2000). Of the 30 cryptic species and cytoforms in the S. damnosum complex in northeastern Africa and East Africa, only six have been incriminated as vectors of the filarial parasite responsible for human onchocerciasis (Post et al. 2007). Further, the vector species of the S. damnosum complex show differential susceptibilities and resistance to insecticides, so accurate identification is required to monitor the development and spread of resistance genes (Kurtak 1990). A synthetic approach is needed to avoid misidentifications, reveal and delineate hidden biodiversity, clarify pest status and epidemiological complexity, and generally keep biodiversity discoveries flowing. Molecular techniques are now part of the toolkit that includes the tried-andtrue methods of classical systematics. Molecular methods provide a reliable means of linking immature stages with adults (including type specimens), and of identifying specimens in poor condition, larvae too young for morphological or chromosomal identifications, and eggs for which no structural characters or species association have been found. No single method, however, is likely to answer all questions regarding species. Even the powerful triumvirate of cytotaxonomy, morphotaxonomy, and molecular taxonomy sometimes fails to resolve or provide concordance for certain crucial species issues among disease-bearing flies such as the An. gambiae complex (della Torre et  al. 2001, 2002). Additional technologies, such as cuticular hydrocarbon analysis (Kather and Martin 2012), have been used in most groups of blood-sucking

flies and generally, although not always, corroborate species limits based on other criteria (Carlson et al. 1997). The resolution of five cryptic species in the North American An. quadrimaculatus complex, using biochemical, chromosomal, ecological, hybridization, molecular, and morphological techniques (Reinert et al. 1997), provided an early blueprint for multifaceted approaches. An integrated strategy also will be needed to relate the vectorial capacity of the five cryptic species of the complex to the 15 or more disease agents they transmit. New approaches and techniques promise exciting advances across multiple levels of biodiversity investigations of blood-feeding flies. The complete-genome sequencing projects now underway for a number of hematophagous Diptera promise to open new frontiers of investigation. Some genomes already have been completed and are beginning to yield new insights (International Glossina Genome Initiative 2014). Although they can be illuminating, novel approaches and techniques also bring problems, some immediately apparent, others latent. A problem of the molecular age is that some (many?) sequences in public databases are linked with misidentified species; this problem surfaced early on for mosquitoes (Krzywinski and Besansky 2003) and continues to plague genetic databases (Grens 2015). To avoid these mistakes, molecular biologists must work collaboratively with morphotaxonomists and cytotaxonomists. More importantly, future biodiversity researchers must be au fait with each of these techniques and capable of applying them to solve the thornier problems. They must “be emboldened to venture across the dissolving disciplinary barriers” (Kafatos and Eisner 2003).

22.6 ­Present and Future Concerns To further guard against misidentifications and facilitate future discoveries of hidden biodiversity, voucher specimens must be deposited in accessible institutions. They provide a measure

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of immortality to an author’s work by permitting subsequent verification or recalibration if hidden diversity is discovered. They also provide a historical basis for evaluating genetic and morphological changes over time, both in natural populations and in laboratory colonies. The notorious cattle pest of the Canadian Prairies, responsible for the deaths of more than 3500 head of cattle since 1886, was long known as Simulium arcticum. In reality, it was an entirely different and undescribed species, subsequently named Simulium vampirum (Adler et al. 2004). So abundant at times that it formed a loud, buzzing fog, the species later proved difficult to study taxonomically because limited specimens had been deposited in museums before it was eradicated from much of its former habitat; evidently, it was so abundant that previous researchers saw little need to deposit material in museums. Future researchers hoping to track the genetic changes from a time of superabundance to virtual extermination (bottleneck) will be challenged to find adequate historical material of this species. More generally, future workers are not likely to view present vouchering practices approvingly. Of 84 articles on hematophagous flies published in the Journal of Medical Entomology in 2003, only 5% mentioned the deposition of voucher specimens  –  the other 95% represent an enormous potential loss of future information. By 2014, the situation had not improved acceptably: 13% of 86 articles on hematophagous flies indicated the deposition of vouchers. Voucher specimens and type series can include not only actual specimens, but also chromosome preparations, preferably with photographs that ensure permanency should the chromosome preparations prove unstable over time (Adler and Kim 1985). Images of biochemical and molecular gels, as well as genetic sequences, similarly can be deposited as complementary items to actual specimens or specimen parts. Although researchers typically deposit genetic sequences in public databases, the disposition of the actual specimen often is not addressed. A gene sequence without the

organismal carcass is inadequate and eliminates future extraction of additional information. So that representative material might be available in depositories for future scrutiny and analysis, the practice of grinding an entire organism for molecular analysis, or grinding a portion and discarding the remainder, must be avoided. At a time when the need for collections and storage of biological material is critical, administrators are calling for the downsizing, sale, or abandonment of collections. Such myopic calls are epitomized by the suggestion of a former administrator at one North American institution to replace the specimens in “space-consuming cabinets” with two-dimensional photographs that could be stored in compact files. Solutions are not easy, but any that do not allow for storage of actual specimens are unsatisfactory. No scientist has the prescience to predict what information will be required from museum specimens that otherwise would be unavailable from photographs, CD-ROMs, and other ersatz items. Nor can the techniques be foreseen that one day might be used to extract information from real specimens. With continued destruction of habitat and concomitant extinctions, all we ever will know of some species will be the information associated with real specimens housed in collections (Wheeler 2004). The greatest need facing future biodiversity studies of blood-sucking flies is a pervasive appreciation of the value of the work and the importance of organismal education. All other needs flow logically from this perspective. Currently, an appreciation is held by only a small cadre of scientists and lay people. A certain irony in acknowledging the value of ­ biodiversity issues comes from the World ­ Health Organization Onchocerciasis Control Programme in Africa. The cytotaxonomists whose discoveries of cryptic species in the S. damnosum complex allowed more precise targeting of the vectors of Onchocerca volvulus nonetheless repeatedly had to justify their efforts to identify the vector species in control programs (Meredith 1988). A majority of all students now graduate from college without an

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adequate understanding of the biodiversity crisis or how blood-sucking flies and vector-borne diseases could affect their lives. Yet another irony, and a dangerous pitfall, is success itself. Effective control can become the enemy of continued biodiversity exploration. The heady success of DDT in controlling malaria, beginning in the late 1940s, led to a false belief that mosquito biologists were no longer needed; a generation or more went untrained, by which time resistance to DDT, and to certain antimalarial drugs, had become entrenched. The unprecedented success of B. thuringiensis var. israelensis against black flies has damped not only studies of natural enemies (Adler et al. 2004), but also studies of the family in general. “Every insect taxon needs a fanatical specialist who will make a life of passionate proprietary concern for his own personal charges” (Lloyd 2003). To improve on James Lloyd’s sentiment, we need only pluralize “specialist” and adjust the corresponding orthography. Yet, the number of trained specialists continues to dwindle while the hackneyed plea goes out for more taxonomic expertise. In more than 250 years of describing and naming blood-sucking flies, about 430 people have authored or coauthored formal species names for the world’s black flies, averaging roughly 5.0 valid species per author. About 50 authors have named biting muscids, for an average of 1.1 valid species and subspecies per author. For tsetse and corethrellids, 24 authors each have described species and subspecies, or about 1.4 and 4.0 valid taxa, respectively, per author. Perhaps with more sophisticated techniques, in the context of rapid information processing, the task of describing all species might be completed with fewer workers, although this view seems naively optimistic. Current papers dealing with complex species problems often involve seven or more authors (e.g., della Torre et  al. 2002, Arrivillaga et  al. 2003, Pesson et al. 2004, Adler et al. 2015). The dynamic, coevolutionary system of vector, vertebrate host, and disease agent requires vigilant monitoring to protect human and ani-

mal welfare. Current control practices and the rapidly changing nature of the world’s ecological landscape exert intense and swift selection on pests and vectors, the development of pesticide resistance being a textbook example. One does not need to look far to find examples of novel environments, complete with native and imported hosts, pathogens, and vectors. Zoos provide classic examples where all of these elements mix freely (Adler et al. 2011), and mosquitoes routinely form bridges among all players in zoos (Tuten et al. 2012). As a result of habitat disturbance and resistance stemming from long-term, repeated insecticide applications in the Onchocerciasis Control Programme area of Africa, two cryptic species in the S. damnosum complex, S. damnosum sensu stricto and Simulium sirbanum, are hybridizing at increased rates (Boakye et  al. 2000). The danger is that genetic material could be transferred from one species to the other, giving rise to new variants or even new species, and compromising vectorcontrol programs. This scenario has been described for mosquitoes in the Culex pipiens complex, which are vectors of West Nile virus. Molecular data suggest that, in the United States, hybridization between the bird-feeding Cx. pipiens and the mammal-feeding Culex molestus (recognized by some workers as a physiological form of Cx. pipiens) has produced efficient vectors that are able to transfer the virus from birds to humans (Fonseca et al. 2004). Similarly, the increased use of insecticidetreated bed nets in Mali favored hybrids of Anopheles coluzzii and An. gambiae, rapidly sweeping the insecticide-resistant genes into An. coluzzii (Norris et al. 2015). Because some species of the An. gambiae complex feed exclusively on humans and breed in artificial containers, which have been available for fewer than 10,000 years, at least some radiation within the complex might have occurred in recent times (Coluzzi et al. 2002). Ongoing speciation within cryptic species of the An. gambiae complex complicates the control of malaria in Africa by extending the transmission potential of the vectors in space and time (della Torre et al. 2002).

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New disease concerns are likely to emerge from previously unappreciated or de novo vector–pathogen relationships. Schmallenberg virus, transmitted by Culicoides, erupted suddenly in 2011 across a large swath of Europe (Rasmussen et al. 2012). The origin of the disease is obscure, but illustrates the importance of biodiversity efforts to link the species of disease-causing agents with their dipteran hosts. The total number of zoopathogens transmitted by blood-sucking flies is unknown, not only because the taxonomy of some microorganisms is poorly developed or confused, but also because many hosts of minimal economic importance (i.e., wildlife) have not been surveyed for pathogens, or the pathogens have not been associated with the vectors. More than 80 species of Leucocytozoon are known from well over 50 families of birds (Peirce 2005), but only a fraction of the species has been linked with vectors (all Simuliidae, except one Ceratopogonidae) (Valkiūnas 2005, Adler and McCreadie 2009). Species resolution of disease-causing organisms, such as protozoans, historically has been difficult because of a dearth of morphological characters. With the ever-increasing sophistication of molecular methods, however, the remarkable biodiversity of these microorganisms is coming to light (Murdock et  al. 2015). Based on the prevalence of cryptic species among vectors, the transmitted microorganisms also might be expected to consist of cryptic species. Molecular evidence consistently supports this hypothesis: for example, in the genus Leucocytozoon (Sehgal et al. 2006, Hellgren et al. 2008). A corollary hypothesis is that the vector specificity and vertebrate-host specificity of transmitted disease agents is greater than currently realized. Molecular approaches also have proven useful in groups such as the tsetsetransmitted Trypanosoma in which species in some subgenera have been over-split, whereas species richness in other subgenera has been underestimated (Gibson 2003). As a final caveat, new disease concerns are likely to emerge as a result of climate change.

The increasingly hot weather and heavy rainfall associated with climate change promote the spread of vectors and reduce their coldrelated mortality, intensifying the associated disease burden, particularly as the vectors move into areas of the world with immunologically naive human and livestock populations. Another aspect of climate change, drought, has been blamed for malaria outbreaks by forcing the vectors to search for breeding sites in new areas that are free of the disease (ProMED 2015b). Teasing the effects of climate change apart from other factors, however, will prove challenging. Initial claims that climate change drove the major Old World vector of bluetongue virus into new areas of Europe and allowed bluetongue virus to expand its range, putatively through the involvement of novel Culicoides vectors (Purse et  al. 2005), have been called into question with subsequent molecular analyses (Mardulyn et al. 2013). The rapid spread of Aedes albopictus over large portions of the globe is fueling outbreaks of diseases, such as chikungunya, with increased potency (Enserink 2008).

22.7 ­Conclusions More than 18,200 species of blood-sucking flies have been described, of which about 75% take blood from vertebrates. The Neotropics are richest in species, although new species continue to be discovered in biodiversity hotspots and inadequately sampled areas throughout the world. Still more biodiversity remains to be harvested from the genomes of currently known species. Structurally similar cryptic species are revealed routinely when appropriate techniques are applied, with some morphospecies consisting of as many as 50 cryptic species. What do biodiversity studies of hematophagous flies reveal about other groups of organisms? More than anything, they suggest that estimates of the total number of life forms are too low. Most estimates of life’s richness are based on known numbers of morphospecies,

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failing to account for cryptic (sibling) species and homosequential sibling species that, with closer scrutiny or more sophisticated techniques, await discovery. The plurality of approaches used to uncover hidden biodiversity in particular groups of blood-sucking flies provides a template for biodiversity investigations of other organisms. As a final thought, we must appreciate that discovering, describing, and cataloging the rich biodiversity of blood-sucking flies is not an end point, but rather a means of addressing a multiplicity of questions directly relevant to the future of humanity. Blood-sucking flies, as pests and vectors, have profoundly influenced human history and continue to exact a brutal toll. They are responsible for more than 1.25 million human deaths annually and an incalculable socioeconomic burden. Threats to human and animal welfare arise not only from well-known pests and vectors, but also from undiscovered species, recent invasive species, novel vector– microorganism associations, and environmental dynamics that foster hybridization and exchange of genomic material between vector taxa. The degree to which risks are eliminated is directly correlated with our understanding of the biodiversity of the incriminated flies. At odds with the destruction levied by the adult flies is the key ecological role of the immature stages. Safeguarding the future of humanity while conserving the ecological benefits of blood-sucking flies hinges on continued investments in biodiversity research.

­Acknowledgments For the first edition, I thank A. Borkent for insights into the number of corethrellid and ceratopogonid species and early access to his world ceratopogonid catalog; F. Bravo, J. F. Burger, and E. A. B. Galati for information on the number of sycoracine, tabanid, and phlebotomine species, respectively; and A. Borkent, R. W. Crosskey, A. C. Pont, and W. K. Reeves for thoughtful reviews of the manuscript.

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23 Reconciling Ethical and Scientific Issues for Insect Conservation Michael J. Samways Department of Conservation Ecology and Entomology, Stellenbosch University, Matieland, South Africa

Insects are the most speciose animal group on Earth (Caley et  al. 2014), with 1,060,704 described species (Chapter 1). But seeing as an estimated 99% of all species of organisms that have ever existed have gone extinct (possibly a billion in total), we may ask why we should concern ourselves with conservation when, on balance, eventual extinction is perhaps the norm. Bearing in mind the dominance of insects, this point becomes particularly salient. Paleontological evidence suggests that insect biodiversity has increased, but not steadily, over the past 350 million years (Labandeira and Sepkoski 1993). Despite comparatively high loss of some specialist species at the end of the Cretaceous, insects as a group, nevertheless, survived into the Tertiary, and indeed some have thrived and diversified (Labandeira et al. 2002). Paleoclimates (see Zalasiewicz and Williams 2012) have played a major part in determining, for example, levels of insect herbivory, more so than has plant diversity (Currano et  al. 2010). During the Quaternary (the past 2.4 million years), with the advance and retreat of the glaciers, insect populations moved north and then south in the northern hemisphere with alternating warm and cold events. The geographical range shifts across latitudes during these relatively recent glacial times were associated with remarkably little species extinction, at least in

the Palearctic (Coope 1995). These population shifts apparently have been a regular feature of insect assemblages for at least 110,000 years (Ponel et  al. 2003, Samways et  al. 2006), and probably much longer. This means that although we may think of conservation as maintenance of biodiversity in its natural place, this is in fact a moving target when we consider the deep past. With the appearance of tool‐wielding humans and agricultural settlement, the landscape began to change rapidly, and insects faced new challenges. From about 6000 years ago, the landscape was gradually and increasingly transformed (Steadman 1995, Burney and Flannery 2005), so that today, insects are experiencing new influences on their habitats. Today, the greatest to the least adverse impacts on threatened terrestrial invertebrates in general are: habitat loss due to logging, habitat loss due to agriculture, infrastructure development, invasive alien species, habitat loss and fragmentation due to transportation/service corridors, change in fire regime, pollution, climate change/ severe weather and mining (Gerlach et al. 2012). These adverse impacts have increased gradually in both extent and intensity, particularly over the past century. Mawdsley and Stork (1995) estimate that between 100,000 and 500,000 insect species could go extinct over the next 300 years, while McKinney (1999) suggests that a quarter of all

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insect species are under threat of imminent extinction. These extinctions are primarily due to human transformation of the landscape and destruction of their habitats as a result of direct competition with humans for space and resources. Many of the effects are additive, one upon another, leading to particularly harsh and threatening conditions for habitat specialists (Travis 2003). Insects seem to be especially sensitive to these modern compound effects – they are declining faster than birds or vascular plants, at least in the United Kingdom (Thomas et  al. 2004). Of concern is that the British biota is essentially post‐glacial and with few narrow‐ range specialists, whereas in the tropics there are many geographically restricted, specialist species. This means that the situation might be even more acute in areas of the world where a host of sensitive specialists are living in small geographical areas and subject to rapid decline when the footprint of humankind coincides with their restricted range (Samways 2006) (Fig. 23.1). A further consideration is that co‐extinctions also are beginning to occur and are associated with the enormous numbers of mutualistic or other co‐evolutionary interactions between different insects and other organisms. This co‐

extinction seems to be the case when the relationships are particularly close. In both the United Kingdom and the Netherlands, pollinator declines are most frequent in habitat and flower specialists, in univoltine species, and in non‐migrants (Biesmeijer et  al. 2006). The decline of pollinators leaves certain plants as the living dead, with the dependent herbivores that live on these plants effectively adrift on a doomed raft (Vamosi et al. 2006). In many parts of the world, all sorts of curious and specific interactions are under threat. The rather uncharismatic and even more uncharmingly named pygmy hog louse (Haematopinus oliveri) is under threat because its host, the Northern Indian pygmy hog, is threatened. For the first time in the history of Earth, an insect‐extinction spasm is taking place that is being caused by just one other species. Humans are steadily and surely pulling the thread out of the jersey of life and rapidly transforming ecosystems across the globe. The point here is that this is also the first time that a supposedly conscious and sentient being is causing such high levels of extinction. To address the opening point: as we are the conscious cause of such extinction, we surely have a moral responsibility to do something Figure 23.1  The Kubusi stream damsel Metacnemis valida, a narrow‐range endemic in South Africa that is Red Listed as Endangered, as its stream habitats are being shaded out by invasive alien trees such as Acacia spp. (See color plate section for the color representation of this figure.)

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about it. Although not all insects will be lost, and indeed some will benefit from our influences, many unique evolutionary characters and even ecologically keystone species will be extinguished. This issue is not just simply a moral one, but a practical one too, with aspects of our survival also being in jeopardy. We must deal with this crisis, because “business as usual” is not an option (Millennium Ecosystem Assessment 2005). How we deal with it, in turn, depends at the outset on the values we hold. Let us now explore this question of values a little more, as it is the platform upon which our action must take place (Haider and Jax 2007). Let us then look at some practical options for this action, bearing in mind that insect conservation is not a separate entity but rather intertwined with biodiversity conservation as a whole.

23.1 ­Valuing Nature 23.1.1  Types of Value

At the morally most simplistic and superficial level, organisms, including insects, are there for our benefit. This level is also one of practicality and the language of most real‐life conservation. Conservation becomes ever more practical as the pressures mount. The human population increase and the conversion of natural resources is, in turn, putting more pressure on insects. This practical level is about instrumental value. Such value can be consumptive or non‐consumptive. A consumptive value might relate, say, to pollinators because they are needed to produce some particular human produce such as nuts or fruit. Direct value is that of insects produced specifically for human consumption, which is an increasingly viable option as other resources become scarcer (Yen et  al. 2013, Chung and Aguirre‐Bielschowsky 2014). An example of non‐consumptive instrumental value is the viewing of insects for our enjoyment at specific sites (e.g., Hill and Twist 1998, Lemelin 2013, Willis and Samways 2011)

(Fig.  23.2). Instrumental value, particularly when it is consumptive, must have sustainability, with due cognizance of the Precautionary Principle (Fauna and Flora International 2006). This principle recognizes that we must be sensitive to the complexity and levels of current biodiversity; yet, also, we must be cautious in using it because we do not know the extent to which using it will adversely affect those natural resources. At the morally deeper level, beyond ­instrumental value, is intrinsic value. Whereas instrumental value is about how we might benefit from nature (but see below), intrinsic value is about organisms having a share in the survival stakes in their own right. Intrinsic value also has come into prominence in one sector, which relates to the International Union for Conservation of Nature (IUCN) Red List of Threatened Species (http://www.iucnredlist. org/). The Red List is proving to have enormous benefit in conservation planning (Baillie et  al. 2004, Rodrigues et  al. 2006), including for insects (Samways and Böhm 2012). The significance for the intrinsic value of insects is that each species has equal space on the Red List. Thus, a bee, bird, or buffalo is given equal exposure, which is a major step forward for insect conservation, as individual insect species are given higher prominence than normally would be the case. Let us now explore some of these values more extensively. 23.1.2  Sensitive Use of Ecosystem Services

The instrumental level of practicality where human interests are uppermost (over intrinsic nature conservation) have been framed in terms of ecosystem services (Millennium Ecosystem Assessment 2005) and economics (Bishop et al. 2007), and can be persuasive for policymakers (Kareiva and Marvier 2012). However, this so‐called New Conservation Science has won only limited support from biological conservationists and the social sciences (Doak et al. 2014). This debate has been healthy,

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Figure 23.2  Non‐consumptive instrumental value can be the viewing of insects that delight us, such as this rare, paleoendemic white malachite Chlorolestes umbratus in the Harold Porter Nature Reserve, South Africa. (See color plate section for the color representation of this figure.)

as it takes the focus away from perceiving protected areas as the sole providers of conservation action and moves conservation into the realm of partnering with business (Marvier and Kareiva 2014). This may involve, for example, taking a conservation agriculture approach (Cunningham et  al. 2013). Such an approach can indeed be effective, as there can be surprisingly good conservation of insects in the agricultural mosaic (New 2005, Vrdoljak and Samways 2014), as well as in set‐aside land such as large‐scale ecological networks (Pryke and Samways 2012) (Fig. 23.3). The instrumental approach emphasizes that we need insects because they supply goods and services of benefit to us, either directly or indirectly through sustaining the natural world on which we depend. In purely monetary terms, these instrumental values are staggering. Losey and Vaughan (2006) estimate that “wild” insects, which control pests, pollinate flowers, bury dung, and provide nutrition for other

wildlife, are worth US$57 billion per year in the United States alone. Even irrespective of the  monetary value, these small creatures are clearly providing big services. Their full complementarity, following recognition of their spatial and temporal heterogeneity, is also an essential part of the fabric of healthy ecosystems as we know them (Coleman and Hendrix 2000, New 2009). However, this basic instrumental approach, in which insects are seen purely as a utility, can separate humans from the rest of nature. It is a value system based on us using them (other organisms). With the connectedness of nature in mind, any separateness is an untenable way of valuing nature, including insects, in the long term, unless we temper it with careful stewardship of ecosystems (Fig. 23.4). Nevertheless, this instrumental approach is the only conceivable one for the near future for both local and international conservation policy and management (see below).

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Figure 23.3  A significant approach to insect conservation is the use of set‐aside land in agro‐forestry production landscapes. Shown here is a grassland ecological network in a pine plantation in South Africa. This remnant set‐aside land has great conservation value for a whole range of biodiversity while maintaining ecosystem processes such as the historic hydrology. (See color plate section for the color representation of this figure.) Figure 23.4  Insect conservation is about conserving connectedness. Here, dung beetles are burying elephant dung within hours of deposition and inside an ecological network in an agro‐forestry landscape. This is stewardship of the landscape while including significant ecological interactions.

23.1.3  Common‐Good Approaches

To value nature in context, we need to bring in common‐good approaches in which farmers and residents contest scientific approaches to valuing nature when adjudicating conflicts over protected natural areas (Harrison and Burgess 2000). For effective conservation, the knowledge base for the goals and practices of

nature conservation must be widened. A way to tackle this challenge is to develop a common‐good approach based on ethical and moral concerns about nature. The important feature is to translate these concerns into practice by expressing the values through a social and political process of consensus building. The aim is to build coalitions and common

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thought between different interests through a process of debate and systematic analysis of values. Different perspectives on the utilitarian values of nature are thus reconciled. The point for insect conservation is that such a process of making decisions at the outset truly benefits conservation of, for example, the agri‐environment, an arena where biodiversity conservation is at a critical stage (Conrad et  al. 2004, Perrings et  al. 2006, Lindenmayer et  al. 2012, Cunningham et al. 2013). Another dimension to this common‐good approach is beginning to surface. It hinges on our loss of touch with nature (Stokes 2006), aptly called by Miller (2005) the “extinction of experience.” His concern is that we are beginning to forget just how much we rely on nature. Because insects are so crucial to so many essential services, yet far from most people’s thoughts, we, as a collective consciousness, are oblivious to what we are doing to the rich tapestry of species that grace and fine‐tune ecosystems. Lyons et  al. (2005) convincingly illustrate that less common species, which by reasonable extension include the majority of insects, make significant ecosystem contributions. Furthermore, many prejudices against insects exist, with mosquitoes and other flies being seen by a large sector of the public to represent insects at large (Lemelin 2013). Entomologists, like other invertebrate conservationists, have a long way to go before the human world recognizes the general instrumental, let alone intrinsic value, of insects as a whole. Additionally, what we (the current adult population) value is not necessarily what our children value, either now or in the future when they are adults. To give one example, children (and the elderly… the wise?) are particularly fascinated by dragonflies, and much more so than economically active (too busy?) adults (Suh and Samways 2001). In response, Palmer and Finlay (2003), speaking on behalf of no less than the World Bank, recommend from Baha’i scriptures: “Train your children from the earliest days to be infinitely tender and loving to animals.” This generational and cultural sensitivity

is what the World Bank considers as valuing and investing in the future. 23.1.4  Intrinsic Value and Conservation Action

Cincotta and Englemen (2000) suggest that our world is in crisis but not doomed. This view is not blind optimism, as biotic recoveries from prehistorical mass extinction events have shown. However, it does not mean that we simply abandon any effort to help nature survive in as much of its entirety as possible. We must apply our moral conscience to the full. Yet it need not be a penance. It makes for much more positive action and creativity when we are joyous about these tasks. This is the language of deep ecology, which not only provides a positive foundation and sense of wisdom, but also a course of action (Naess 1989). With this deep‐ecology approach, humans and nature are inseparable. A course of action then arises when all critics are recognized, alongside a more simplistic lifestyle, where harmony with nature is the goal. This is not a vague notion, but builds on sound ecological knowledge, including identifying which of our actions are beneficial for nature and which are harmful. Yet these terms are presumptuous: “we know best for nature.” Arguably, a better way of expressing this sentiment, and interpreting it in terms of quantitative biodiversity, is to say that our actions should maintain ecological integrity (compositional and structural diversity) and encourage ecological health (functional diversity) (Rapport et al. 1998). In turn, a combination of these two, integrity and health, as well as recognition of the interdependency of social and ecological systems, begets ecosystem resilience (Peterson et al. 1998, Fischer et al. 2009). Through a wide range of natural conditions and heterogeneity, as well as intraspecific variation among many species (Bolnick et al. 2011), they also make available many more evolutionary and community opportunities than would an impoverished system. Thus, scientific values easily can be reconciled with those of intrinsic

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value, even down to the level of intraspecific variation (Violle et al. 2012). This recognition of ecosystem health, integrity, and resilience goes to the heart of insect conservation simply because the insect world is so vast and complex, with such an unimaginable number of biotic interactions, that we are obliged to employ the Precautionary Principle, whereby we maintain all the parts and their function in as many places and as intact as we can. Translated into practical terms, landscape conservation over large areas is crucially important for conserving insects. With the landscape‐scale approach, we let nature “know best” by employing some basic, interrelated tenets that are beginning to emerge (Samways 2007a, Samways and Böhm 2012). A central population tenet is the combination of (i) maintaining large landscape patches, (ii) encouraging patch quality, and (iii) reducing patch isolation, all three of which relate to a set of one management and five landscape design principles or descriptors, with a socio‐ecological overlay recognizing the importance of humans on the landscape (Fig. 23.5). With this landscape‐scale approach (which does not exclude species‐level approaches as fine‐tuning (New 2009), and includes complementary features of the landscape such as logs, rocks, ponds, and patches of bare ground (the mesofilter; Crous et  al. 2013)), we emerge with an ethical foundation as well as a practical one. In effect, this foundation is Earth harmony, where all living things, no matter how small, have the right to live. This approach, according to Johnson (1991), is also the only morally acceptable way forward, and is based on practical methodology of the three operational scales of coarse filter (landscape), mesofilter (features), and fine filter (species and their intraspecific variation). This landscape way of thinking inherently also incorporates a sense of place (Lockwood 2001) and, additionally, a sense of change across place. This change across place is, in ecological terms, change across space (i.e., beta and gamma diversity), and is where deep ecology departs from spirituality, as it favors location over

omnipotence. Moving this thought into the realm of insect conservation means maintaining population levels of insect species in situ across the multitude of habitats across the globe: that is, giving habitat heterogeneity an important place on the conservation agenda (Pryke and Samways 2015) (Fig. 23.6). 23.1.5  Reconciling Values

We can argue for reconciliation between instrumental and intrinsic value from yet another perspective. At their extremes, instrumental‐ and intrinsic‐value approaches could be considered confrontational because, according to Norton (2000), they share four questionable assumptions and obstacles: (i) a mutual exclusion of each other; (ii) an entity, not process, orientation; (iii) moral monism; and (iv) placeless evaluation. He also draws attention to things: that is, organisms that supposedly have either instrumental or intrinsic value. Reconciliation comes when one takes an ecological (short‐term) as well as an evolutionary (long‐term) dynamic view at large spatial scales, giving prominence to ecological integrity, ecosystem health, and resilience. The obstacle is only apparent when instrumental and intrinsic values are each taken in their extreme, monistic sense. Intrinsic value has to be seen alongside a deep ecological sense of place before reconciliation can begin. Norton (2000) summarizes this by suggesting an alternative value system that recognizes a continuum of ways in which we value nature. Such a spectrum gives value to all the natural interactions in their natural place in a pluralistic way. He calls this a Universal Earth Ethic, which means all places on Earth. This is not, however, a melting down into a common currency of homogenous biota, which is happening, for example, with the vast interchange of invasive alien organisms. The importance of such an Earth ethic is that it values nature for the creativity of its processes. Rolston (2000), another influential environmental ethicist, also envisions an Earth ethic, with a blending of anthropocentric and b ­ iocentric

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rating n g e t n I rvatio conse duction & pro

Design Principle 3: Reduce contrast

Design Principle 1: Protected areas

Design Principle 2: Heterogeneity

CENTRAL POPULATION TENET

Design Principle 4: Soften landscape

Maintain Metapopulation Trio

Design Principle 5: Connect habitat

Management Principle: Disturbance Socio-ecological overlay: human needs

Figure 23.5  Around a central population tenet, based on the ‘metapopulation trio’ of maintaining large patch size, reduced patch isolation and good patch quality, are five design principles of (1) maintaining protected areas wherever possible, especially for habitat specialist and sensitive species, (2) maintaining natural, quality habitat heterogeneity, (3) reducing contrast wherever possible alongside a transformed patch, (4) softening the landscape with conservancies, agri‐environment schemes and organic agriculture, and (5) connecting protected areas or patches of high quality with corridors, a group of which constitute an ecological network. Yet a landscape has to be maintained in its historic condition, and so it is essential to have a management principle that, is its basic form, seeks to maintain natural disturbance such as fire and grazing where appropriate (bottom middle). Humans cannot be ignored, and so there is always a socio‐ecological overlay (bottom right).

values. This melding is for the patent reason that we and this planet share entwined destinies. This wider Earth ethic does not exclude a land ethic, nor does it ignore differences across the planet. It simply recognizes that we must think globally as well as locally. Even among insects, some interactions are local, such as a parasitoid and its host, whereas others are global and even affect

­ lanetary function. This point is brought home p by the calculations of Bignell et  al. (1997) that global gas production by termites in tropical forests represents 1.5% of carbon dioxide and a massive 15% of all methane. Plausibly, if we upset termites too much, we could be tinkering with planetary function. When primary forest in Indonesia is converted to cassava fields, for

23  Ethical and Scientific Issues for Insect Conservation

Figure 23.6  Besides maintaining set‐aside land in the form of interconnected corridors (ecological networks; in the far distance), landscape‐scale conservation for insects and other biodiversity involves preserving features of the land (mesofilters), such as rocks, and the natural range of habitat (biotope) heterogeneity, which is often maintained by differential processes (such as localized levels of rainwater percolation) and by stochastic processes such as fire.

example, termite species diversity drops from 34 to 1 (Jones et al. 2003). Justus et al. (2009) provide an alternative perspective, and they raise concerns over the use of intrinsic value as a tool for conservation action. For example, in reality many conservation goals require trade‐offs where some entities are protected to the detriment of others, and where other interests have to be considered. Also, they point out that intrinsic value implies that all species and natural ecosystems are of (equal) value, which provides little guidance for conservation action. Justus et al. (2009) then take the line that theoretical difficulties with intrinsic value preclude the formulation of clear and compelling justifications for conservation relative to other interests. By contrast, focusing on instrumental value does not have these difficulties, and despite its negative connotation, instrumental conservation is simply value that depends on perspectives from a broad range of valuers. This approach should not be confused with market value, nor denigrated as implying that entities are only of value for human manipulation. In this way, instrumental conservation is seen as a toolbox of best strategies for conservation action. It is a means for weighing options and identifying ways forward that maximize the values involved. Intrinsic value need not be invoked for this task. Rather, non‐monetary

instrumental value such as aesthetic, cultural, functional, scientific and existence values are recognized. In short, the value of an entity is based on its continued existence. This is the ethical foundation that Haider and Jax (2007) consider essential for effective conservation. This then takes us back again to our opening question of why we should even consider doing conservation when extinction in Earth’s history has been commonplace. However, insects are going extinct today, in the Anthropocene, possibly faster than at any time since the end of the Cretaceous. Rather bizarrely, we humans, the causal agent, realize what we are doing. Yet we are sentient beings and it is hoped that most of us have a conscience and would not wish to see an impoverished world, nor a functionally inadequate one. And so we must do conservation, and this, in Justus et al.’s (2009) view, is based on a level of instrumental value, which gives us the necessary decision toolbox as well as an ethical foundation.

23.2 ­Insects and Ecosystems 23.2.1  Interactions and Multiple Effects

Insects are inseparable from the rest of nature. That insects are open systems – yet there are so many of them, both as individuals and as

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s­pecies  –  inevitably means that they are ­functionally integral to ecosystem processes as we know them, a point clearly illustrated by the gaseous termites of Bignell et al. (1997). Viewed in another way, an enormous number of niches were open, and the selection pressures were such that insects diversified enormously. Then, as a group, they became fundamental to the connectance within most terrestrial ecosystems. If we compare the estimated total biomass of vascular plants to that of animals, the ratio is about 99.999 to 0.001, whereas the total number of estimated vascular plant species to animal species (and mostly insects) is almost an exact reversal, with a ratio of about 0.026 to 99.974 (Samways 1993) (Fig. 23.7). Among plants, functional diversity, as measured by the value and spectrum of species’ traits, rather than simply by species numbers, strongly determines ecosystem functioning (Diaz and Cabido 2001, Mouillot et  al. 2013). However, a basic difference exists between plants and insects in terms of presence. Plants are fixed on the spot, but insect populations often blink on and off like lights across the landscape, as populations survive and thrive and then locally disappear (Dempster 1989). Insects, thus, are an intrinsic part of the ecological tissue of the landscape, yet dynamic in terms of their presence and influence, and hence in their

c­onnectance relationships (Cross et  al. 2011, Kehinde and Samways 2012). What we see as a land mosaic is not necessarily how insects perceive and react to it (Haslett 2001, Pryke et al. 2013). This dynamic population response of insects to the world around them was particularly evident in the Quaternary when geographical ranges of species shifted back and forth, tracking optimal temperatures. This response emphasizes that the “sense of place,” in terms of evolutionary conservation, is an artifact of time. Although rapid evolutionary change in insects does occur (Mavárez et al. 2006), there are only a few examples of adaptive changes to the anthropogenic landscape (anthropovicariance; Williams 2002). However, in general, the modern mix of intense pressures, and the speed at which these changes are occurring, will be too much for many insect species to survive, even though there is strong evidence of biodiversity persistence in the paleo‐ecological record (Willis et al. 2010). This current level of discontinuity is largely because many anthropogenic effects are synergistic, as with the effects of fragmentation and global climate change, described by Travis (2003) as a “deadly anthropogenic cocktail.” Habitat loss and global climate change seem to be responsible for huge declines of some British butterflies (Warren et al. 2001) and Figure 23.7  It is an extraordinary phenomenon that the ratio of estimated biomass of vascular plants to that of metazoan animals (mostly insects) is about 99.999 to 0.001, whereas the estimated total number of vascular plant species to that of animal species is almost the exact converse of 0.026 to 99.974.

23  Ethical and Scientific Issues for Insect Conservation

probably also of some British moths (Conrad et al. 2004). In Europe at least, nature reserves alone are beginning to seem as if they will be unable to cope with the dynamic geographical range shifts that are necessary for the long‐term survival of many insect species (Kuchlein and Ellis 1997, Hochkirch et al. 2013). The crucial question, then, hinges on whether there will be a decoupling of interactions (e.g., pollination, herbivory, and parasitism), with cascade effects as the climate changes across a world dominated by human landscapes. These human‐made mosaics inhibit movement of many species and prevent them from finding suitable source‐habitat conditions. This predicament, combined with deterioration of patch quality, is causing considerable local extinction, especially among habitat specialists (Kotze et al. 2003, Valladares et al. 2006), leading to ecosystem discontinuities (Samways 1996). 23.2.2  Insects and Food Webs

Because insects function at various trophic levels, multiple effects involving insects are likely to occur in food webs. Dunne et al. (2002) have shown that food‐web structure mediates dramatic biodiversity loss, including secondary and cascading extinctions. Their findings emphasize how removal of a number of species affects ecosystems differently depending on trophic functions of the species removed. They found that food webs are more robust to random removal of species than to selective removal of species that have the most trophic links to other species. The implication is that the robustness of a food web is improved by increasing the number of connections within it, although this is apparently independent of species richness per se. Removal of ecologically highly connected species can have a devastating cascading effect. Conversely, but not always, removal of species with few trophic connections generally has a much lesser effect. The upshot is that to maintain food‐web stability, the diversity of highly connected species must be maintained (Kehinde and Samways 2014a). Removal of only 5–10% of

these highly connected species can lead to major ecosystem change (Sole and Goodwin (2000). Loss of only a few important predators of grazers can have a disproportionately large effect on ecosystem diversity, which may involve subtle effects with time delays (Duffy 2003). Evidence also is accumulating that changes in biodiversity can be both the cause and the result of changes in productivity, as well as in stability. This two‐way effect creates feedback loops and other effects that influence how communities respond to biodiversity loss. Food webs mediate these interactions, with consumers modifying, dampening, and even reversing these biodiversity–productivity linkages (Worm and Duffy 2003). There can be whole‐ecosystem changes in function as a result of changes in the species present and their abundance, which has important conservation implications (Thompson et al. 2012). This was seen on Christmas Island, where there was a radical change in species composition (and abundance) and food‐web structure after invasion by the yellow crazy ant Anoplolepis gracilipes (O’Dowd et  al. 2003). The reverse can occur, as when the big‐headed ant Pheidole megacephala was controlled on the Seychelles island of Cousine. On removal of the ant, there was remarkable recovery of the parasitoids (of the invasive mutualist scale Pulvinaria urbicola) and many other indigenous insects, and effectively a re‐assembly of the ecosystem (Gaigher and Samways 2012, Gaigher et  al. 2013) (Fig. 23.8). Trophic cascades can occur even across ecosystems. When fish consume large numbers of dragonfly larvae, pressure is reduced on pollinators, which are normally eaten by adult dragonflies (Knight et al. 2005). As a result, plants near ponds with fish receive higher levels of pollination than plants away from ponds. 23.2.3  Importance of Maintaining Landscape Connectance

Evidence is beginning to point toward the importance of conserving whole landscapes, with all levels and types of connectance intact.

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Figure 23.8  An increasingly strong mutualism between two alien insects, the ant Pheidole megacephala and the scale insect Pulvinaria urbicola, almost led to “meltdown” of the biodiversity on the small Seychelles island of Cousine through destruction of the native trees, especially Pisonia grandis, a keystone species. The mutualism was finally broken by a combination of highly selective insecticide baiting and the upsurge of natural enemies of the scale, returning the island to a semblance of its historic condition.

Such connectance should include the myriad of species (and their intraspecific variation with respect to traits), including insects, which collectively make up a major component, even though individually they might appear ecologically somewhat redundant. Evidence from plant communities suggests that the collective effect of rare species increases community resistance to invasion by aliens and minimizes any effect (Lyons and Schwartz 2001), while maintaining rare species in the community also helps to maintain ecosystem function (Lyons et al. 2005). With the increased stresses on and gradual loss of rare species and specialists, some catastrophic regime shifts are likely, where pressures build to reach a point where a radical change to a new state occurs (Scheffer and Carpenter 2003). Transformation of formerly extensive ecosystems into remnant patches, therefore, does not leave these fragments as simply smaller reflections of the whole. Each patch will gradually go on its own trajectory, sometimes catastrophically. These changes come about because the stability of food webs can be subtle. Although local species richness can affect ecosystem functioning, such as productivity and stability, generally species diversity positively influences this functioning – but not always. The differences seem to arise depending on the spatial scale under

consideration. At the small, local scale, an increase might occur to a point where all available niches are filled, but as species diversity increases further, through high immigration of sink‐population competitors, functioning decreases. By contrast, at the larger spatial scale, regional species complement each other, with the result that ecosystem functioning increases with an increase in species diversity (Bond and Chase 2002). This relationship emphasizes the importance of maintaining large complementary patches (Valladares et  al. 2006) and landscape networks (Samways 2007b, Samways and Pryke 2015) across wide areas to maximize insect and other biotic diversity.

23.3 ­Two Challenges 23.3.1  The Taxonomic Challenge

One of the greatest tasks for insect conservation is identifying the focal species in any ­particular study (New 2009). The lack of taxonomic information on the very things we are trying to conserve is the taxonomic challenge. How do we deal with this? If landscape conservation is an umbrella for such a wide range of insects and all their interactions, we may even ask whether it matters to know all their names.

23  Ethical and Scientific Issues for Insect Conservation

When deciding which landscapes have value (which might not simply be rarity value), we need to know the components that make up those landscapes to assess their value. One of the components  –  and not the only one, of course – is the actual species that live there and are something tangible into which we can get our conservation teeth (New 1999). Explicit population models suggest that prediction of the effects of fragmentation requires a good understanding of the biology and habitat use of the species in question, and that the uniqueness of species and the landscape in which they live confound simple analysis (Wiegand et al. 2005). Yet, for practical large‐scale conservation, and given the regular shortage of resources, we cannot know all the species, even in a small area, especially in the species‐rich lower latitudes and other biodiversity hotspots. This taxonomic challenge is further highlighted because some, and probably many, ­putative species are species complexes (Hebert et al. 2004). To get a measure of the value of a landscape, we choose a subset of taxa. This subset can be certain taxa that are well known, or a size class, particular functional types, and even Red Listed species, which can be used effectively to stand in for the rest of the insects, and indeed much of the rest of biodiversity. In other words, we select surrogates and even icons. Use of icons is widespread, and important even in mammal conservation, where charismatic species get preference over less glamorous ones. A whole range of possible focal taxa exists, the choice of which, in part, depends on the conservation question being posed (Samways et  al. 2010b, Gerlach et  al. 2013). In most cases – and this is a harsh reality in all realms of invertebrate conservation  –  the final choice depends on the taxonomic knowledge available. Identified species are so much more valuable for quality landscape conservation than are unidentified species. This issue of using named species is crucial when, for example, selecting landscapes that have rare and endemic taxa that might be threatened and irreplaceable (New 2011).

23.3.2  The Challenge of Complementary Surrogates

Landscape planners have been exploring ways to prioritize areas of conservation value so that conservation management can be directed first to physical areas of high biodiversity value and those that are under most threat. Evidence is accumulating that the best way forward is to use surrogates for the landscape, in addition to surrogates for species, in this planning process. This approach, in turn, enables selection of reserve areas. When such thorough and insightful selection is done, about half the land area needs to be conserved if regional biodiversity is to be maintained (Reyers et al. 2002). This situation is not generally tenable if we wish to conserve all biodiversity, given the human demand for land, meaning also that there is an urgent need to explore the value of agricultural land in particular for its biodiversity conservation value (Vrdoljak and Samways 2014). We are facing a situation where we have to consider some sort of landscape and species triage, whereby the land and its organisms will benefit most from our intervention when it is focused on the points for which we can obtain maximum return for minimum resources. The alarming feature of this approach is that even if we select optimally, those reserves of today will not necessarily be optimally sited for the future, given global climate change.

23.4 ­Synthesizing Deeper Values and Practical Issues From our discussion on conservation value, we found that conservation of whole landscapes across the whole of the globe is a moral way forward. This perspective involves a distinct sense of place, while recognizing the importance of spatial and temporal dynamics, and thus dynamic heterogeneity, at the local scale. It includes recognition of the operational scales of mesofilter, fine filter, and coarse filter. However, there also needs to be reconciliation of human

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needs along with this foundation, as can be done in the case of set‐aside land in the form of large‐ scale ecological networks (Samways and Pryke 2015). Furthermore, an Earth ethic (Norton 2000, Rolston 2000) purports to maintain the differences between landscapes. In short, we aim, through a sense of moral concern and joy for nature, to conserve as much of the world’s natural integrity as possible, alongside human needs, even if it has to involve some triage. The quantitative ecological approach is leading to the same conclusion. To maintain ecological health and resilience in a socio‐ecological context, we need to conserve the widest range of connectance as possible, even involving rare species, throughout a range of landscapes (Kehinde and Samways 2014b). A dark cloud facing us is that much of the human effect has momentum that is not stoppable for a long time, with the inevitability of extinction debt (Tilman et  al. 1994, Dullinger et al. 2013). In the past, insect populations could shift across natural landscapes on a regional scale unimpeded by anthropogenic obstacles, but the situation today is not the same as a result of the myriad of human‐transformed land mosaics. To maintain any semblance of the past, we need to think of ecological health and vigor in terms of massive linkages between large, quality‐landscape patches. This approach has been forcefully emphasized by Erwin (1991) in a landmark but neglected paper. For many parts of the world it is too late to develop these huge networks proactively, but we can engage restoration triage (Samways 2000), and we can introduce ecological networks at the landscape level (Hilty et al. 2006, Samways 2007b). Whatever path we chose, for terrestrial ecosystems at least, the collective moral, human consciousness must consider insects as part of the initiative.

23.5 ­Summary Despite various global catastrophes over the past 350 million years, insects have increased in species diversity. Yet today, they face a human

meteoric impact that could eliminate perhaps a quarter of them. We need to be concerned because insects have enormous roles in ecosystem services and great monetary value. Besides, we have a moral duty to conserve them, as they are our planetary partners. Because insect biodiversity is so vast and essentially unknowable, we need to adopt a precautionary approach, whereby we conserve as much natural and near‐ natural land as possible. We also need to maintain diversity of landscapes across the globe; such landscape diversity is an umbrella for a huge range of insect species. Where insects per se are not the focal issue, and where the concern is for ecosystem health, integrity, and resilience, we still need to maintain as much species diversity and food‐web connectance as possible. This approach will, in turn, benefit an enormous range of insects. Although keystone species, whether insects or not, have the major role in shaping ecosystems as we know them, rare species en masse also play a part. Thus, all efforts now should be directed to reduce homogenization of the world and to radically stem biodiversity loss. These efforts need to take place across the whole globe as part of an Earth ethic for the survival of all.

­Acknowledgments This work was supported by the South African Department of Science and Technology/ National Research Foundation Future Proofing Food Project.

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24 Taxonomy and Management of Insect Biodiversity Ke Chung Kim Frost Entomological Museum, Department of Entomology, Pennsylvania State University, University Park, Pennsylvania, USA

Insects are incredibly diverse, abundant, and spectacular in color, form, and function. They are found in nearly every conceivable habitat throughout the world. Their lives are inter­ twined with the lives of humans, and they make up a major portion of global biodiversity. They feed on plants and animals, through which con­ siderable economic losses are incurred, and transmit parasites to humans, causing diseases such as malaria, onchocerciasis, and plague. Above all, insects are important ecological part­ ners in sustaining our life‐support system (Coleman and Hendrix 2000). Biodiversity, the totality of living things and their variations, is the essence of life on Earth. All species of ani­ mals, plants, and microorganisms are elements of our life‐support system, of which insects rep­ resent the most diverse and important partners (Wilson 1992, Kim and Weaver 1994, Kim 2001a). As the most successful group of animals, insects and arachnids make up more than 60% of global biodiversity and are major players and important ecological partners in ecosystem function and humanity’s existence (Kim 1993b, Coleman and Hendrix 2000). Despite centuries of extensive studies, global biodiversity is still poorly known. Fewer than 2 million species have been described of what currently is esti­ mated to be a total of 13.6 million species (10 million is commonly used). Our knowledge

base, however, has been skewed toward ­vertebrates (>90% described) and plants (>84% described), leaving behind small animals such as insects, arachnids, and lower plants (algae, ferns, mosses, and others). Only about 12% of the insects and 10% of the arachnids have been described, along with 4.8% of the fungi and 0.4% of the bacteria (Heywood and Watson 1995). Our current knowledge of global biodiver­ sity  –  with a current human population of 7.3 billion – is not too much better than what it was a century before, when the human population was barely 1.65 billion. Today’s known biodiver­ sity is far too small, perhaps 13% of the extant total. At the same time, we barely know what biodiversity exists in our own backyards. “Backyard biodiversity,” defined as “local biodi­ versity in and near human habitation,” refers to the natural resources and capital for ecosystem services at the grassroots level (Tallamy 2009). Backyard biodiversity, the foundation for local sustainable development, is poorly explored and documented for almost all places in the world (Kim and Byrne 2006). Insect biodiversity is important in managing ecosystems. Insects, with their combination of unique biological traits and ecological roles, are valuable indicator organisms for assessing, moni­ toring, and managing biodiversity in natural eco­ systems and combating the invasion and spread of non‐indigenous insects (Kim and Wheeler

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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1991; Kim 1993a, b; US Congress 1993; Büchs 2003). Today’s biodiversity is the culmination of long‐term ecological and evolutionary processes going back more than 410 million years to the Devonian period. The composition and abun­ dance of species on Earth is constantly changing. As a result, no one community contains the same biodiversity as any other unit, even in rather homogenous forests, due to site‐specific charac­ teristics of soil, topography, vegetation, weather, and other environmental factors. Because biodi­ versity conservation and resource management are targeted for specific local units, biodiversity assessment must be designed specifically for the particular site. Yet, few locally defined sites exist where the local or “backyard” biodiversity has been inventoried for natural resources and capi­ tal (Kim and Byrne 2006). In this chapter, I discuss the state of insect biodiversity in the context of insects as ecologi­ cal partners for sustaining our lives. I also dis­ cuss the need for taxonomy in biodiversity assessment and monitoring, the problems associated with taxonomic bottlenecks, new ­ opportunities for taxonomy in biodiversity sci­ ence, and the application of insect‐biodiversity science and taxonomy to ecosystem manage­ ment, pest management, and conservation.

24.1 ­Insect Biodiversity Honeybees, American cockroaches, and Japanese beetles are distinct species of insects, but they are not biodiversity – they are units of biodiversity. Biodiversity is not something we can touch, although we see and feel the parts of a community. Biodiversity is commonly defined as “the totality of variety of species of plants, animals, fungi, and microbes, the genetic varia­ tion within them, the ecological roles they play, and their interrelationships in biological com­ munities in which they occur” (Kim 2001a), although it is defined somewhat differently by leading scientists (Takacs 1996). The essence of biodiversity, however, is perceived differently by people of different backgrounds.

Our lives depend completely on biodiversity; dynamic ecosystem processes are sustained by the interactions of all species of animals, fungi, microbes, and plants (Kinzig et al. 2001). From an economic perspective, biodiversity includes the natural resources and capital assets that provide the basic resources for all organisms and human enterprises (Baskin 1997, Kim 2001a). Biodiversity also is the end point of anthropocentric influences on the biosphere, which is continually infused with chemicals, many of which are newly created by humans. A person strolling through a flower garden, a hon­ eybee visiting a flower, a cow grazing in a pas­ ture, or a woodpecker pecking on a tree are all parts of the interconnected whole of our living world. Our survival depends on this intricate web of life, the network of interacting organ­ isms. The world’s biodiversity supplies our basic necessities such as food, clean air and water, fuel, fibers, building materials, medicines, and natural areas where we enjoy recreational activ­ ities (Kim 2001a). More than 1 million species of insects make up 58% of all described species. Insects and ter­ restrial arachnids are also cosmopolitan animals closely associated with human enterprises. Because humans are exploring and exploiting every corner of the world, we should expect to find and document many new species and new distributions. Insects continue to exploit new habitats and expand their ranges, producing lin­ eages of great ecological and behavioral diver­ sity and making their study – entomology – one of the most fascinating and important sciences. Natural biodiversity in wild lands, such as the Amazon, northern Alaska, and Siberia, contin­ ues to be threatened by human enterprises such as clearing, logging, gas and oil drilling, mining, housing development, and urban sprawl. As a result, biodiversity continues to decline, and likely will continue to do so as the human popu­ lation grows and economic development expands in developing nations such as China and India. As our ancestors moved from a hunter‐­gatherer to an agrarian lifestyle, human s­ettlement and

24  Taxonomy and Management of Insect Biodiversity

farming offered new territory and habitats for insects (Ponting 1991). Many of these insects readily invaded human habitation. The close rela­ tionship between humans and insects, known as “synanthropy” (Harwood and James 1979), also can be referred to as “human–insect biodiversity.” In other words, insects have successfully evolved with humans in agricultural societies. Insects are not merely pests of our crops or vectors of disease agents such as malarial para­ sites. They also are the most successful group of organisms in terms of the numbers of species and individuals. They are small and agile with short life cycles, enabling long‐distance disper­ sal and invasion of new territories and habitats (Kim 1983, 1993a). They have exploited ecologi­ cal opportunities to occupy unique niches and microhabitats (Kim 1993a, b) and have become major players in maintaining ecosystems and providing diverse ecosystem services (Coleman and Hendrix 2000).

24.2 ­Biodiversity Loss and Humanity Earth is rapidly becoming a network of human ecosystems, with urban and suburban commu­ nities transforming natural environments into human habitats. This process continues every­ where that humans live, at nature’s expense. The destruction of natural habitats and loss of spe­ cies draw different groups of insects and other invertebrates, forming secondary human‐asso­ ciated biodiversity that includes pests and imported exotic species of plants and animals. Today’s cities and suburbs are being connected or merged with other newly developed munici­ palities, forming megacities (Cohen 2006, Lee 2007). Secondary biodiversity of synanthropic arthropods often contributes to economic loss or causes diseases in humans and animals. In most developing and underdeveloped countries in Africa, South America, and Southeast Asia, people still live in natural ecosystems with bus­ tling biodiversity (Kim 1993b, UNDP et al. 2000, Sodhi et al. 2004). These lands, with their rich

backyard biodiversity, are exploited for local economic development, becoming agricultural and industrial lands. In tropical regions, people make their living without knowing what they have in their backyard beyond some species of herbal plants and common animals. In this set­ ting, biodiversity represents a basic economic resource and natural capital for human survival, but it is not considered important to the econ­ omy or land‐use planning. This paradigm should be corrected for sustainable develop­ ment; the assessment of backyard biodiversity is the first step in managing biological resources and ecosystems (UNDP et al. 2000). Extinction is a natural process. Today’s global biodiversity represents less than 1% of all spe­ cies that ever existed. Throughout the history of life, enormous numbers of species – from 5 bil­ lion to perhaps 50 billion  –  arose and then became extinct. Estimates based on fossils sug­ gest that for every 4 million species that have gone extinct, only one species met its demise as result of human involvement (Raup 1991). Today, however, extinction is caused primarily by humans, particularly during the past two centuries. In recent human history, global biodi­ versity has been destroyed at an unprecedented rate because of rapid human population growth and economic development that increases urbanization and land conversion (Kolbert 2014). The loss of biodiversity has become the primary concern for our own sustainability. Humans, the greatest force shaping the evolu­ tion of global ecosystems, continue to convert natural ecosystems to human habitat (Palumbi 2001). Without environmental safeguards, this process will continue to destroy habitats and their native species, perhaps as many as 1000 per year, throughout the world (Myers 1979; Wilson 1985, 1992; Kim and Weaver 1994), but this problem has not been recognized by politi­ cal leaders or the public in most countries. The great challenge is to estimate and predict anthropogenic extinctions in a void of knowl­ edge about global biodiversity, especially for small organisms that make up the core of this biodiversity. The 1995 Global Biodiversity

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Assessment shows that 484 animal and 654 plant species have become extinct since 1600. The World Conservation Monitoring Centre listed 602 species of vertebrates, 582 inverte­ brates, and 2632 plants as endangered, and 5366 animals and 26,106 plants as threatened or of special concern (Heywood and Watson 1995). For vertebrates and plants, 5–20% of biodiver­ sity for some taxa is threatened with extinction. If this estimate is applied to insects, the expected number of species that would be lost in the next 25 years comes to 51,250 species at 5% and 2,005,000 species at 20%. This loss of global bio­ diversity is caused by two mechanisms: extirpa­ tion (local population loss) and extinction (permanent species loss from the planet). Accurate estimation of the actual numbers lost remains difficult because our knowledge base for global biodiversity is inadequate and back­ yard biodiversity is practically unknown (Heywood and Watson 1995, MEA 2005).

24.3 ­Biodiversity and  Taxonomy Biodiversity does not refer to a single species, such as human (Homo sapiens Linnaeus) or European corn borer (Ostrinia nubilalis (Hübner)), but rather to the totality of all species in a defined area. The importance of biodiver­ sity lies not in numbers but in the interactions of species in a specific habitat, community, or eco­ system. On the other hand, taxonomy (= alpha and beta taxonomy of Mayr’s “systematics”) is the science of discovery, documentation, and organization of organisms (Mayr and Ashlock 1991). Good taxonomy for a specific taxon is built by taxonomists who study the taxon at the species level. Biodiverse taxa, such as the Insecta, pose great challenges to scientists in community ecology and natural resource man­ agement who are interested in designing biodi­ versity studies and processing large field samples. This is because species identification is difficult for many taxa, even for general taxono­ mists, and often requires specialists (Kim and Byrne 2006).

Today’s knowledge of global biodiversity r­epresents the culmination of research by tax­ onomists and natural historians over more than 250 years  –  since the publication of Species Plantarum in 1753 (the starting point for plant nomenclature) and the 10th edition of Systema Naturae in 1758 (Linnaeus 1758; the starting point for zoological nomenclature) (Mayr and Ashlock 1991). Taxonomists have been highly motivated, determined, and dedicated scientists who continue to add new species and informa­ tion on global biodiversity by discovering, nam­ ing, and describing unknown organisms one by one from the thicket of unknowns. In other words, discovery and documentation of biodi­ versity began with backyard efforts, then expanded to regional and global efforts from the late 19th century to the present, which involved both western expeditions around the world and taxon‐based surveys by natural historians and taxonomists. Taxonomy is the oldest discipline in biology. Carl von Linnaeus (1707–78) brought a hierar­ chical order to natural history and established the basis for biological nomenclature and clas­ sification that guides the science of life to this day (Blunt 2001, Nature 2007, Warne 2007). Linnaeus’s followers, natural historians and tax­ onomists, have explored nature and methodi­ cally documented biodiversity worldwide all the way into the 21st century. The culmination of these efforts is what we call “global biodiversity.” Yet, today’s taxonomy barely scratches the sur­ face of extant global biodiversity (Heywood and Watson 1995). Taxonomy with evolutionary and speciation perspectives is known as “sys­ tematics” – it is the foundation of biology, and is fundamental to all branches of biological and environmental sciences since the New Systematics (Huxley 1940). Systematics encom­ passes three aspects: (i) alpha taxonomy, the most basic aspect, involving biodiversity explo­ ration and description, documentation of extant species, and development of taxonomic tools; (ii) beta taxonomy, involving the synthesis of taxonomic data and development of biological classifications; and (iii) gamma taxonomy,

24  Taxonomy and Management of Insect Biodiversity

involving the study of speciation and phylogeny of organisms, which is increasingly fragmented under the umbrella of evolutionary biology (Mayr and Ashlock 1991). Taxonomy is funda­ mental to all biological sciences. Taxonomic data are applied to all aspects of agriculture, conservation, ecology, fisheries biology, for­ estry, and environmental studies (Kim and Byrne 2006). Yet, we are facing a continued decline of taxonomy worldwide and are now left with a small pool of taxonomists and qualified parataxonomists (a term initially used for trained lay professionals of Costa Rica’s Instituto Nacional de Biodiversidad (INBio)). These indi­ viduals are explicitly trained professionals who explore, collect, sort, document, and identify specimens, usually to order, family, or generic levels. At the same time, demands for taxo­ nomic services are growing in biodiversity sci­ ence, conservation, and natural resource management (Kim and Byrne 2006). Sucking lice (Anoplura) are obligate, perma­ nent ectoparasites of selected groups of mam­ mals; Anoplura biodiversity can be estimated accurately because the survival of sucking lice depends on the host’s survival (Kim et al. 1993). If the host species becomes extinct, sucking lice that specialize on that host also become extinct (Stork and Lyal 1993). The world fauna of suck­ ing lice is estimated at 1540 species, of which 532 from more than 828 species of mammals were listed in “The sucking lice (Insecta, Anoplura) of the world” (Durden and Musser 1994, Kim et  al. 1993, Kim 2007). Thus, about 1831 species of extant mammalian host species are expected to harbor 1008 new species of sucking lice. Even a well‐studied regional fauna, such as North American insects, is barely 50% known, with only a small proportion of species described in the larval stage (Kosztarab and Schaefer 1990a). North American biodiversity of insects was estimated to be about 200,000 species: the total number of known species (90,968), plus the estimated total number of undescribed spe­ cies (98,257–98,767). The task of describing North American insects, including the imma­

ture stages and both sexes, would involve about 1,200,000 descriptions for 200,000 species (Kosztarab and Schaefer 2009b). Although rapid advances have been made in molecular biology, genetics, theoretical ecology, and other branches of biology over the past quarter century, alpha taxonomy has declined precipitously. Financial support and training for taxonomists has been eroded by declining pres­ tige and job opportunities. The most troubling aspects of this erosion are the rapid decline in human resources, namely practicing taxonomic specialists at the PhD level and parataxonomists with undergraduate degrees and one or two years of postgraduate training in taxonomic ser­ vices. Some important taxa have a shortage or absence of taxonomists. Even if the level of human resources at the 1990 level were main­ tained, the number of taxonomists still would be too low to facilitate the advancement of alpha taxonomy for the roughly 8 million species that require description. The moribund state of insect taxonomy has negatively affected the advancement of community ecology, ecosystem management, and conservation (Gotelli 2004), forcing ecologists and conservation biologists to come up with taxonomic surrogates (e.g., genus taxa or family taxa instead of species) and “morphospecies” without generic names (Krell 2004, Bertrand et al. 2006, Kim and Byrne 2006, Biaggini et al. 2007). DNA barcoding initiatives have to rely on the “BIN” (Barcode Index Number) concept (Ratnasingham and Hebert 2013) to accommodate clusters of similar DNA barcodes without taxonomic verification. Taxonomy is no longer solely the taxonomists’ domain but has become an important scientific tool for applied biologists and environmental scientists, particularly those working at the spe­ cies level. A dichotomy exists in the perspective of taxonomy. Systematists view taxonomy as a research discipline, whereas all other scientists consider it a service discipline (Donoghue and Alverson 2000, Brooks and McLennan 2002). In reality, it is both. In recent years, demand for taxonomic services has increased, while the capacity for taxonomic services has declined.

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These contradictory trends have stymied the advancement of community ecology and nature conservation. Taxonomic keys that can be used by people without much training in insect iden­ tification are increasingly demanded by the con­ servation community. Because of this trend, professional concern over misidentification has been raised (Ehrlich 2005, Kim and Byrne 2006). A shortage of taxonomists is now felt at all levels because of the decline in job and training opportunities and the lack of taxonomic instruc­ tion at educational institutions (Wheeler et  al. 2004, Kim and Byrne 2006). Efforts in taxonomy are slowly shifting from Europe and North America, where taxonomic training and research has been historically centered, to developing regions of the world where hotspots of biodiversity exist (Kim and Byrne 2006). Global climate change, along with habitat destruction and pollution, directly affects biodi­ versity at various spatial and temporal scales, making the study of biodiversity an urgent chal­ lenge for the scientific community everywhere (Strange and Ayres 2010, Zeuss et al. 2014). The community must take these challenges seri­ ously, building new infrastructure and provid­ ing taxonomic services through which a new generation of applied taxonomists can be edu­ cated. A self‐supporting infrastructure would promote biodiversity science that trains under­ graduate students and attracts young scientists who enjoy working with insects. Backyard bio­ diversity, thus, could be explored and docu­ mented for local sustainable development at the grassroots level, enriching and expanding the knowledge base of global biodiversity (Kim and Byrne 2006).

24.4 ­Biodiversity Inventory and Ecology Biodiversity can be discussed in abstract or the­ oretical terms, without referring to spatial or geographic units. We can talk about biodiversity and ecosystem functions without regard to spe­ cific locations or scales because they are

i­nterdependent and related. However, biodiver­ sity is meaningless when it is not defined by spa­ tial or geographic coordinates or at specific biological scales because species composition and assemblage patterns are site specific. We can understand patterns of what and how differ­ ent species or guilds function and interact in a community by using numerical indices of diver­ sity, richness, and evenness. Such observations appear obvious to most eyes for large organisms such as primates, seals, and trees. But observa­ tions and statistics do not provide information about what species are present and what they do in sustaining ecosystem functions at a spe­ cific site. There is an urgent need to undertake explora­ tion and documentation of biodiversity through­ out the world. In my view, we should increase our knowledge base of global biodiversity to at least 50–60% of the extant biodiversity on the planet by 2025. With what remains of the con­ temporary taxonomic cohort, however, this challenge seems to be impossible. We need new approaches to global biodiversity inventories. Although individual taxonomists continue to discover and describe new species, efforts to explore and document backyard biodiversity at the grassroots level everywhere in the world are needed. The resulting database will be funda­ mental to building a local economy based on local natural resources and capital. Ecology, the study of the interactions among organisms and their physical environment, is the science of uncovering the cause of patterns in natural and managed ecosystems (Tilman and Lehman 2001). Biodiversity, from an eco­ logical perspective, is commonly expressed in terms of the number of species and their relative abundance in a locality (e.g., the Shannon index), without much reference to species com­ position. Tilman and Lehman (2001) recognized two different perspectives of biodiversity: (i) species diversity, that is, the number of species, or species richness versus evenness, in a habitat; and 2) functional diversity, that is, the range of species traits in an area. Because ecological models usually focus on quantitative indices to

24  Taxonomy and Management of Insect Biodiversity

study productivity, resource dynamics, and ­stability in the context of ecosystem function (Kinzig et  al. 2001), taxonomic diversity and species composition of a community are consid­ ered unimportant and are often ignored. However, the goals of biodiversity science include assessing taxonomic diversity and spe­ cies composition of a community because inter­ acting species can be affected by specific stresses. In this context, we must know which species of insects are involved. Conservation and ecosystem management need specific data on species composition because community assemblages differ in habi­ tat characteristics and show different responses to extinction thresholds (Lande 1987; Bascompte and Solé 1996, 1998; Lin et al. 2005; Lin and Liu 2006). There is a void where surveying and sam­ pling methodologies in insect diversity invento­ ries should be (Mahan et al. 1998, Boone et al. 2005). As a result, most natural resource agen­ cies, such as national and state parks, lack base­ line, site‐specific biodiversity data that should be a basic guide for all other resource‐manage­ ment programs. Biodiversity inventory data should be available for ecosystem management of public lands. The species composition and assemblage of every community and ecosystem are site specific (Hector and Bagchi 2007). In other words, the management of communities and ecosystems requires more than just know­ ing general patterns. It needs to focus on build­ ing the baseline data on species composition, assemblage structure, and interactions of guilds (Mahan et al. 1998, Boone et al. 2005, Kim and Byrne 2006), particularly for insects and other invertebrates that make up the bulk of every community and ecosystem (Coleman and Hendrix 2000). Every species is unique; thus, species are not interchangeable (Nee and May 1997, Brooks and McLennan 2002). Site‐specific biodiversity is unique because of different physical architec­ tures and ecological processes at each site, although general patterns of distribution and species richness might be similar among habi­ tats. Local species assemblages are influenced

and shaped by local and regional processes (Ricklefs 1987, 2004; Cornell and Karlson 1997; Gaston and Blackburn 2000; He et  al. 2005; Shurin and Srivastava 2005). Biodiversity involves the total composition of resident spe­ cies in a spatially defined area. Every species matters in conservation until we know more about global biodiversity and what the species are doing to sustain our life‐support system. We simply do not know enough about biodiversity to make a final call about the destiny of certain species. Ecological processes at both local and regional scales include competition, distur­ bance factors, immigration, mutualism, parasit­ ism, and predation. Species of a guild in one community might not have the same ecological role as related species of the same guild in a dif­ ferent community (Kim 1993b, Coleman and Hendrix 2000, Hector and Bagchi 2007). This trend is particularly evident when insect biodi­ versity is involved in any community or ecosys­ tem (Coleman and Hendrix 2000, Wardle 2002, Schmitz 2007). To manage natural resources, restore habitats, or conserve species of concern, the biodiversity of specific areas or targeted habitats needs to be assessed, requiring a comprehensive but effi­ cient means to inventory the organisms and what they do in the system (Kinzig et al. 2001; Loreau et al. 2001, 2002; Hooper et al. 2005; Kim and Byrne 2006). Without knowing which spe­ cies are represented or which species previously recorded are now missing, biodiversity assess­ ment would be meaningless and could not con­ tribute much to conservation, restoration, or management of ecosystems. To advance biodi­ versity science, therefore, biodiversity assess­ ment and appropriate measures of biodiversity change become important. Ecosystem management requires biodiversity assessment with social and humanistic factors considered, which includes documentation of endangered or threatened species for ultimate mitigation (Kim 1993b). Assessing and conserv­ ing biodiversity invariably involve serious taxo­ nomic issues that include both taxonomic inflation (Bertrand and Härlin 2006, Padial and

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de la Riva 2006) and taxonomic surrogacy (e.g., so‐called morphospecies, albeit not in a taxo­ nomic sense) (Oliver and Beattie 1996, Derraik et al. 2002, Bertrand et al. 2006, Biaggini et al. 2007). These approaches are taken by applied scientists to support their immediate problem solving and do not add much understanding to biodiversity patterns (Krell 2004, Bertrand et al. 2006). They actually make taxonomic problems in biodiversity conservation more complicated, without adding much useful information. Considering the heterogeneity and diversity of ecological niches, no simple survey technique can cover all species in a community. Many sur­ vey techniques used in taxon‐based surveys and ecological research are suitable only for targeted taxa or specific research objectives. Biodiversity inventories must be designed for specific objec­ tives. If an inventory is to assess the biodiversity of an area, a survey strategy must consider quantitative and qualitative information on the resident biodiversity over all seasons. The inventory design must include a sampling scheme, techniques, and protocols for capturing representatives of all resident species at the site (Mahan et al. 1998; Kim 2001b, 2006). Because quantitative techniques often miss species that are seasonal, periodic, or influenced by local weather conditions, taxon‐based collecting or specific surveys can be supplemented with sur­ veys to capture unique or specialized species that do not appear in standard samples or gen­ eral surveys.

24.5 ­Backyard Biodiversity and Sustainability Since our ancestors became settlers with farm­ ing technology, natural ecosystems have been transformed into cultivated lands, with selected species of plants and animals domesticated for food and other human amenities. With the development of farming communities, small towns began to flourish and eventually expanded and merged with others into larger cities (Ponting 1991). This process invariably destroyed

biodiversity and habitats of resident species in the transformed land. Modern development likewise transforms nature into farmland or human habitation. In the process, primary (or natural) biodiversity is destroyed. Anthro­ pocentric transformation of natural lands then acquires secondary (or human‐based) biodiver­ sity that usually has limited species richness. The concept of backyard biodiversity high­ lights the importance of appreciating local bio­ diversity on a scale at which human activities determine local ecosystem services. Backyard biodiversity promotes local conservation efforts by providing the basic natural knowledge for local leadership (Schwartz et  al. 2002, Mascia et al. 2003, Berkes 2004). Backyard biodiversity also encompasses those organisms inhabiting private properties, neighborhoods, and local municipalities. All these perspectives are rele­ vant to local needs, cultures, and land‐use regu­ lations (Center for Wildlife Law 1996, Farber et al. 2006). Because global biodiversity hotspots (Mittermeier et al. 2005) are located in under­ developed or developing countries of the world, backyard biodiversity will promote local con­ servation efforts as a part of sustainable eco­ nomic development. Since the Rio Declaration of Biological Diversity and Sustainable Development in 1992, conservation plans and policies for biodiversity and ecosystems have been developed at global, national, and regional levels. However, biodi­ versity conservation and ecosystem manage­ ment must occur at a local scale, at which factors influencing realistic conservation practices are related to cultural and economic interests of the local people. Knowing backyard biodiversity provides the necessary knowledge base for improving economic well‐being. Comprehensive backyard biodiversity databases provide the baseline information about local natural resources and capital for ecosystem services (Lundmark 2003). A backyard biodiversity data­ base provides a scientific basis for sustainable economic development, and collectively, the global database of all backyard biodiversity from around the world will aid the establishment of a

24  Taxonomy and Management of Insect Biodiversity

comprehensive plan for sustainable economic development at all geographic levels, from local to global.

24.6 ­Taxonomic Bottlenecks in Managing Insect Biodiversity Biodiversity assessment requires taxonomic services. The assessment process involves: (i) inventory of an area, which yields a large col­ lection of specimens; (ii) field‐collection man­ agement, which requires preparation, sorting, labeling, and management of specimens; (iii) taxonomic services, which include the iden­ tification of sorted specimens; and (iv) building a biodiversity database for the inventory site (Kim 1993b, Mahan et  al. 1998, Kim and Byrne 2006). A biodiversity inventory program faces major scientific and technical challenges that require resolution. Taxonomic infrastructure must be built for each country or a core of regional set­ ups. Biodiversity inventories generate great numbers of specimens, from several thousand in small projects to a million or more in large, multi‐year projects (Mahan et  al. 1998; Kim 2001b, 2006), which must be processed and pre­ pared for species identification and which invariably include new species that require description. Species identification and taxo­ nomic processing of field samples involve a good number of trained taxonomic technicians (e.g., parataxonomists) and taxonomic scien­ tists. New technologies, such as DNA barcod­ ing, have been developed for identification (Wilson et al., this volume; www.barcodeoflife. org). However, all of this requires a stable infra­ structure with a regular source of funding to retain well‐trained parataxonomists and a net­ work of taxonomic scientists for providing iden­ tifications. This inventory process is time consuming and labor intensive for technicians or parataxonomists and requires the close atten­ tion of taxonomic specialists; these aspects often discourage ecologists and conservation biologists from undertaking biodiversity

a­ ssessments involving insects. As a result, prac­ tically no resource management units in federal and state public lands (e.g., national parks) in the United States have developed biodiversity assessments, and little advancement has been made in community ecology and conservation biology (Gotelli 2004, Kim and Byrne 2006, Rohr et al. 2006). Taxonomic bottlenecks in biodiversity research have been recognized and their ­resolution advocated (Gotelli 2004, Boone et al. 2005). Taxonomic bottlenecks have serious con­ sequences for applied science, conservation biology, and natural resource and ecosystem management (Kim and Byrne 2006). Historically in the United States, species identification was provided gratis by taxonomic specialists and parataxonomists of federal (e.g., the US Department of Agriculture/Agriculture Research Service Systematic Entomology Laboratory) and state agencies associated with agriculture (e.g., the Florida State Collection of Arthropods and taxonomists in land‐grant institutions). This practice has virtually ceased. With the decline of taxonomy worldwide and the shortage of taxonomic specialists, taxo­ nomic services are becoming increasingly costly and difficult to obtain. Backyard biodiversity must be documented so that the resulting database becomes the basis on which ecosystem management and sustain­ able development can be applied to local, human‐dominated ecosystems. New strategies for taxonomic services and biodiversity educa­ tion must be developed. Even if education pro­ grams were instituted now, at least five years would be needed before taxonomic specialists were available for taxonomic services. An Integrated Biodiversity Assessment Center (IBAC), an infrastructure for providing taxo­ nomic services, could be networked from the grassroots to the national level to share specific taxonomic expertise and informatics through­ out the world (Kim and Byrne 2006). Each IBAC, with several permanently employed taxonomists, should be based on a national systematics collection, or at least

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a­ssociated with established collections, for ­reference and voucher deposition. IBACs would provide taxonomic services, including (i) plan­ ning and execution of exploratory field sam­ pling and collection, (ii) sorting and preparation of field samples for identification and manage­ ment, (iii) species identifications, (iv) individu­ alized biodiversity databases, and (v) long‐term storage and management of voucher collections and archival field collections. Once established with government funds and grants, IBACs should be self‐supporting from the fees for ser­ vices rendered. Taxonomic services provided by IBACs would be tailored for specific needs of users in research, conservation, detection of exotic and invasive species, and ecosystem management, and could provide diverse train­ ing programs such as annual seminars, work­ shops for specific regional taxa, and internships for undergraduate and graduate students in applied taxonomy (Kim 2006, Kim and Byrne 2006). IBACs would promote the advancement of biodiversity science, which in turn would increase the knowledge base of global biodiver­ sity from approximately 1.8% to as much as 50% by 2025. Local IBACs and a network of IBACs globally will facilitate the process of building taxonomic human resources and training future biodiversity scientists. At the grassroots level, IBAC associates who are familiar with local backyard biodiversity could be trained as para­ taxonomists. They then could lead biodiversity‐ related activities such as integrated pest management, sustainable agriculture, and mon­ itoring of non‐indigenous invasive pests (Kim and Byrne 2006). A centralized international IBAC database, based on the merger of back­ yard biodiversity databases through a network of global IBACs, would be a de facto global bio­ diversity database, providing the scientific basis for a broad range of civic and public works that would be readily available to users across diverse scientific and technical communities, including systematics, ecology, conservation biology, environmental technology, land‐use planning, and drug prospecting. The globally networked backyard biodiversity inventory would not only

produce local biodiversity databases, but also facilitate the discovery and documentation of new species.

24.7 ­Advancing the Science of Insect Biodiversity Massive industrial and technological advance­ ments during the past century brought about great economic development and affluence. This anthropocentric success came with enor­ mous environmental baggage. The process con­ tinues, but at a far faster pace throughout the world. In the last part of the 20th century, we identified the largest environmental decline caused by human abuse of the environ­ ment  –  global warming and climate change. Humanity is now at a crossroads where it must decide whether and how to control the causes and effects of human endeavors, such as defor­ estation, development, and pollution. Global climate change affects all organisms, including insects and humans, and could cause devastation to human infrastructure and the economy. Its effect on biodiversity, particularly insect biodiversity, would be serious and long lasting, involving changes in physiologies, pop­ ulations, and life histories of organisms; shifts in distributions and geographic ranges of species; and changes in species composition and the structure and function of ecosystems (Canadell and Noble 2007). The effects of these changes might show up, for example, in seasonal pat­ terns of events, such as the timing of migration and reproductive cycles (McCarty 2001). Global climate change affects the population growth and ecological roles of insects, particularly of common herbivores that eat crops and those species that transmit pathogens to humans and animals (Kim and McPheron 1993, McCarty 2001, Botkin et  al. 2007, Easterbrook 2007, IPCC 2007). Ecosystem processes that are already stressed, such as carbon cycling and storage, and species that are already endangered or threatened will probably feel the brunt of global warming (Sala et al. 2000, Parmesan and

24  Taxonomy and Management of Insect Biodiversity

Galbraith 2004). Climate changes due to global warming, such as the frequency and strength of hurricanes and droughts, will elevate the risk of extinction or extirpation. In addition to global warming, today’s envi­ ronmental concerns, such as biodiversity loss, land transformation, habitat loss, pollution, and changes in ecosystem services, are caused by human activities (MEA 2005). Global warming and climate change represent the foremost manifestation of the anthropocentric effects of development and pollution. Our basic approaches to economic development have not changed much, despite global environmental movements persistently pursued by the United Nations (CBD 2000, 2014). We must systematically inventory backyard biodiversity throughout the world as a part of sustainable economic development. These inventories are fundamental to a scientific basis for land‐use planning, conservation and management of lands, natural resource man­ agement, and sustainable economic develop­ ment. They provide the information for combating immigrant pests and invasive spe­ cies that are major factors in current biodiver­ sity loss. Our knowledge base for biodiversity, particularly of insects, would contribute to the protection and management of backyard bio­ diversity. The pursuit of sustainability requires new conceptual and practical approaches, and biodiversity science provides a means to meet those challenges. We face a paradox involving the need for tax­ onomic services on the one hand and taxonomic demise on the other (Kate and Kress 2005, Olden and Rooney 2006, Stribling 2006, Walter and Winterton 2007). Concerns over the scien­ tific and social effects of taxonomic decline have been expressed in major scientific journals, without much heed (Savage 1995, Wheeler 2004, Wheeler et al. 2004). In recent years, how­ ever, renewed pronouncements on the needs for taxonomy and a reversal of taxonomic decline have appeared in popular magazines and news media. They differ from past efforts because the writers represent broader scientific disciplines,

such as conservation biology and ecology (Ehrlich and Wilson 1991, Kim 1993b, Godfray and Knapp 2004, Gotelli 2004, Ehrlich 2005, Kim and Byrne 2006). Yet, the core issues in the taxonomic domain have not shifted to meet the applied needs. Global climate change, along with habitat destruction and pollution, directly affects biodiversity at various spatial and tem­ poral scales, making the study of biodiversity urgent. All of these issues represent important challenges to science policymakers and the sci­ entific community at large. The historic decline of taxonomy and the increasing shortage of taxonomic specialists make it difficult to obtain accurate identifica­ tion of scientifically and economically impor­ tant species. At the same time, no other means are available to have insects identified to lower taxonomic units because trained and knowl­ edgeable parataxonomists are scarce and no pri­ vate infrastructure for taxonomic services exists (Gotelli 2004, Kim and Byrne 2006). New gen­ erations of biologists and environmental scien­ tists bypassed taxonomic training and natural history. This is mainly because many institu­ tions of higher learning reduced curricular requirements in these subject areas as a result of funding opportunities and new discoveries in molecular biology, which shifted the interests of young scientists away from systematics. Major curricular shifts in undergraduate and graduate education produced biologists who are knowl­ edgeable about molecular biology, genetics, and perhaps phylogenetics but who have little understanding of species concepts, taxonomy, or basic methods for classification and identifi­ cation of organisms. As a result, today’s genera­ tion of biologists is ill prepared to conduct the alpha‐taxonomic tasks required.

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Pew Center on Global Climate Change, Washington, DC. 56 pp. Ponting, C. 1991. A Green History of the World: the Environment and the Collapse of Great Civilizations. Penguin Books, New York, NY. 432 pp. Ratnasingham, S. and P. D. N. Hebert. 2013. A DNA‐based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8 (8): e66213. Raup, D. M. 1991. Extinction: Bad Genes or Bad Luck? W. W. Norton, New York, NY. 228 pp. Ricklefs, R. E. 1987. Community diversity: relative roles of local and regional processes. Science 235: 167–171. Ricklefs, R. E. 2004. A comprehensive framework for global patterns in biodiversity. Ecology Letters 7: 1–15. Rohr, J. R., C. B. Mahan and K. C. Kim. 2006. Developing a monitoring program for invertebrates: guidelines and a case study. Conservation Biology 21: 422–435. Sala, O. E., F. S. Chapin, J. J. Armesto, E. Berlow, J. Bloomfield, R. Dirzo, E. Huber‐Sanwald, L. F. Huenneke, R. B. Jackson, A. Kinzig, R. Leemans, D. M. Lodge, H. A. Mooney, M. Oesterheld, N. L. Poff, M. T. Sykes, B. H. Walker, M. Walker and D. H. Wall. 2000. Global biodiversity scenarios for the year 2100. Science 289: 1770–1774. Savage, J. M. 1995. Systematics and the biodiversity crisis. Bioscience 45: 673–679. Schmitz, O. J. 2007. Ecology and Ecosystem Conservation. Island Press, Washington, DC. 184 pp. Schwartz, M. W., N. L. Jurjavcic and J. M. O’Brian. 2002. Conservation’s disenfranchised urban poor. BioScience 52: 601–606. Shurin, J. B. and D. S. Srivastava. 2005. New perspectives on local and regional diversity: beyond saturation. Pp. 399–417. In M. Holyoak, M. A. Leibold and R. D. Holt (eds). Metacommunities. University of Chicago Press, Chicago, IL. Sohdi, N. S., L. P. Koh, B. W. Brook and P. K. L. Ng. 2004. Southeast Asian biodiversity: an

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25 Insect Biodiversity – Millions and Millions May Berenbaum Department of Entomology, University of Illinois, Urbana, Illinois, USA

Relatively few scientific truths persist across centuries; new technologies, new hypotheses, and new information mean that most scientific conclusions are constantly modified, updated, or even sometimes discarded. One conclusion, however, seems robust even as new information has accumulated across the centuries – namely, that there are a lot of insects. Ever since Linnaeus imposed order on the classification of living organisms, six‐legged animals with exoskeletons have had an edge over other groups. Of the 4203 species of animals described by Linnaeus, insects constituted 2102, more than half of the known animal diversity at the time. Species descriptions proceeded apace once Linnaeus provided a flexible framework for naming and classifying them, but as species piled up across all taxa, they piled up fastest for insects. Between 1758 and 1800, 58,833 insect species were described, and between 1800 and 1850, 363,588 species were added to the pantheon of known species. As other paradigms in biology came and went, the notion that insects are the dominant life form on the planet remained unchanged by new data. Relatively early in the history of insect taxonomy, even before Linnaeus imposed order and structure on biological diversity, the question arose as to just how many insects might be on the planet. Almost every chronicler of insect life

dating back to the 17th century has felt ­obligated to venture a guess. Sir John Ray, the great British naturalist who authored the Wisdom of God in the Works of His Creation in 1691, attempted a projection based on his own experiences in his homeland: Supposing, then, there be a thousand several sorts of insects in this island and the sea near it, if the same proportion holds between the insects native of England and those of the rest of the world…, the species of insects in the whole earth (land and water) will amount to 10,000: and I do believe they rather exceed than fall short of this sum. (Cited in Westwood 1833) Ray later revised his own estimate upward by twofold, based on his own discoveries of new species of English moths of butterflies, but in 1815 William Kirby and William Spence, authors of An Introduction to Entomology, the first textbook of entomology, still regarded the estimate of 20,000, “which in his time was reckoned a magnificent idea” as “beggarly,” by 19th‐ century standards. Their own assessment was influenced by the fact that their contemporary DeCandolle had estimated the number of plant species at 110,000 to 120,000. Observing that each British plant was typically associated with

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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at least six insect species, Kirby and Spence reasoned, “if we reckon the phanerogamous ­vegetables of the globe, in round numbers at 100,000 species, the number of insects would amount to 600,000.” By 1833, John Obadiah Westwood, a curator at Oxford and thus familiar with the “immense influx of novelties which has been poured into our museums and cabinets since the days of Linnaeus … especially in the insect tribes” attempted to estimate the “numerical extent of this department of nature.” He arrived at his estimate, a more conservative 400,000, by comparing the rate at which new species were described to the number already known across different key groups. Illustrative of the expansion of knowledge were the carabid genera Carabus and Cicindela; within 70 years, the 50 species collectively described within these genera by Linnaeus had expanded to more than 2000 species, a 40‐fold increase. Such estimates opened a can of (very diverse) worms and kicked off a discussion among insect systematists that continues to this day. Howard (1931) provided a summary of the controversy through the end of the 19th century in his book The Insect Menace. He quotes, for example, one Dr David Sharp, a British coleopterist, who in 1833 hazarded his guess: “As the result of a moderate estimate it appears probable that the number of species of true insect existing at present on our globe is somewhere between five hundred thousand and one million,” adding that, “the number probably exceeds the higher of these figures and will come in near to two million.” Howard also quotes Lord Thomas de Grey Walsingham, President of the Entomological Society of London from 1889 to1890, who chose in his presidential address to endorse Sharp’s estimate. Across the Atlantic, however, Charles Valentine Riley arrived at a different conclusion: [A]fter considering the fact that the species already collected are mostly from the temperate regions of the globe and that many portions of the world are as yet unexplored by collectors of insects, and further that the

species in many groups of insects are apparently unknown  –  that the estimate of 2,000,000 species in the world, made by Dr.  Sharp and Lord Walsingham, was extremely low and that it probably represented not more than one fifth of the species that actually exist. And, with that, Riley boldly elevated the estimate by an order of magnitude to 10,000,000. Such a high estimate did not sit well with the entomological establishment of the era; according to Howard, “it met with no favorable comment. Everyone thought it was too high.” In reviewing the history, Howard speculated that at the time few people other than astronomers and geologists had any grasp of a figure as large as 10 million. Having reviewed the various estimates, Howard himself tried another approach. He took the question to a meeting of the Entomological Society of Washington, attended by a number of experts in many of the larger insect taxa. There, he asked everyone present to estimate the proportion described within the groups they knew best, figuring that “because of the character of the men who took part in this discussion it was probably the most authoritative expression of opinions that could very well be had.” Summing the individual estimates led Howard to suggest that an estimate of 4 million was reasonable. Character notwithstanding, debate did not end with the meeting of the Entomological Society of Washington. Metcalf (1940) picked up the gauntlet soon thereafter. Eschewing any effort to count the total number of insect individuals (because “no one has been foolhardy enough to attempt to make a world census of insect individuals”), he attempted, as his predecessors had, to estimate the number of species. At the time, textbooks pegged the number at between 250,000 and 1 million. As the basis for his estimate, he examined the changing ratios of genus to species over time and revised the estimate upwards to 1.5 million. He was realistic enough to recognize the limitations on his

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e­ stimate, however, and philosophized about the futility of such efforts: At least they have done this; they have occupied my thoughts on a hazy Indian summer day; their calculations have kept an otherwise idle adding machine busy; and last by no means least important I hope they have stimulated your thoughts in this field. … they will make those of us who profess to be systematists more systematic as we go about our daily business of describing new genera and species, so that those who come after us will not have to do too much counting and recounting. Despite the good intentions, counting and recounting continued. In addition to citing estimates by Metcalf and Flint (1939, 1951), who suggested that there were 916,000 species of insects in the world, and by Ross (1948), who pegged the number at 1.115 million, Sabrosky (1952) pointed out in his chapter of the 1952 Yearbook of Agriculture that 6000 to 7000 species of insects were being described every year. He engaged in a different kind of calculation to convey the magnitude of the number of species already described, estimating that, “If the names were printed one to a line in an eight‐page, eight‐column newspaper of average size, without headlines and pictures, more than eight weeks, including Sundays, would be needed to print only the names of the insects that are already known in the world” (Sabrosky 1953). Sabrosky was among the first to suggest that synonymies might inflate the count of described insects and accordingly elevate estimates of total insect diversity. Subsequently, he proposed a one‐time census of all animal species, to commemorate the 200th anniversary of Systema Naturae (Sabrosky 1953). As it happens, 1958 came and went without that definitive census and, after an extended pause, discussions of total insect biodiversity resumed once more. What apparently precipitated the next round of pitched discussion was an estimate based on a new approach. Terry

Erwin (1982) evaluated the number of beetle species found in association with one species of tropical tree, Luehea seemannii, exhaustively collecting them by fogging the canopy with an insecticide. After identifying the species known to science, he could estimate the ratio of described to undescribed species of Coleoptera. He then estimated the degree of host specificity of each feeding guild represented in the collection, calculated the ratio of coleopterans to other arthropods, guessed at the relative ratio of canopy to ground‐dwelling arthropods, and multiplied by the estimated number of tropical tree species in the world, to obtain an estimate of world insect diversity of approximately 30 million (Erwin 1988). Although Erwin’s estimates were advanced as a testable hypothesis, rather than a definitive number (Erwin 1991), the sheer magnitude of the number commanded attention among entomologists (e.g., Stork 1988, Adis 1990). Not everyone embraced the new methodology, and a flurry of publications followed; in the context of growing concerns about biodiversity losses, estimates of total insect diversity had gained new importance. Robert May (1988, 1990) took another tack, extrapolating based on the general relationship between size and species diversity across all organisms. Basically, over the range of body lengths from several meters to 1 cm, for each order of magnitude reduction in length (or 100‐fold reduction in body weight), the number of species increases 100‐fold. Problematically, the relationship is less clear for taxa less than 1 cm long, which encompasses the majority of insects, but extrapolating the relationship leads to an estimate of approximately 10 million species of terrestrial animals (May 1988), of which approximately three‐quarters are insects. Yet another approach was taken by Hodkinson and Casson (1990), who enumerated the hemipteran species represented in an exhaustive collection of Sulawesi arthropods; they determined that approximately 62.5% of the 1690 species collected were undescribed. Assuming that the same proportion of the world’s true bugs were undescribed, they arrived at an estimate of

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184,000–193,000 species of bugs worldwide, and assuming that true bugs comprise approximately 7.5–10% of the world’s insects, they ­produced an estimate of 1.84 million to 2.57 million insect species in total. Gaston (1991a, 1991b) returned to the approach used by Westwood (1833) and Howard (1931) in earlier centuries and polled expert taxonomists for their best estimate of what proportion of their taxon of interest was undescribed; most estimates were optimistic (i.e., that the difference was less than fivefold), leading him to an estimate of 5 million (given that the number of described species was in the neighborhood of 1 million). Concerns about synonymies reared their ugly head once again, as did concerns about sampling, leading Stork (1993) to revise the Erwin estimates downward to between 5 million and 15 million. By 2002, sufficient data existed from a variety of biotic diversity inventories to allow Odegaard et al. (2000) to correct earlier estimates based on the degree of host‐ plant specialization of phytophagous insects associated with a restricted number of plant species. He extrapolated this to a larger number of plants, as did Kirby and Spence (1815) almost two centuries earlier, arriving at a modified estimate of 5 million to 10 million species. Systematists have argued not only about the total number of insect species, but also the number of insects already described, a figure that would seem to be robust and beyond dispute. On the one hand, there are problems with synonymies; Alroy (2002) has estimated that “24–31% of currently accepted names eventually will prove invalid” due to synonymies or nomina dubia (that is, “30% of named species are illusions created by unsettled taxonomy”). On the other hand, new molecular approaches have revealed substantially greater species diversity than was hitherto suspected to exist. Smith et al. (2007) used DNA barcoding to evaluate 16 morphospecies of apparently generalist tropical parasitoid flies in the family Tachinidae and found that the 16 generalist species apparently represent nine generalist species and 73 specialist lineages. Given that parasitoids are

thought to represent 20% of all insect species, gross underestimates of parasitoid species diversity might mean that the global species richness of insects may also be grossly underestimated. Adding to the challenge of estimating insect diversity is the fact that systematists keep getting better at their job; as DNA sequencing methods become faster and cheaper, the number of new species discovered keeps increasing (Bickford et al. 2007), particularly when multiple methods are used to differentiate species. Smith et al. (2008), for example, combined morphological analysis, host specificity, and DNA barcoding to evaluate 2597 microgastrine braconid parasitoid wasps from three different habitats in northwestern Costa Rica; an initial morphological analysis revealed 171 provisional species, but that number nearly doubled when barcoding was applied and revealed an additional 142 species (for a total of 313). Moreover, as entomologists are gaining access to more and more remote habitats as a result of rapidly increasing rates of development and less‐life‐ threatening modes of transportation, species are being discovered and described at unprecedented rates. The State of Observed Species report from the International Institute for Species Exploration revealed that 13,903 new living species of insects were discovered in 2009 alone, of which 3485 were beetles (Wilkins 2012). Thus, the rate of discovery of new species has tripled in the past 120 years, which in turn was quadruple the rate 120 years before that (Marlatt 1898). In recent years, the suggestion has been made that entomologists and other systematists might finally be running out of new species to find; the number of systematists in business today by some estimates is greater than at any previous time in history (Costello et al. 2013, 2014) and the rate of discovery of new species per investigator is declining, at least for some insect taxa (Löbl and Leschen 2014). Indeed, at least among British beetles, larger species have historically been discovered and described earlier than smaller (and presumably harder‐to‐find) ­species

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(Gaston 1991c). Stork et  al. (2015) are, thus, sanguine about the prospects of finally settling on an estimate of the total number of all insect species in existence, in large part because comparisons of four autonomous estimates of beetle species diversity (which constitutes the biggest portion of insect diversity, at least according to prevailing wisdom) have converged on values between 0.9 million and 2.1 million; using a similar comparative method, these authors calculated convergent estimates for total global insect diversity of between 2.6 million and 7.9 million species, which is, indeed, “surprisingly narrow” in the context of the wildly divergent historical estimates. That there has been a debate raging among entomologists about Earth’s total inventory of insect species for more than four centuries has gone largely unnoticed by the general public. Indeed, it is unlikely that there is even a vague notion among the general public of the extent of arthropod diversity. The level of appreciation of insect diversity rarely extends beyond the ordinal level and at times fails to achieve even that degree of differentiation. This unfortunate state of affairs is not new; Dan Beard, for example, in his 1900 book Outdoor Games for All Seasons: the American Boy’s Book of Sport, bemoaned the fact that: “With the exception of butterflies, the general public class the whole insect world under two heads – worms and bugs – and regard them with unqualified disgust. But this is only a sign of universal ignorance.” In attempting to characterize public attitudes toward invertebrates, Kellert (1993) administered a questionnaire to determine the “level of knowledge” of invertebrates in general. Individuals surveyed included randomly selected residents of the New Haven, Connecticut area, along with subsamples of farmers, conservation organization members, and scientists. Of the various categories of knowledge investigated, the general public “revealed the least knowledge of taxonomic differences among invertebrates … and  –  ­ taxonomically  –  toward bees, cockroaches, grasshoppers, termites and beetles.” Specifically, “only a minority had much concept

of the overall number of insect species,” fewer than one‐quarter knew that spiders are not insects, and only 11% recognized that cockroaches are not beetles. Taxonomic confusion extended beyond the phylum Arthropoda  –  a majority of respondents thought that “snails are more closely related to turtles than to spiders” and that “the snail darter [a fish] is an endangered butterfly.” Even relatively sophisticated members of the public appear content with their taxonomic ignorance. Snopes.com, a website devoted to myth‐busting and correcting popular misconceptions on a wide range of topics, including scientific ones, claims that the statement “The food colorants cochineal and carmine are made from ground beetles” is “True” (Mikkelson 2013), despite the fact that cochineal and carmine are derived not from any of the 350,000 or so species in the order Coleoptera but rather from Dactylopius coccus, a scale insect in the order Hemiptera. Oddly enough, the species is accurately named on the website but is described as “a beetle that inhabits a type of cactus called Opuntia.” When an entomologist pointed out their error in an e‐mail message, he was curtly informed that the authoritative reference for calling cochineal scale a beetle was Webster’s Dictionary, which defines “beetle” not only as a member of the order Coleoptera, but anything even vaguely beetle‐like (“any of various insects resembling a beetle,” http://www.m‐w.com/dictionary/beetles) (S. Bambara, personal communication). So, while biologists passionately debate the number of species awaiting discovery, the general public appears blissfully unaware of, and indifferent to, this discussion. In fact, the business of differentiating among insect species has long been regarded as a pursuit of dubious value. Kirby and Spence (1815), in the introduction to their entomology text, lamented the fact that, in the 18th century, the will of one Lady Glanville was “attempted to be set aside on the ground of lunacy, evinced by no other act than her fondness for collecting insects; and [Sir John] Ray had to appear at Exeter on the trial as a witness

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of her sanity.” What the public rarely recognizes, however, is that differentiating among and inventorying insect species is not now, nor has it ever been, an irrelevant or trivial pursuit. Insect species, as numerous and as seemingly similar as they may appear, are generally not ecologically interchangeable, and failing to recognize that fact has had tremendous economic and public health consequences over the centuries. Examples of the importance of differentiating among arthropod species are legion. In agriculture, identifying pest species correctly is often key to understanding their life histories and developing approaches for managing them. The varroa mite, for example, is a devastating parasite of the European honeybee Apis mellifera. When mites first appeared attacking honeybees in North America in the 1980s, they were assumed to be Varroa jacobsoni, a species native to Indonesia and Malaysia that had hitherto been thought to attack only Apis cerana, the Eastern honeybee. However, Anderson and Trueman (2000) conducted morphological and molecular studies and determined that the mite attacking bees in North America is a distinct species, which they named Varroa destructor. Unlike V. jacobsoni, V. destructor infests A. cerana throughout much of mainland Asia and is also capable of parasitizing A. mellifera throughout the world, to devastating effect (National Academy of Sciences 2007). No less important than identifying pest species to control them is identifying and appreciating the diversity of potential biological control agents that can be used in pest‐management programs. Many programs have failed or experienced decades‐long delays simply because the diversity of potential control agents was not fully recognized (Caltagirone 1981). California red scale, Aonidiella aurantii, for example, is an important pest of citrus that was accidentally introduced into California in the 19th century, most likely from Southeast Asia. For close to 60 years, biocontrol efforts ignored ectoparasitoid wasps in the genus Aphytis as potential control agents because Aphytis chrysomphali was already present in the state, having been

a­ ccidentally introduced at the turn of the 20th century, and apparently had little impact on the pest. Thus, dismissing ectoparasitoids as ineffective, entomologists concentrated on potential predators and endoparasitoids, without much success. Eventually, taxonomic study of the genus revealed a complex of species, including two, Aphytis lingnanensis and Aphytis melinus, which, once introduced, proved to be significantly superior biocontrol agents for the scale (Price 1997). As biocontrol agents are not interchangeable, neither are insect pollinating agents. The establishment of a fig industry in California – which today is second only to Turkey in production of figs worldwide – was stymied for a decade in the late 19th century until entomologists recognized that one particular agaonid fig wasp species, one of hundreds within the genus, had to be imported to pollinate the trees (Swingle 1908). Similarly, cacao cultivation in Africa, outside its area of indigeneity in Mexico, was not profitable until the specific pollinators – midges in the genus Forcipomyia – were imported (Young 1982). There have been significant public health consequences of the failure to recognize and differentiate among insect species. Anopheles gambiae, for example, was long regarded as the most important vector of malaria in Africa south of the Sahara. The species An. gambiae, however, turned out to be in reality a complex of seven essentially morphologically identical species, some of which are efficient vectors and others of which are not vectors (White 1974, Hunt et al. l998). These species also differ in the degree to which they are resistant to insecticides, a fact that has major implications for control efforts (Davidson 1964). Effective management of vectors of malaria, a disease that kills 2 million to 3 million people worldwide annually, requires precise identification of species (Gentile et al. 2002). Even such unglamorous ecosystem services as waste disposal depend on a diversity of non‐ interchangeable arthropods. Introduction of placental mammals such as cattle and sheep into

25  Insect Biodiversity – Millions and Millions

Australia led to monumental problems with dung accumulation; Australian dung beetles, adapted to using dung of marsupial mammals, could not process the dung of the introduced placental livestock species. The accumulated dung threatened the livestock industry by taking substantial amounts of pastureland out of commission and led to population explosions of Musca vetustissima, the bush fly, whose larval stages thrived in the dung of the introduced species. Ultimately, more than 50 species of dung beetles, with different habitat requirements, food preferences, and phenologies, were imported to manage the dung problem (Doube 1991). More than 5000 species of scarabaeine dung beetles have been described to date (Hanski and Cambefort 1991), but how many species remain to be described is an open question. The general public would probably consider an inventory of the dung beetles of the world to be a scientific enterprise of little import. Typically, arguments made for inventorying biodiversity are based on utilitarian grounds – that hitherto undescribed species may contribute valuable new pharmaceuticals or provide useful genes for bioengineering. The vast majority, however, contribute in smaller ways that might not become apparent until they are no longer abundant enough to make that contribution. May (1990) has argued that there is a compelling argument, beyond utilitarian concerns, for cataloging biodiversity – the “same reasons that compel us to reach out toward understanding the origins and eventual fate of the universe or the structure of the elementary particles that it is built from.” Cosmology, however, has long enjoyed greater popularity with the general public than have coleopterans, and it is unlikely that appealing to the public thirst for pure knowledge will soon pay dividends in the form of increased appreciation for insect biodiversity (or even a greater understanding of the ordinal limits of the group). This has long been true; even Kirby and Spence (1815) bemoaned the fact that their detailed illustrations were viewed as amusing diversions to inspire ladies’ needlework.

Unfortunately, although the long‐term future of atomic particles seems assured and immutable, the same cannot be said for Earth’s insect biodiversity. Although there may not be a consensus on how many insect species remain to be described, an examination of known numbers is an argument for stepping up the inventory effort. According to the International Union for Conservation of Nature Red List of Threatened Species (http://www.iucnredlist.org/), 9932 species of birds have been described, of which 100% have been evaluated as to their ability to survive; of the 4842 species of mammals that have been described, 4782, almost 97%, have been evaluated (Fig. 25.1). By contrast, of the 950,000 or so species of insects that have been described, only 768 – about 0.08% – have been evaluated. Of the mammal species that have been evaluated, 1130 of 4782, or 23.6%, are threatened; of the 9932 bird species, 1194, or 12%, are threatened. By contrast, of the 768 insect species that have been evaluated, 563, or 73%, are threatened. Insects, then, despite their almost ungraspably large numbers, are at disproportionate risk of extinction. How disproportionate is an open question in that, of all of the major animal taxa on the planet, they are the least well‐characterized group. To characterize even the majority of insect species would be a massive undertaking, but the fact that the rate at which species are being described has steadily increased since Linnaeus’s day suggests that it is not an impossible one. If there is general consensus that conserving biodiversity is a good thing, then a necessary first step is to inventory that which is to be conserved. It would be a shame if one of the most durable and time‐tested biological observations – that there are a lot of insects – ceases to be true in the foreseeable future.

­Acknowledgments I thank Robert Foottit not only for inviting me to contribute this chapter, but also for patiently waiting for me to complete it well after the

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Mammals

Birds

Reptile/Amphibians

1194

1130

450

13,712

9932

4842

1532

553

28,100

950,000

Fish

Insects

(a)

Mammals

Birds

Reptile/Amphibians

98.9%

100%

6.4%

4789 4842

9932 9932

474 3712

5.4% (b)

0.08%

1532 28,100

768 950,00

Fish

Insects

Mammals

Birds

Reptile/Amphibians

1194

1130

874

450

9932

4789

768 1532

750

553

(c) Fish

Insects

Figure 25.1  Taxa threatened (in white) with extinction worldwide. (a) Number threatened as a percentage of species described. (b) Number evaluated as a percentage of species described. (c) Number threatened as a percentage of species evaluated (data from http://www.iucnredlist.org/ 2004).

25  Insect Biodiversity – Millions and Millions

­ eadline had passed (and waiting even longer for d the new edition), and I thank Peter Adler for his patience in waiting for seriously late revisions. My University of Illinois at Urbana–Champaign colleague Jim Whitfield graciously provided helpful comments on the manuscript on short notice. This manuscript was supported in part by an US National Science Foundation OPUS award.

­References Adis, J. 1990. Thirty million arthropods—too many or too few? Journal of Tropical Ecology 66: 115–118. Alroy, J. 2002. How many named species are valid? Proceedings of the National Academy of Sciences USA 99: 3706–3711. Anderson, D. and J. W. H. Trueman. 2000. Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology 24: 165–189. Beard, D. 1900. Outdoor Games for All Seasons: the American Boy’s Book of Sport. Charles Scribner’s Sons, New York, NY. 496 pp. Bickford, D., D. J. Lohman, N. S. Sodhi, P. K. L. Ng, R. Meier, K. Winkler, K. K. Ingram and I. Das. 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22: 148–155. Caltagirone, L. 1981. Landmark examples in classical biological control. Annual Review of Entomology 26: 213–222. Costello, M. J., S. P. Wilson and B. Houlding. 2013. More taxonomists but a declining catch of species discovered per unit effort. Systematic Biology 62: 616–624. Costello, M. J., B. Houlding and S. Wilson. 2014. As in other taxa, relatively fewer beetles are being described by an increasing number of authors: response to Löbl and Leschen. Systematic Entomology 39: 395–399. Davidson, G. 1964. Anopheles gambiae, a complex of species. Bulletin of the World Health Organization 31: 625–634. Doube, B. M., A. Macqueen, T. J. Ridsill‐Smith and T. A. Weir. 1991. Native and introduced

dung beetles in Australia. Pp. 255–278. In I. Hanski and Y. Cambefort (ed). Dung Beetle Ecology. Princeton University Press, Princeton, NJ. Erwin, T. 1982. Tropical forests: their richness in Coleoptera and other arthropod species. Coleopterists Bulletin 36: 74–75. Erwin, T. 1988. Tropical forest canopies: the heart of biotic diversity. Pp. 123–129. In E. O. Wilson and F. M. Peter (eds). Biodiversity. National Academies Press, Washington. Erwin, T. L. 1991. How many species are there?: Revisited. Conservation Biology 5: 330–333. Gaston, K. J. 1991a. The magnitude of global insect species richness. Conservation Biology 5: 283–296. Gaston, K. J. 1991b. Estimates of the near‐ imponderable: a reply to Erwin. Conservation Biology 5: 564–566. Gaston, K. J. 1991c. Body size and probability of description: the beetle fauna of Britain. Ecological Entomology 16: 505–508. Gentile, G., A. della Torre, B. Maegga, J. R. Powell and A. Caccone. 2002. Genetic differentiation in the African malaria vector, Anopheles gambiae s. s., and the problem of taxonomic status. Genetics 161: 1561–1578. Hanski, I. and Y. Cambefort (eds). 1991. Dung Beetle Ecology. Princeton University Press, Princeton, NJ. 481 pp. Hodkinson, I. D. and D. Casson. 1990. A lesser predilection for bugs: Hemiptera (Insecta) diversity in tropical rain forests. Biological Journal of the Linnaean Society 43: 101–109. Howard, L. O. 1931. The Insect Menace. The Century Company, New York, NY. 347 pp. Hunt, R. H., M. Goetzee and M. Fettene. 1998. The Anopheles gambiae complex: a new species from Ethiopia. Transactions of the Royal Society of Tropical Medicine and Hygiene 92: 231–235. Kellert, S. R. 1993. Values and perceptions of invertebrates. Conservation Biology 7: 845–855. Kirby, W. and W. Spence. 1815. An Introduction to Entomology: or Elements of the Natural History of Insects. Longman, London. 558 pp. Löbl I. and R. A. B. Leschen. 2014. Misinterpreting global species numbers:

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examples from Coleoptera. Systematic Entomology 39: 2–6. Marlatt, C. L. 1898. A brief historical survey of the science of entomology: with an estimate of what has been, and what remains to be, accomplished. Proceedings of the Entomological Society Washington 4: 83–120. May, R. L. 1988. How many species are there in the world? Science 241: 1441–1449. May, R. L. 1990. How many species? Philosophical Transactions of the Royal Society of London B 330: 293–304. Metcalf, Z. P. 1940. How many insects are there in the world? Entomological News 51: 219–222. Metcalf, C. L. and W. Flint. 1939. Destructive and Useful Insects. 2nd edition. McGraw‐Hill, New York, NY. 981 pp. Metcalf, C. L. and W. Flint. 1951. Destructive and Useful Insects. 3rd edition. McGraw‐Hill, New York, NY. 1004 pp. Mikkelson, D. 2013. Red red whine: are the red food colorants cochineal and carmine made from ground bugs? http://www.snopes.com/ food/ingredient/bugjuice.asp [Accessed 8 February 2017]. National Academy of Sciences. 2007. The Status of Pollinators in North America. National Academies Press, Washington. 322 pp. Ødegaard, F., O. H. Diserud, S. Engen and K. Aagaard. 2000. The magnitude of local host specificity for phytophagous insects and its implications for estimates of global species richness. Conservation Biology 14: 1182–1186. Ross, H. H. 1948. A Textbook of Entomology. John Wiley and Sons, New York, NY. 532 pp. Price, P. 1997. Insect Ecology. 3rd edition. John Wiley and Sons, New York, NY. 888 pp. Sabrosky, C. W. 1952. How many insects are there? In A. Stefferud (ed). Insects: the Yearbook of Agriculture. US Department of Agriculture, Washington, DC. Sabrosky, C. W. 1953. How many insects are there? Systematic Zoology 2: 31–36. Smith, M. A, D. M. Wood, D. H. Janzen, W. Hallwachs and P. D. N. Hebert. 2007. DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera,

Tachinidae) are not all generalists. Proceedings of the National Academy of Sciences USA 104: 4967–4972. Smith, M. A., J. J. Rodriguez, J. B. Whitfield, A. R. Deans, D. H. Janzen, W. Hallwachs and P. D. N. Hebert. 2008. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proceedings of the National Academy of Sciences USA 105: 12359–12364. Stork, N. E. 1988. Insect diversity: fact, fiction and speculation. Biological Journal of the Linnean Society 35: 321–337. Stork, N. E. 1993. How many species are there? Biodiversity and Conservation 2: 215–232. Stork, N. E, J. McBroom, C. Gely and A. J. Hamilton. 2015. New approaches, narrow global species estimates for beetles, insects, and terrestrial arthropods. Proceedings of the National Academy of Sciences USA 112: 7519–7523. Swingle, W. T. 1908. The fig in California. Papers and discussions presented before the 34th and 35th Fruit‐Growers’ Convention, California. State Commission on Horticulture, Sacramento, California. Westwood, J. O. 1833. On the probable number of species of insects in the creation; together with descriptions of several minute Hymenoptera. Magazine of Natural History and Journal of Zoology, Botany, Mineralogy, Geology, and Meteorology 6: 116–123. Wilkins, A. 2012. Meet the 20,000 new species we discovered in a single year. http://io9. com/5877595/meet‐the‐20000‐new‐species‐ we‐discovered‐in‐a‐single‐year [Accessed 8 February 2017]. White, G. B. 1974. Anopheles gambiae complex and disease transmission in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 68: 278–295. Young A. M. 1982. Effects of shade cover and availability of midge breeding sites on pollinating midge populations and fruit set in two cocoa farms. Journal of Applied Ecology 19: 47–63.

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Index of Arthropod Taxa Arranged by Order and Family. Non‐insect classes and other supraordinal taxa and informal clades are listed as primary entries coordinate with insect orders. Taxa and informal clades between order and family level are treated as secondary entries coordinate with family within the relevant order (or class). Family‐ group names below family level are treated as tertiary entries coordinate with genus under the appropriate family. Page numbers in bold indicate table entries, and numbers in italic face indicate entries on figures and in figure captions.

a

Arachnida  69, 80 Arachnida–Acari Ixodidae Ixodes scapularis 12 Parasitidae Varroa destructor 788 Varroa jacobsoni 788 Tetranychidae 250 Arachnida–Araneae (= Araneida)  48, 77, 292, 444, 609, 610, 665 Agelenidae Agelena orientalis 304 Pisauridae Dolomedes 209 Arachnida–Scorpiones 608 Archaeognatha. See Microcoryphia

b Blattaria. See Blattodea Blattodea (= Blattaria, = Blattoptera + Isoptera)  51, 77, 80, 121, 147, 148, 154, 184, 208, 212, 579, 581, 646 Blaberidae Panesthia lata 120 Blattellidae Balta similis 648 Blattidae Angustonicus 122

Blatta orientalis 648 Mastotermitidae Mastotermes darwiniensis 120 Rhinotermitidae Amitermes 113 Coptotermes formosanus  659 Nasutitermes 300 Termitoidea  11, 12, 21, 93, 97, 118, 120, 237, 245, 349, 351, 577, 579, 581, 647, 754 Blattoptera. See Blattodea

c

Chilopoda 608 Coleoptera 2, 3, 10, 12, 52, 56, 57, 59, 66–84, 70, 78, 80, 82, 84, 100, 117, 118, 119, 126, 147, 154, 173, 180, 206, 210, 212, 337–395 (chapter 11), 579, 582–583, 605, 606, 607, 609, 646, 650, 785 Acanthocnemidae  340, 353 Acanthocnemus nigricans 353 Ademosynidae (extinct)  358 Adephaga 346–347 Aderidae  342, 355, 387 Agapythidae  341, 354 Agyrtidae  338, 348, 383 Akalyptoischiidae  341, 354 Alexiidae  341, 354 Alleculidae  181, 185, 187 Amphizoidae 146, 338, 347, 383

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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Index

Coleoptera (contd.) Anamorphidae 354 Anobiidae. See Ptinidae Anthicidae  187, 342, 355, 387, 394 Anthicus  187 Formicomus  187 Notoxus  187 Steropes latifrons  187 Anthribidae  153, 157, 176, 183, 187, 342, 356, 387, 394 Anthribus nebulosus 391 Araecerus fasciculatus 357 Onycholips 168 Urodontinae. See Urodontidae Apionidae  173, 182, 183, 187 Fremuthiella vossi  151 Necatapion bruleriei 159 Perapion myochroum  151 Archeocrypticidae  341, 355, 386 Archostemata 344–345 Artematopodidae  339, 385 Macropogon pubescens 156 Asiocoleidae (extinct)  358 Aspidytidae 175, 338, 347 Aspidytes wrasei  175, 178 Attelabidae  122, 183, 342, 356, 387 Caenorhinus marginellus  369 Euops 122 Belidae  342, 356, 387 Belohinidae  338, 350 Berendtimiridae (extinct)  358 Biphyllidae  340, 353, 385 Boganiidae  340, 354 Boridae  342, 355, 387 Bostrichidae  160, 185, 186, 340, 352, 385, 394 Amphicerus cornutus  364 Dinoderus 352 Heterobostrychus aequalis  364 Lyctus 352 Prostephanus 352, 364 Prostephanus truncatus 348 Sinoxylon unidentatum  364 Trogoxylon 352 Bothrideridae  341, 354, 386 Brachyceridae  160, 183, 343, 387 Brachycerus  369 Erirhininae  160, 173, 183

Grypus 161 Lepidonotaris petax 183 Lissorhoptrus oryzophilus  369 Notaris 170 Notaris dauricus 183 Tanysphyrus lemnae 392 Tournotaris 170 Tournotaris bimaculata 391 Brachypsectridae  339, 385 Brentidae  168, 176, 177, 185, 187, 343, 356, 387 Apioninae 357 Amorphocephala coronata 168 Arrhenodes minutus  369 Cylas  369 Eutrichapion viciae 392 Ischnopterapion loti 392 Ischnopterapion virens  369 Bruchidae. See Chrysomelidae–Bruchinae Buprestidae  81, 154, 160, 174, 185, 186, 339, 345, 350, 351, 378, 384, 394, 437, 508, 647 Acmaeoderella  186 Acmaeodera  186 Acmaeoderini 162 Agrilus  186, 363 Agrilus (Xenagrilus) 182 Agrilus planipennis  142, 360, 660, 667 Anthaxia  186 Anthaxia quadripunctata 177 Buprestis rustica 176 Buprestis strigosa 177 Capnodis carbonaria  149 Chrysobothris affinis 177 Chrysobothris femorata  363 Chrysobothris pulchripes 177 Coroebina 180 Cylindromorphus  160, 182, 186 Cyphosoma 160 Cyphosoma euphraticum  149 Dicerca furcata 176 Endelus 161 Eurythyrea aurata 177 Eurythyrea eoa 177 Habroloma 182 Julodella 180 Julodella abeillei  150 Julodis 180

Index

Julodis variolaris  150 Lamprodila amurensis 177 Lamprodila rutilans 177 Melanophila fulvoguttata  363 Microacmaeodera 180 Nipponobuprestis 180 Perotis cuprata 161 Phaenops guttulatus 177 Polyctesis 179 Ptosima 179 Rhaebus  187 Sapaia 180 Sphenoptera 182, 186 Sphenoptera gossypii  363 Sternocera 180 Trachys 182 Byrrhidae  339, 351, 384 Byrrhobolus 171 Byrrhus (Aeneobyrrhus) 170 Byturidae 156, 340, 353, 385 Byturus 353 Callirhipidae  339, 385 Cantharidae  185, 186, 340, 351, 385 Carabidae  50, 76, 80, 81, 83, 173, 184, 185, 186, 338, 343, 345, 346, 383, 390, 394, 646, 656 Anillini 346 Arthropterus wilsoni  344 Brachinini 346 Broscosoma 169 Broscus 168 Callisthenes 180 Calosoma  141, 180 Calosoma sycophanta  149, 347 Carabus  164, 170, 176, 784 Carabus auronitens 163 Carabus lopatini  156 Carabus variolosus 163 Cicindela  169, 663, 784 Craspedonotus tibialis 168 Cychrini 346 Dalyat 346 Harpalini 346 Lebiinae 346 Miquihuana 346 Nebria 170 Paussinae 346

Platyninae 123 Pseudomorphini 346 Rhadine 346 Rhysodinae  338, 346, 383 Rivacindela 583 Scarites 169 Trachypachinae  338, 346, 383 Trechini  169, 346 Trechus 170 Zabrini 346 Zabrus tenebrioides  362 Caridae  342, 356 Catiniidae (extinct)  358 Cavognathidae  341, 354 Cerambycidae  152, 160, 174, 176, 185, 187, 342, 343, 345, 356, 387, 390, 394, 437, 647 Agapanthia 182 Aeolesthes sarta  365 Anoplophora chinensis  366, 660 Anoplophora glabripennis 360, 366, 652, 660, 673 Anthores leuconotus  366 Aphanisticus 160 Apomecyna binubila  366 Apriona  366 Arhopalus ferus  367 Aromia bungii  365 Asias mongolicus  187 Batocera rufomaculata  366 Bixadus sierricola  366 Calamobius 160 Callidiellum  365 Callipogon relictus 178 Chloridolum  365 Cerambyx cerdo  365 Chlorophorus ubsanurensis  187 Chlorophorus obliteratus  187 Cordylomera torrida  365 Dectes texanus  366 Desmiphora hirticollis  366 Dorcadion  152, 160, 180, 182, 356 Enaphalodes rufulus  365 Encyclops caerulea  367 Eodorcadion  160, 180 Eodorcadion kozlovi  187 Euryphagus lundi  365 Hesperophanes campestris  365

795

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Index

Coleoptera: Cerambycidae (contd.) Hylotrupes bajulus  365 Lagocheirus araneiformis  366 Lamia textor 175 Mallosia armeniaca  150 Monochamus  366 Oberea  366 Oberea erythrocephala 161 Oemona hirta  365 Paracylindromorphus 160, 186 Phoracantha  365 Phoracantha recurva 172 Phoracantha semipunctata  172, 664 Phytoecia 182 Placosternus difficilis  365 Plagionotus arcuatus  365 Prionus  367 Psacothea hilaris  367 Saperda  367 Saperda populnea 175 Steirastoma breve  367 Stromatium barbaratum  365 Tetropium  367 Tetropium fuscum 660 Theophilea 160 Trichoferus campestris  365 Xylotrechus  365 Xystrocera globosa  366 Cerophytidae  339, 385 Cerylonidae  341, 354, 386 Chaetosomatidae  340, 353 Chalcodryidae  342 Chelonariidae  339, 384 Chrysomelidae  70, 152, 154, 160, 173, 181, 184, 185, 187, 210, 342, 343, 345, 356, 361, 387, 390 Acalymma vittatum 359, 368 Acanthoscelides obtectus  367 Acanthoscelides pallidipennis 182 Agasicles hygrophila 217 Alocypha bimaculata  368 Alticinae  81, 148, 152, 154, 182, 184 Aphthona  148, 161 Aphthona coerulea  153 Aphthona nonstriata 161 Aphthona sarmatica 166 Aphthona testaceicornis 170

Argopus 176 Atomyria 166 Aulacophora  368 Benedictus 161 Brontispa longissima  367 Bruchidius 182, 187 Bruchinae  159, 184, 187 Bruchus 182, 367 Callosobruchus  367 Calomicrus pinicola 160 Caryedon serratus  367 Caryoborus  187 Cassidini 152 Cerotoma bifurcata  368 Chaetocnema 160, 368 Chlamysini  176, 177 Chrysolina  151, 163, 171, 176, 182 Chrysolina (Pezocrozita) 182 Chrysolina caviger 163 Chrysolina convexicollis 163 Chrysolina jakovlevi 163 Chrysolina sauanica 163 Chrysolina subsulcata 163 Chrysolina tuvensis 163 Chrysolina urjanchaica 163 Chrysomelinae  119, 151, 170 Clavicornaltica 161 Clavicornaltica dali  153 Clytrini  152, 182 Coelaenomenodera elaeidis  367 Crioceris  368 Crosita 171 Cryptocephalinae  151, 160, 170, 184 Cryptocephalini 152 Cryptocephalus  160, 182 Cryptocephalus duplicatus  149 Cryptocephalus ochroloma  153 Cryptocephalus pini 160 Cryptocephalus quadripustulatus 160 Diabrotica  368 Diabrotica virgifera  368, 642, 652 Dicladispa  367 Donacia  166, 210 Donaciinae 160 Epitrix 161, 368 Eumolpinae  152, 170, 184 Exosoma lusitanicum  368

Index

Galeruca rufa 159 Galerucella 668 Galerucinae  151, 170 Gastrophysa 166 Gratiana spadicea 380 Gonioctena fornicata  367 Hippuriphila 161 Hispini  81, 160 Hypocassida 159 Ivalia 161 Jaxartiolus 166 Kiskeya 161 Kiskeya baorucae  153 Kytorhinoides thermopsis 182 Kytorhinus kergoati 182 Kytorhinus pectinicornis 182 Lamprosominae 177 Lema decempunctata 161 Leptinotarsa decemlineata  367, 381, 652 Lilioceris lilii  368 Longitarsus  152, 157, 159, 170, 179 Luperomorpha xanthodera  368 Luperus longicornis 160 Madurasia obscurella  368 Manobia 161 Margarinotus kurbatovi  153 Medythia quaterna  368 Megabruchidius dorsalis  172, 182 Megabruchidius tonkineus  172, 182 Mesoplatys cincta  367 Microtheca ochroloma  367 Mniophila muscorum  153, 161 Odontota dorsalis  367 Ootheca  369 Oreomela  169, 171 Oulema melanopus  368, 657 Paraminota 161 Paraminotella 161 Parnops 166 Paropsidis charybdis 360 Paropsis atomaria 360 Phaedon  166, 218 Phaedon brassicae  367 Phaelota 161 Phyllotreta  369 Promecotheca cumingii  367 Psylliodes  160, 161

Psylliodes valida  170, 171 Pyrrhalta viburni  369 Spermophagus  159, 182, 187 Spermophagus sericeus 182 Trichispa sericea  367 Typophorus nigritus  368 Xenomela 170 Chrysomeloidea  342 Ciidae 167, 342, 355, 386 Clambidae  339, 384 Cleridae 76, 81, 186, 340, 353, 380, 385 Emmepus  186 Necrobia  167, 186 Necrobia rufipes  186 Opetiopalpus sabulosus  186 Thanasimus 353 Cleroidea  394 Cneoglossidae  339 Coccinellidae  173, 187, 341, 345, 355, 386 Chilocorus kuwanae  364 Chnootriba similis  364 Coccinella  187 Coccinella septempunctata 664 Coleomegilla maculata  364 Epilachna  364 Epilachninae 355 Harmonia axyridis  141, 355, 364, 664 Henosepilachna  364 Hyperaspis  187 Pharoscymnus  187 Pharoscymnus auricomus 161 Rodolia cardinalis  11, 14, 250, 603, 669 Sasajiscymnus tsugae  365 Scymnus  187 Stethorus punctatum  365 Tetrybrachys 152 Colymbotethidae (extinct)  358 Coprinisphaeridae (extinct)  358 Coptoclavidae (extinct)  358 Corylophidae  341, 354, 386 Crowsoniellidae  338, 345 Cryptophagidae  157, 187, 341, 354, 386 Cucujidae 186, 341, 354, 386, 394 Cupedidae 175, 338, 345, 383 Rhipsideigma raffrayi  344 Curculionidae  55, 152, 154, 173, 181, 182, 185, 187, 343, 343, 345, 357, 361, 387, 394

797

798

Index

Coleoptera: Curculionidae (contd.) Acalles 177 Alatavia 171 Alcidodes dentipes  372 Alcidodes karelinii  159, 172 Ancipitis punctatissimus  373 Anisandrus  373 Anthonomini 177 Anthonomus 161, 370 Anthonomus grandis 357, 370, 659 Anthonomus (Anthonomidius) 181 Anthypurinus kaszabi  151 Aphelini 168 Apsis albolineatus 160 Arixyleborus  374 Augustinus koreanus 162 Aulacobaris picitarsus  157 Aulacobaris coerulescens  158 Bagoinae 160 Bagous 161 Baridinae  152, 157, 160, 162, 166 Barypeithes pellucidus 656 Blosyrus asellus  370 Bothynoderes punctiventris  371 Brachyderini 168 Brachysomus echinatus 163–164 Caulophilus oryzae  369 Ceutorhynchinae 142, 142, 152, 154, 157, 160, 162, 166, 183 Ceutorhynchus  157, 162, 170 Ceutorhynchus cakilis 168 Ceutorhynchus cochleariae 163 Ceutorhynchus chalibaeus  157 Ceutorhynchus hamiltoni 168 Ceutorhynchus inaffectatus  158 Ceutorhynchus isatidis  158 Ceutorhynchus pervicax 163 Ceutorhynchus potanini 163 Ceutorhynchus sophiae  157 Ceutorhynchus tesquorum 163 Cionus zonovi  151 Cnestus mutilatus  374 Coccotrypes subcribrosus  374 Coeliodes 162 Coniatus zaslavskii  151 Coniatus minutus  151 Cosmobaris scolopacea  151

Cossonus 161 Crossotarsus  372 Cryphalus latus  374 Cryptorhynchus mangiferae  370 Cryptorhynchus lapathi 175 Cryptoxyleborus subnaevus  374 Crypturgus cinereus  374 Curculio  162, 177, 370 Curculioninae 183 Conoderinae 153 Conorhynchus pulverulentus  150, 170 Conotrachelus  372, 374 Copturus aguacatae  369 Cyclominae 153 Cyclorhipidion sexspinatum  374 Dendroctonus frontalis 359 Dendroctonus micans 360 Dendroctonus ponderosae  13, 360, 361 Dendroctonus valens 360 Deracanthus faldermanni  151 Diaprepes  370 Diapus  372 Dichotrachelus 177 Dinoplatypus  372 Dolurgus pumilus  374 Dorytomus  166, 174, 176 Dryocoetes  374 Dryocoetes autographus 391–392 Eccoptopterus spinosus  374 Elytroteinus subtruncatus  370 Entiminae  81, 82, 152, 158, 177, 183 Eremochorus inflatus  151 Eremochorus mongolicus  151 Eremochorus sinuatocollis 163 Eremochorus zaslavskii 163 Euplatypus  373 Euscepes postfasciatus  370 Euwallacea  375 Geniocremnus chilensis  370 Genyocerus  373 Gnathotrichus  375 Gonipterus  370 Gronops semenovi  151 Heilipus lauri  372 Hemitrichapion reflexum 163 Hylastes ater  375 Hylesinus  375

Index

Hylobius 161, 372 Hylurgopinus rufipes  375 Hylurgops  375 Hylurgus ligniperda  375 Hypera postica  371, 659 Hyperinae  152, 153, 170 Hypohypurini 154 Hypolixus truncatulus  371 Hypomeces squamosus  371 Hypothenemus hampei  375 Ips 176, 375 Ips typographus  359, 360 Isonycholips gotoi 168 Larinus planus 668 Lepyrus 170 Limnobaris 160 Lioxyonychini 154 Lissorhoptrus oryzophilus 218 Listroderes  370 Listronotus  370 Lixinae  152, 153, 162, 166, 183 Lixus  157, 161 Lixus juncii  371 Lixus incanescens  151 Macrotarrhus kiritshenkoi  151 Magdalini 177 Magdalis 174 Mecysmoderes  157, 176 Mecysolobini 176 Megaplatypus mutatus  373 Melanobaris 157 Melanobaris atramentaria  157 Melanobaris hochhuthi  157 Melanobaris nigritarsis  157, 158 Melanobaris gloriae  158 Mesoptiliinae 183 Metamasius callizona 664 Mitrastethus baridioides  370 Monarthrum  376 Mongolocleonus gobianus  151 Mononychini 160 Mononychus punctumalbum 161 Nastus 161 Naupactus  371 Neochetina bruchi 217 Neochetina eichhorniae 217 Neophytobius 170

Neoplatygaster venustus 162 Oprohinus  160, 161 Orchestes alni 172, 370 Orchestes mutabilis 172 Orobitis 155 Orthotomicus  376 Otibazo 168 Otidocephalinae 79, 81, 82 Otiorhynchus  158–159, 161, 166, 169, 177, 371 Otiorhynchus aurifer 172 Otiorhynchus ovalipennis 172 Oxoplatypus quadridentatus  373 Oxyonychini  159, 161 Oxyonyx kaszabi  151 Ozopemon 381 Pagiocerus frontalis  376 Pantomorus cervinus  371 Parorobitis 155 Parorobitis gibbus  156 Philernus gracilitarsis  151 Philopedon plagiatus 168 Phloeosinus  376 Phloeotribus  376 Phlyctinus callosus  371 Phyllobius thalassinus 163 Piazomias  150 Pissodes  372 Pissodini 177 Pityoborus comatus  376 Pityogenes 176, 376 Pityophthorus juglandis  376 Platygasteronyx humeridens  151 Platypodinae  357, 359 Platypus  373 Plinthini 177 Plinthus 177 Polydrusus corruscus 391 Polydrusus impressifrons 391 Polygraphus 176, 376 Premnotrypes  371 Prisistus 160 Pseudips concinnus  376 Pseudocneorhinus bifasciatus  371 Pseudohylesinus granulatus  376 Pseudopityophthorus  376 Pseudorchestes  151, 152

799

800

Index

Coleoptera: Curculionidae (contd.) Pseudorchestes convexus 180 Pseudorchestes furcipubens  151 Pseudostyphlus leontopodi 170 Pseudorchestes tschernovi 180 Ptochus daghestanicus 164 Ptochus porcellus 164 Rhamphini  152, 162, 177 Rhamphus choseniae 175 Rhinocyllus conicus 668 Rhythirrinini 153 Scleropterus 170 Scolytinae  21, 160, 174, 357, 359, 647 Scolytus 183, 376 Scolytus multistriatus 660 Scolytus schevyrewi 660 Sibinia sp. pr. beckeri  151 Sitona 170, 371 Sitonini 152 Stephanocleonus  170, 180 Stephanocleonus excisus  151 Stephanocleonus inopinatus  151 Stephanocleonus paradoxus  151 Stephanocleonus persimilis  151 Stephanocleonus potanini  151 Sternochetus  370 Sthereus ptinoides 168 Tanymecini 168 Tanymecus dilaticollis  371 Thamnurgus caucasicus 183 Thamnurgus pegani 187 Thamnurgus russicus 183 Tomicus  377 Tomicus piniperda 359 Trachyphloeus 158 Treptoplatypus solidus  373 Trichosirocalus barnevillei 163 Truncaudum agnatum  377 Trypodendron domesticum  377 Tychius  153, 159 Tymbopiptus valeas 124 Xyleborus  377 Xyleborus glabratus 660 Xylosandrus  377 Xyloterinus politus  377 Xyloterus lineatus  377 Curculionoidea 356–357

Cybocephalidae  186, 354 Cyclaxyridae  341, 354 Dascillidae  339, 384 Dacillus elongatus 156 Dascillus cervinus 156 Dascilloidea 352 Dasytidae. See Melyridae–Dasytinae Decliniidae  339 Declinia relicta 178 Dermestidae  186, 187, 340, 352, 380, 385 Anthrenus  186, 359, 646 Attagenus  186 Attagenus smirnovi 168 Dermestes  167, 186, 359 Dermestes lardarius 379 Eremoxenus chan 168 Orphilus 352 Thorictus 168 Trogoderma granarium  364, 646 Thaumaglossa 352 Thylodias 359 Thylodrias contractus 187 Derodontidae  340, 351, 385 Laricobius 351 Diphyllostomatidae 49, 339, 350, 384, 390 Discolomatidae  341, 354 Disteniidae  342, 356 Drilidae. See Elateridae–Drilini Dryophthoridae  153, 160, 176, 182, 343, 387 Cosmopolites sordidus  369 Diocalandra  369 Metamasius  369 Odoiporus longicollis  369 Rhabdoscelus obscurus  369 Rhinostomus barbirostris  369 Rhynchophorus  369 Scyphophorus acupunctatus  369 Sphenophorus venatus  369 Temnoshoita nigroplagiata  369 Tryphetus incarnatus  373 Dryopidae  186, 210, 339, 384 Dytiscidae  119, 173, 186, 338, 347, 383, 394 Colymbetinae 381 Hydroporinae 347 Elateridae  81, 173, 186, 339, 345, 351, 378, 385, 390, 394 Aeoloides  186

Index

Aeloderma  186 Agriotes  186, 364 Ampedus nigrinus 391 Berninelsonius hyperboreus 392 Cardiophorus  186 Conoderus rufangulus  364 Drasterius  186 Drilini  340, 351 Limonius californicus  364 Melanotus communis  364 Zorochrus  186 Elmidae 210, 339, 351, 384, 394 Elodophthalmidae (extinct)  358 Endecatomidae  340, 352, 385 Endomychidae 167, 341, 354, 386 Erirhinidae. See Brachyceridae–Erirhininae Erotylidae  81, 82, 167, 340, 354, 385, 394 Eucinetidae  339, 384 Eucnemidae  339, 385, 394 Eulichadidae  339, 384 Eupsilobiidae 354 Euxestidae 354 Georyssidae  186 Geotrupidae 12, 338, 350, 361, 383, 383 Geotrupes inermis 171 Glaphyridae  339, 350, 384 Amphicoma 181 Glaphyrus 181 Glaresidae  339, 350, 384 Gyrinidae  186, 338, 347, 380, 383 Haliplidae  186, 338, 383 Helodidae  157, 186 Helophoridae  186 Helophorus lapponicus 148 Helotidae 175, 340, 354 Heteroceridae  186, 339, 384 Histeridae  167, 168, 186, 338, 348, 380, 383, 383–390 Chlamydopsinae 348 Hetaeriinae 348 Teretrius nigrescens 348 Hobartiidae  341, 354 Hybosoridae  339, 350, 384 Ceratocanthinae  81, 82 Hydraenidae  186, 210, 338, 348, 383 Ochthebius figueroi 148 Hydrobiidae

Hydrobius fuscipes 380 Hydrophilidae 167, 186, 338, 347, 348, 383 Acidocerinae 348 Cercyon 168 Epimetopinae 348 Helophorinae 348 Hydrochinae 348 Hydrophilus 141 Spercheinae 348 Sphaeridiinae 348 Hydrophiloidea 347–348 Hydroscaphidae 57, 338, 346, 383 Hygrobiidae  338, 347 Inopeplidae 175 Ischaliidae 175 Jacobsoniidae  340, 348, 351, 385 Jurodidae (including Sikhotealiniidae)  338, 345 Sikhotealinia zhiltzovae (extinct) 177 Kateretidae  341, 354, 386 Brachypterus urticae 392 Labradorocoleidae (extinct)  358 Laemophloeidae  386 Cryptolestes 354 Laemophloeidae (including Propalticidae)  341, 354 Cryptolestes  364 Lamingtoniidae  341, 354 Lampyridae 177, 340, 351, 381, 385 Photuris 15 Lasiosynidae (extinct)  358 Latridiidae 157, 341, 354, 386 Leiodidae  167, 185, 186, 338, 349, 383, 394 Agathidium laevigatum 167 Catopinae 167 Leptodirus 349 Platypsyllus castor 349 Ptomaphagus hirtus  344 Speonomus 349 Lepiceridae  338, 346 Lepicerus inaequalis  344 Liadytidae (extinct)  358 Limnichidae  339, 384 Lucanidae  339, 350, 384, 394 Lutrochidae  339, 384 Lycidae  340, 385 Dictyoptera aurora 391

801

802

Index

Coleoptera: Lycidae (contd.) Lymexylidae  340, 352–353, 385 Melittomma insulare  364 Promelittomma insulare 353 Malachiidae. See Melyridae–Malachiinae Magnocoleidae (extinct)  358 Mauroniscidae  340, 353 Megalopodidae  342, 356, 387 Megalopodinae  176, 177 Melandryidae  342, 355, 376 Meloidae  187, 342, 355, 357–359, 378, 387 Lytta vesicatoria 379 Melyridae  340, 345, 353, 385 Anthocomus equestris 392 Dasytinae  181, 186, 353 Malachiinae  181, 353 Rhadalinae 353 Meruidae  338, 347 Mesocinetidae (extinct)  358 Metaxinidae  340, 353 Metaxina ornata 353 Micromalthidae  338, 345, 383 Micromalthus debilis  346, 381, 507 Monommidae. See Zopheridae–Monomminae Monotomidae  341, 354, 385 Rhizophagus 354 Mordellidae 80–82, 81, 82, 83, 187, 342, 355, 386 Conaliini  82, 83 Glypostenoda  82 Mordella  82 Mordellini  82, 83 Mordellistena  82, 187 Mordellistenini 82 Pentaria  187 Murmidiidae 354 Mycetaeidae 354 Mycetophagidae  341, 355, 386, 394 Mycteridae  342, 355, 387 Hemipeplus 355 Mycterus curculionoides 157 Myraboliidae  341, 354 Myxophaga 345–346 Nanophyidae 182 Corimalia reaumuriae  151 Nemonychidae 182, 342, 356, 387 Cimberis attelaboides  156

Nitidulidae  167, 185, 186, 341, 354, 386 Aethina tumida 354, 364, 659 Carpophilus obsoletus  364 Cyllodes ater 167 Epuraea  167, 177 Meligethes 177 Meligethes aeneus  364 Pocadius 167 Stelidota geminata  364 Nosodendridae  340, 351, 385 Noteridae  338, 347, 383 Copelatinae 347 Phreatodytes 347 Oborocoleidae (extinct)  358 Obrieniidae (extinct)  358 Ochodaeidae  339, 350, 384 Oedemeridae  185, 187, 342, 355, 378, 387 Homomorpha cruciata  187 Nacerdes melanura 355 Omalisidae  340, 351 Telegeusinae  340, 351, 385 Omethidae  340, 385 Ommatidae  338, 345 Orsodacnidae  342, 356, 387 Othniidae 175 Oxypeltidae  342, 356 Pallichnidae (extinct)  358 Parahygrobiidae (extinct)  358 Parandrexidae (extinct)  358 Passalidae  338, 350, 383 Passandridae  341, 354, 386 Permocupedidae (extinct)  358 Permosynidae (extinct)  358 Phalacridae 186, 341, 354, 386 Olibrus 354 Phengodidae  340, 385 Phloeostichidae  341, 354 Phloiophilidae  340, 353 Phloiophilus edwardsii 353 Phycosecidae  340, 353 Phycosecis 353 Pilipalpidae 175 Plastoceridae  339 Platypodidae 177 Pleocomidae 49, 338, 349, 383, 390 Podabrocephalidae  339 Polyphaga  342, 347–357

Index

Praelateriidae (extinct)  358 Priasilphidae  341, 354 Prionoceridae  340, 353 Promecheilidae  342, 355 Propalticidae. See Laemophloeidae Prostomidae  342, 355, 387 Protocoleoptera (extinct)  358 Protocucujidae  340, 354 Pselaphidae. See Staphylinidae–Pselaphinae Psephenidae 210, 339, 384 Pterogeniidae  342, 355 Ptiliidae  338, 349, 383 Ptiliolum 393 Scydosella musawasensis 349 Ptilodactylidae  339, 384 Ptinidae  160, 174, 186, 340, 352, 385, 394 Anobium punctatum 352 Dorcatominae 167 Lasioderma 168 Lasioderma serricorne 352 Theca  186, 352 Xyletinus  186 Pyrochroidae  342, 355, 387 Pythidae  342, 355, 387 Rhadalidae. See Melyridae–Radalinae Rhagophthalmidae  340 Rhinorhipidae  339 Rhipiceridae  339, 351, 384 Rhipiphoridae. See Ripiphoridae Rhombocoleidae (extinct)  358 Rhynchitidae 183 Rhysodidae. See Carabidae–Rhysodinae Ripiphoridae 187, 342, 355, 383, 386 Macrosiagon  187 Salpingidae  342, 355, 387 Aegialites stejnegeri 169 Scarabaeidae  12, 49, 50, 81, 99, 104, 120, 185, 186, 244, 339, 343, 345, 350, 361, 378, 384, 394, 663 Adoretus  363 Amphimallon  363 Anoplognathus chloropyrus 360 Aphodius  167, 181, 186 Aphodius fimetarius 392 Aphodius holdereri 148 Anomala sulcata  363 Canthonini  104, 105

Cheirolasia burkei  362 Chiloloba acuta  362 Chioneosoma 164 Coprini 104 Copris 167 Costelytra zealandica  363 Cotinus mutabilis 380 Dichotomiini  104, 105 Diloboderus abderus  362 Drepanocerina 105 Eucraniini 104 Eurysternini 104 Exomala orientalis  363 Golofa eacus  362 Gymnopleurini 104 Helictopleurina 105 Heteronychus arator  362 Holotrichia  363 Hoplia praticola 163 Leucopholis  363 Maladera castanea  363 Melolontha  363 Oniticellina 104 Onitini 104 Onthophagini 104 Onthophagus  167, 181, 186 Oryctes  362 Pachnoda  362 Pachnoda marginata 380 Papuana  362 Pentadon 141 Phanaeini 104 Phyllophaga  363, 390 Planolinoides borealis 48 Platycoelia lutescens 378 Podischnus agenor  362 Popillia  363 Protaetia  362 Rhyssemus germanus 392 Scarabaeinae  105, 789 Scarabaeini 104 Scarabaeus 167 Scarabaeus sacer 23 Scarabaeus zambesianus 380 Serica 390 Sisyphini 104 Sisyphus 167

803

804

Index

Coleoptera: Scarabaeidae (contd.) Smaragdesthes africana  362 Tomarus gibbosus 50 Xylotrupes gideon  362 Scarabaeoidea  97, 181 Schizocoleidae (extinct)  358 Schizophoridae (extinct)  358 Schizopodidae  343, 384 Scirtidae  339, 384, 390 Cyphon 393 Scraptiidae  187, 342, 355, 387, 390 Anaspis 393 Scraptia straminea  187 Scydmaenidae. See Staphylinidae–Scydmaeninae Sikhotealiniidae. See Jurodidae Silphidae  167, 185, 338, 349, 380, 383, 383, 394 Lyrosoma 168 Necrophorus argutor 185 Nicrophorus 349 Nicrophorus americanus 53 Thanatophilus 167 Silvanidae 186, 341, 354, 386 Ahasverus 354 Airaphilus  186 Cathartus 354 Nausibius 354 Oryzaephilus 354 Sinisilvanidae (extinct)  358 Smicripidae  341, 354, 386 Sphaeritidae 146, 338, 348, 383 Sphaeriusidae  338, 346, 383 Sphindidae  340, 354, 385 Staphylinidae  50, 55, 157, 168, 173, 176, 181, 185, 186, 338, 343, 345, 349, 380, 383, 516, 646 Aleochara 349 Aleocharinae  157, 349 Himalusa 349 Paederidus 378 Paederus 378 Pselaphinae  120, 185, 186, 349 Scydmaeninae 348 Stenus  157, 380 Staphylinoidea 348–349 Stenotrachelidae  342, 355, 387

Synchroidae  342, 355, 387 Synteliidae  175, 178, 338, 348 Taldycupedidae (extinct)  358 Tasmosalpingidae  341, 354 Telegeusidae. See Omalisidae–Telegeusinae Tenebrionidae  164, 173, 184, 185, 187, 342, 345, 355–356, 386, 394, 506 Alphitobius diaperinus  165, 359 Alphitophagus bifasciatus  165 Ammobius rufus  165 Anatolica 181 Anatolica amoenula  185 Anatolica cechiniae  185 Anatolica mucronata  185 Anatolica polita borealis  185 Anatolica sternalis gobiensis  185 Anemia dentipes  185 Asida lutosa  165 Blaps 181 Blaps femoralis medusula  185 Blaps halophila  165 Blaps kashgarensis gobiensis  185 Blaps kiritshenkoi  185 Blaps miliaria  185 Bolitophagus reticulatus 167 Catomus mongolicus  185 Centorus tibialis  165 Cossyphus tauricus  165 Crypticus quisquilius  165 Cyphogenia intermedia  185 Cyphosthete mongolica  185 Dendarus punctatus  165 Diaclina testudinea  165 Dilamus mongolicus  185 Epitrichia intermedia  185 Eumilada punctifera amaroides  185 Gonocephalum granulatum  165 Laena starcki  165 Leichenum pictum  165 Melanimon tibialis  165 Melanesthes 181 Melanesthes czikii  185 Melanesthes heydeni  185 Microdera kraatzi  185 Monatrum prescotti  185 Nalassus 164 Nalassus faldermanni  165

Index

Nesotes 381 Oodescelis polita  165 Opatrum sabulosum  165, 181 Pedinus  164, 181 Pedinus femoralis  165 Penthicus 181 Penthicus lenczyi  185 Phaleria pontica  165 Phaleriini 168 Phtora reitteri  165 Pimelia subglobosa  165 Platyope mongolica  185 Prosodes 164 Psammoestes dilatatus  185 Pterocoma reitteri  185 Scaphidema metallicum  165 Scythis 181 Stenosis punctiventris  165 Sternoplax mongolica  185 Strongyliini  82 Tenebrio obscurus  165 Tentyria nomas  165 Trachyscelis aphodioides  165 Trachelostenini  342, 355 Tribolium castaneum  20, 356, 359, 381 Tribolium confusum 20 Trigonoscelis schrencki  150 Trigonoscelis sublaevigata granicollis  185 Ulomoides dermestoides 379 Upis ceramboides 355 Teredidae 354 Tetratomidae  342, 355, 386 Thanerocleridae  340, 353 Throscidae  339, 385, 390 Trixagus 393 Torridincolidae  338, 345 Trachelostenidae. See Tenebrionidae–Trachelostenini Trachypachidae. See Carabidae–Tracypachinae Triadocupedidae (extinct)  358 Triaplidae (extinct)  358 Tricoleidae (extinct)  358 Trictenotomidae 175, 342, 355 Tritarsusidae (extinct)  358 Trogidae 167, 338, 350, 384 Trogossitidae 156, 340, 353, 385, 394 Ostoma ferrugineum 156

Peltis 156 Tenebrioides mauritanicus 156 Thymalus 156 Tshekardocoleidae (extinct)  358 Ulodidae 124, 342, 355 Ulyanidae (extinct)  358 Urodontidae  162, 183 Bruchela 157, 187 Bruchela albosuturata  158 Bruchela anatolica  157 Bruchela concolor  158 Bruchela exigua  158, 183 Bruchela fortirostris  158 Bruchela hesperidis  158 Bruchela kasparyani  158 Bruchela kaszabi 183 Bruchela medvedevi  158 Bruchela muscula  157 Bruchela orientalis  157, 183 Bruchela parvula  157 Bruchela rufipes  157 Bruchela schusteri  157 Bruchela sugonyaevi  158 Bruchela suturalis  157 Bruchela verae  158 Vesperidae  342, 356 Philus antennatus 356 Zopheridae 176, 342, 355, 386 Monomminae 175 Collembola  3, 10, 69, 558, 578, 579

d

Dermaptera  3, 51, 55, 147, 148, 154, 184, 206, 208, 578, 579 Anisolabididae Anisolabis maritima 208 “Dictyoptera” (see also Blattodea, Mantodea, Phasmatodea)  609 Diplopoda  346, 608 Diplura  3, 558, 578, 579 Diptera 2, 3, 52, 55, 57, 69, 78, 79, 80, 97, 103, 117, 122, 126, 146, 154, 173, 179, 206, 211, 229–257 (chapter 9), 579, 584, 605, 606, 607, 609, 646, 650, 713–734 (chapter 22) Acartophthalmidae  233 Acroceridae 229, 231, 242 Acrolophidae. See Tineidae–Acrolophinae

805

806

Index

Diptera (contd.) Agromyzidae  233, 244, 246, 611 Liriomyza brassicae 246 Liriomyza huidobrensis 246 Liriomyza trifolii 246 Liriomyza sativae 246 Anisopodidae  230 Anthomyiidae  234, 245, 249 Chiastocheta 252 Anthomyzidae  233 Apioceridae 155, 231 Apsilocephalidae  231 Apystomyiidae  231 “Aschiza” 242–243 Asilidae  231, 234, 242 Proctacanthus  235 Asteiidae  233 Atelestidae  231 Athericidae  213, 231, 241, 715, 718, 720–721 Atherix  238 Atrichops  716, 721 Dasyomma  716, 721 Suragina  716, 721 Suraginella  716, 721 Aulacigastridae  233 Australimyzidae  233 Austroconopidae. See Ceratopogonidae–Austroconops Austroleptidae  231 Axymyiidae  213, 229, 230, 240 Axymyia  235, 236 Bibionidae  230, 240 Bibio  235 Blephariceridae  119, 128, 213, 230, 234, 240, 241, 255 Agathon  238 Blepharicera  238 Horaia  236 Bolbomyiidae  231 Bolitophilidae  230 Bombyliidae  231, 234, 242, 246–247 Heterostylum robustum 247 Brachycera  231, 234, 241–245 Brachystomatidae  231 Braulidae  234 Calliphoridae 234, 234, 245, 248, 584 Bellardia  238

Calliphora 252 Chrysomya 252 Chrysomya bezziana 249 Chrysomya rufifacies 656 Cochliomyia hominivorax  249, 657 Hemipyrellia  235 Lucilia  236 Lucilia cuprina 249, 659, 660 Mesembrinellinae  229, 237 Onesia  238 Pollenia 239 Protocalliphora 713 Calyptratae 245 Camillidae 155, 234 Canacidae  213, 233, 255 Canthyloscelidae 155, 230 Hyperoscelis 155 Carnidae  233 Carnus  716 Cecidomyiidae  120, 154, 230, 241, 246, 251 Aphidoletes aphidimyza 250 Feltiella acarisuga 250 Mayetiola destructor  644, 648, 657, 659, 713 Celyphidae  232 Ceratopogonidae 154, 212, 229, 230, 240, 241, 252, 714, 715, 718, 720, 721, 727, 733 Austroconops 120, 716, 721 Culicoides 250, 716, 717, 721, 733 Culicoides imicola [complex]  730 Culicoides variipennis  728, 729 Culicoiodes sonorensis 729 Forcipomyia  252, 253, 788 Forcipomyia (Lasiohelea)  716, 721 Leptoconops  716, 721 Chamaemyiidae  232, 244, 251 Leucopis tapiae 251 Chaoboridae  212, 229, 230, 239, 240, 250 Chaoborus edulis 250 Chironomidae  19, 57, 119, 126, 155, 173, 210, 212, 229, 230, 239, 240, 241, 250, 255, 716 Chironomus 255 Cladotanytarsus lewisi 250 Goeldichironomus amazonicus 653 Polypedilum nubifer 653 Sergentia koschowi 240 Zelandochlus 121 Chloropidae 229, 233, 244, 245, 250

Index

Batrachomyia 245 Chlorops pumilionis 245 Hippelates 250 Meromyza americana 245 Oscinella frit 245 Thaumatomyia glabra 245 Thaumatomyia notata  239, 249 Chyromyidae  233 Clusiidae  233, 244 Coelopidae  213, 232 Conopidae  232, 244 Stylogaster  235 Stylogastrinae 244 Corethrellidae  212, 230, 715, 718, 721, 727 Cryptochetidae (= Cryptochaetidae)  155, 234, 603 Cryptochetum iceryae  250–251, 603, 606 Ctenostylidae  232 Culicidae  22, 55, 154, 166, 212, 218, 229, 230, 240, 255, 299, 584, 646, 714, 715, 718, 720, 721–722, 727 Aedes  13, 247 Aedes aegypti  660, 662, 713, 726 Aedes albopictus  662, 733 Aedes campestris 19 Aedes seriatus 662 Aedes taeniorhynchus 19 Anopheles  13, 247, 537, 575 Anopheles coluzzii 732 Anopheles crucians 717 Anopheles filipinae 729 Anopheles gambiae  575, 662, 717, 730, 732, 788 Anopheles punctulatus 717 Anopheles quadrimaculatus complex  726, 730 Anopheles varuna 729 Coquillettidia 240 Culex  235, 247 Culex molestus 732 Culex pipiens 732 Culex quinquefasciatus 660 Mansonia 240 Malaya  716 Ochlerotatus japonicus 662 Toxorhynchites  716 Culicoidea  230

Curtonotidae  234 Cuterebridae. See Oestridae–Cuterebrinae Cylindrotomidae  230 Cypselosomatidae  232 Deuterophlebiidae  213, 230, 234, 240, 255 Deuterophlebia  236 Diadocidiidae  230 Diastatidae  234 Diopsidae  232, 244 Teleopsis  235 Ditomyiidae  230 Dixidae  212, 230, 240 Dolichopodidae 122, 213, 231, 242, 255 Campsicnemus 256 Emperoptera 256 Drosophilidae  234, 244 Drosophila  16–18, 23, 253–254, 256, 555 Drosophila melanogaster  16–17, 20, 244, 506, 657 Drosophila subobscura 657 Dryomyzidae  213, 232 Oedoparena glauca 237–238 Empididae 119, 213, 231, 234, 239, 242 Empidinae 242 Empis  235 Empidoidea 242 Iteaphila group  231 Ephydridae  213, 229, 234, 244, 245, 255 Scatella stagnalis 246 Eurygnathomyiidae 148 Evocoidae  231 Fanniidae  234, 245, 253 Fergusoninidae 120, 233 Fergusonina turneri 237 Gasterophilidae. See Oestridae–Gasterophilinae Glossinidae  154, 234, 234, 245, 718, 722–723, 727 Glossina  13–14, 728 Gobryidae  232 Heleomyzidae  213, 232, 233 Helosciomyzidae  232 Hesperinidae  230 Heterocheilidae  213, 233 Heteromyzidae  233 Hilarimorphidae  231 Hippoboscidae 154, 234, 245, 715, 716, 718, 720, 723

807

808

Index

Diptera: Hippoboscidae (contd.) Melophagus ovinus 723 Nycteribiinae 245 Streblinae 245 Hippoboscoidea  229, 237 Homalocnemidae  231 Huttoninidae  233 Hybotidae  231 Inbiomyiidae  233 Ironomyiidae  232 Ironomyia 243 Keroplatidae  230, 239 Arachnocampa 239 Arachnocampa luminosa  113, 239 Keroplatus 239 Orfelia fultoni 239 Lauxaniidae  232, 244 Limoniidae  230 Lipsothrix 240 Prionolabis  235 Lonchaeidae  232 Lonchopteridae  213, 232, 243 Lonchoptera bifurcata 243 Lygistorrhinidae  230 Marginidae  233 Megamerinidae 155, 233 Mesembrinellidae. See Calliphoridae–Mesembrinellinae Micropezidae  232, 234 Grallipeza  235 Milichiidae  233 Mormotomyiidae  233 Mormotomyia hirsuta 256 Muscidae  213, 229, 234, 245, 253, 715, 719, 723 Coenosia 251 Haematobia exigua 248 Haematobia irritans  248, 660, 723 Hydrotaea irritans 248 Musca autumnalis  248, 714 Musca crassirostris  716, 723 Musca domestica  16, 250, 348, 646, 648, 714 Musca sorbens 248 Musca vetustissima  112, 249, 789 Philornis downsi  4, 249, 660 Spilogona 57 Stomoxyinae  646, 716

Stomoxys calcitrans  648, 660, 723 Mycetophilidae  79, 154, 230, 241 Mydidae  231 Rhaphiomidas terminatus abdominalis 256 Mystacinobiidae  234 Nannodastiidae  233 Natalimyzidae  233 “Nematocera” 239–241 Nemestrinidae  231, 234, 242 Moegistorhynchus longirostris 242 Neminidae  233 Neriidae  232 Neurochaetidae  233 Nothybidae  232 Nymphomyiidae  213, 230, 237 Nymphomyia  236, 238 Odiniidae  233 Oestridae  154, 229, 234, 234, 245, 248 Cobboldia russanovi 256 Cuterebrinae  245, 248 Dermatobia hominis  237, 248 Gasterophilinae  245, 248 Gasterophilus 237 Gasterophilus intestinalis 19 Gedoelstia 249 Gyrostigma rhinocerontis 256 Gyrostigma sumatrensis 256 Hypoderma  237, 249 Hypoderma bovis 248 Hypodermatinae 245 Oestrinae 245 Oestrus ovis 249 Opetiidae  232 Opomyzidae  233 Oreogetonidae  231 Oreoleptidae  213, 231 “Orthorrhapha” 241–242 Pachyneuridae  230 Pallopteridae  233 Pantophthalmidae  231, 241 Pediciidae  230 Pelecorhynchidae  213, 231, 234 Periscelididae  233 Perissommatidae  230 Phaeomyiidae 148, 233 Phoridae  213, 232, 237, 243, 246, 249, 251, 253, 606, 607, 608, 610

Index

Apocephalus  605, 608 Megaselia  243, 608 Megaselia scalaris 247 Melaloncha  247, 608 Myriophora 608 Pseudacteon 608 Pseudohypocera kerteszi 247 Termitophilomya  238 Termitoxeniinae 237 Thaumatoxena  238 Piophilidae  232, 244, 253 Piophila casei  244, 252 Protopiophila litigata 244 Thyreophora cynophila 256 Thyreophorini 229 Pipunculidae 229, 232, 235, 243, 251 Nephrocerus 243 Platypezidae  232, 242 Microsania 242 Platystomatidae  232 Psilidae  232, 244, 249 Chamaepsila hennigi 244 Psila rosae 244 Psychodidae 154, 213, 218, 229, 230, 240, 249, 299, 584, 715, 719, 724 Lutzomyia 724 Lutzomyia longipalpis 728 Pericoma  236 Phlebotominae 247, 716, 724 Phlebotomus 724 Phlebotomus perniciosus 728 Psychoda 255 Psychoda phalaenoides 246 Sycoracinae  716, 724 Ptychopteridae  213, 230 Bittacomorpha  238 Pyrgotidae  232, 244 Rangomaramidae  231 Rhagionidae  231, 241, 715, 719, 720, 724 Spaniopsis  716, 724 Symphoromyia  716, 724 Rhiniidae  234, 245 Rhinophoridae  234, 245 Rhopalomeridae  233 Richardiidae  232, 244 Risidae 148

Sarcophagidae  170, 229, 234, 237, 245, 248, 253, 584, 606 Blaesoxipha 606 Metopia  238 Microcerella bermuda 256 Miltogramminae  229, 245 Sarcophaga  235 Sarcophaga aldrichi 250 Senotainia tricuspis 247 Wohlfahrtia 249 Scathophagidae 234, 234, 245 Scathophaga  235 Scatopsidae  213, 230, 240 Scenopinidae  231 Schizophora  232, 233, 234 Sciaridae  231, 241, 246, 252 Bradysia coprophila 246 Bradysia impatiens 246 Sciomyzidae  213, 233, 244, 251 Tetanocera  236 Sepsidae  233, 252 Simuliidae  18, 154, 155, 212, 218, 230, 234, 240, 247, 584, 714, 715, 719, 720, 724– 725, 733 Austrosimulium 113 Simulium arcticum 731 Simulium damnosum  717, 726, 730, 731, 732 Simulium metallicum 717 Simulium ochraceum 726 Simulium sirbanum 732 Simulium vampirum 731 Simulium (Wilhelmia) 537 Somatiidae  232 Sphaeroceridae 229, 233, 244–245 Stratiomyidae  213, 231, 235, 241, 253 Caloparyphus  236 Hermetia illucens 252 Syringogastridae  232 Syrphidae 170, 213, 229, 232, 243, 255 Episyrphus balteatus 243 Eristalis 255 Eristalis tenax  149 Ornidia obesa 252 Syrphus  236 Tabanidae  154, 170, 213, 229, 231, 234, 241, 247, 584, 714, 715, 719, 720, 725

809

810

Index

Diptera: Tabanidae (contd.) Chrysops  23, 725 Fidena 242 Goniops  716, 725 Mycteromyiini  716, 725 Pangoniinae 241–242 Philoliche 242 Scepsidinae  716, 725 Stonemyia  716, 725 Stonemyia velutina 256 Tabanus conterminus 729 Tabanus nigrovittatus 729 Tabanomorpha  231, 241–242 Tachinidae  148, 170, 229, 234, 237, 245, 251, 437, 584, 606, 607, 610, 612, 786 Belvosia 614 Bessa remota 251 Billaea claripalpis 251 Blepharipa scutellata 610 Compsilura concinnata  251, 466, 608, 668 Cyzenis albicans 251 Lixophaga diatraeae 251 Lydella minense 251 Phasiinae 614 Stackelbergomyiinae 148 Tachiniscidae  232 Tanyderidae  213, 230 Araucoderus  235 Tanypezidae  232 Tephritidae  97, 229, 232, 244, 246, 251, 646, 647 Anastrepha 246 Bactrocera 246 Bactrocera cucurbitae  100, 101, 659 Bactrocera dorsalis  100, 101 Bactrocera invadens  100, 101 Bactrocera latifrons  100, 102 Bactrocera oleae 102–103 Bactrocera orientalis 244 Bactrocera papayae  659 Bactrocera zonata  100, 101 Ceratitis 246 Ceratitis capitata  100, 102, 244, 659 Ceratitis cosyra 102 Ceratitis fasciventris 102 Ceratitis rosa 102

Dacus 246 Dacus bivittatus 102 Dacus ciliatus 102 Dacus frontalis 102 Dacus vertebratus 102 Eurosta  236 Paracantha culta 668 Phytalmia 122 Rhagoletis 246 Trirhithrum coffeae 103 Trirhithrum nigerrimum 103 Urophora 669 Teratomyzidae  233 Thaumaleidae 119, 212, 230, 234, 241 Therevidae  231, 255 Tipulidae  173, 179, 229, 230, 240 Epiphragma  236 Tipuloidea  213, 230, 241 Trichoceridae  230 Ulidiidae  232 Valeseguyidae  230 Vermeleonidae  231 Vermileonidae  229, 239 Xenasteiidae 155, 233 Xylomyidae  231, 241 Xylophagidae  231 Xylophagomorpha  231

e Embiidina. See Embiodea Embioptera. See Embiodea Embiodea( = Embiidina, = Embioptera)  51, 118, 147, 292, 579, 581, 654 Ephemeroptera  3, 10, 51, 69, 93, 147, 155, 173, 206, 212, 516, 579, 580 Ameletopsidae 119 Leptophlebiidae 119 Nesameletidae 119 Oniscigastridae 119 Rallidentidae 119 Siphlaenigmatidae 121 Teloganodidae 119

g

Grylloblattodea (= Notoptera– Grylloblattodea)  3, 51, 57, 95, 118, 147, 579, 581

Index

h

Hemiptera  3, 11, 51, 69, 117, 119, 122, 147, 208, 279–313 (chapter 10), 579, 582, 646, 647, 650, 785–786 Acanthosomatidae  283, 306–308 Rolstonus rolstoni  307 Adelgidae  351, 628 Adelges piceae  633, 667 Adelges tsugae 667 Aenictopecheidae  281, 285 Aepophilidae  290, 290 Aepophilus bonnairei 290 Aleyrodidae  294, 296, 608, 646, 652, 674 Aleurothrixus floccosus  603, 614 Bemisia tabaci  540, 582, 660 Alydidae  283, 301–302 Alydus 301 Esperanza texana 301 Leptocorisinae 301 Anthocoridae  282, 290–292, 312 Anthocoris nemoralis 645 Montandoniola moraguesi 656 Orius insidiosus  291 Aphalaridae Spondyliaspinae 121 Aphelocheiridae 209, 281, 288 Aphididae 628 Amphorophora 632 Aphis citricidus  633, 660 Aphis fabae 632 Aphis glycines  615, 633, 657, 660 Aphis gossypii 632 Aphis sambuci 628, 629 Aulacorthum solani 632 Baizongia pistaciae 628 Brachycaudus helichrysi 632 Brevicoryne brassicae 627 Cinara 633 Diuraphis noxia  615, 633, 659, 659, 664 Eriosoma lanigerum 634 Macrosiphum rosae  629 Myzus antirrhinii 633 Myzus persicae 632 Pemphigus 633 Pemphigus populivenae 245 Rhopalosiphum maidis 633

Rhopalosiphum padi  615 Schlechtendalia chinensis 628 Aphidoidea  124, 154, 184, 236, 296, 608, 627–634 (chapter 20), 646, 647 Aphylidae  283, 308 Aradidae  121, 167, 283, 301 Aradus acutus  298 Aradus cimamomeus 301 Artheneidae 303 Chilacis typhae 303 Holcocranum saturejae 303 Auchenorrhyncha  3, 147, 160, 161, 168, 182, 184, 208, 243 Belostomatidae 209, 281, 289 Abedus  208, 289 Belostoma  208, 289 Belostoma flumineum  286 Berytidae  283, 304 Gampsocorinae 304 Hoplinus 304 Metacanthinae 304 Metacanthus annulosus 304 Plyapomus longus 304 Pronotacantha 304 Pronotacantha annulata  298 Blissidae  283, 304 Blissus leucopterus  298, 304 Canopidae  283, 308 Canopus burmeisteri 308 Canopus fabricii 308 Ceratocombidae  281, 285 Ceratocombius vagans  286 Cicadellidae  54, 152, 209, 296, 444, 482, 539, 647 Alnetoidia alneti 537 Homalodisca coagulata  20, 642, 664–665 Homalodisca vitripennis 617 Opsius stactagalus 657 Scaphoideus titanus 660 Cicadidae  122, 177, 539 Cicadetta montana 539 Cosmopsaltriina 122 Dundubiina 122 Fijipsalta 122 Kikihia 122 Kikihia convicta 121

811

812

Index

Hemiptera: Cicadidae (contd.) Maoricicada 122 Rhodopsalta 122 Cimicidae  282, 292, 312 Cimex lectularius  291, 646, 648 Cimicomorpha  209–301, 312 Pulvinaria urbicola 757, 758 Coccina 154 Coccoidea  119, 154, 295, 391, 482, 646, 647 Coelostomidiidae 125 Ultracoelostoma 666 Coleorrhyncha 279 Colobathristidae  283, 304 Coreidae  283, 302, 312 Acanthocephala femorata  298 Amblypelta 302 Chelidinea vittiger 302 Chelinidea vittiger  298 Clavigralla gibbosa 302 Coreinae 302 Leptoglossus phyllopus  298, 302 Coreoidea 301–303 Corixidae 209, 281, 288, 653 Sigara hubbelli  286 Cryptococcidae Cryptococcus fagisuga 660 Cryptorhamphidae  283, 304 Curaliidae 292 Curalium cronini 292 Cydnidae  283, 308 Scaptocoris castaneus  307 Cymidae 304 Cyrtocoridae  283, 308 Dactylopiidae Dactylopius coccus  24, 787 Delphacidae 539 Nilaparvata lugens  13, 537, 539 Perkinsiella saccharicida 658 Diaspididae Aonidiella aurantii  613, 788 Chrysomphalus aonidum 613 Diaspidiosus perniciosus  656, 658 Lepidosaphes ulmi 648 Dinodoridae  283, 308 Dipsocoridae  208, 285 Cryptostemma uhleri  286 Dipsocoromorpha  285–287, 312

Enicocephalidae  281, 285 Systelloderes biceps  286 Enicocephalomorpha 312 Flatidae Metcalfa pruinosa  141, 655 Fulgoroidea 482 Gelastocoridae  281, 289 Gelastocoris oculatus  286 Nerthra 289 Geocoridae  283, 304–305, 312 Cattarus 305 Cephalocattarus 305 Geocorinae 305 Geocoris punctipes  298 Pamphantinae 305 Gerridae 209, 281, 287 Gerris marginatus  286 Gigantometra gigas 287 Halobates 209 Gerromorpha  287–288, 312 Hebridae  281, 287 Hebrus concinnus  286 Helotrephidae  281, 289 Henicocoridae  283, 303 Hermatobatidae  281, 287 Heterogastridae  283, 305 Heteroptera  3, 54, 77, 80, 147, 168, 184, 212, 279–313 (chapter 10), 609, 646 Homoptera  77, 80 Hydrometridae  281, 288 Hydrometra martini  286 Hyocephalidae  283, 302–303 Hypsipterygidae  281, 287 Idiostolidae  283, 303 Joppeicidae  282, 292 Joppeicus paradoxus 292 Kerriidae Kerria lacca 24 Largidae  283, 311 Araphe 311 Arhaphe carolina  307 Larginae 311 Largus 311 Pararaphe 311 Physopeltinae 311 Lasiochilidae  282, 292 Lasiochilus 292

Index

Leptopodidae  282, 290 Patapius spinosus  286, 290, 654 Leptopodomorpha  209, 290, 312 Lestoniidae  283, 308 Lestonia haustorifera 308 Lyctocoridae  282, 292 Lyctocoris 292 Lyctocoris campestris  291 Lygaeidae  283, 305 Kleidocerys resedae 305 Lygaeinae 305 Lygaeus 305 Lygaeus kalmii  298 Nysius 305 Oncopeltis 305 Oncopeltus fasciatus 19 Orsillinae 305 Spilostethus 305 Lygaeoidea  303–306, 312, 646 Macroveliidae  281, 287 Malcidae  284, 305 Chauliopinae 305 Chauliops 305 Malcinae 305 Margarodidae (See Coelostomidiidae, Monophlebidae) Coelostomidiinae. See Coelostomidiidae Medocostidae  282, 297 Medocostes lestoni 297 Megarididae  284, 309 Membracidae 539 Enchenopa binotata 539 Meschiidae  284, 305 Mesoveliidae  281, 288 Darinwinivelia fosteri  286 Mesovelia mulsanti  286 Microphysidae  282, 293 Chinaola quercicola 293 Mallochiola gagates 293 Miridae  282, 293–296, 311, 312, 664 Barberiella formicoides 295 Biliranoides 296 Blepharidopterus angulatus 296 Bothynotus modesus  291 Bryocorinae 294 Bryocorini 294 Callichilella grandis 295

Campylomma verbasci 296 Ceratocapsus 296 Ceratocapsus modestus  291 Clivinematini 294 Coridromius 296 Cylapinae 294 Cylapus 293 Cylapus tenuis 294 Cyrtopeltocoris illini  291 Deraeocorinae 294 Deraeocoris 295 Deraeocorus nebulosus 295 Dicyphini 294 Dicyphus agilis  291 Distantiella theobroma  293, 294 Eccritotarsini 294 Eccritotarsus 294 Fulvius 294 Fulvius imbecilis  291 Gigantometopus rossi 295 Hallodapini 296 Halticini 296 Halticotoma valida 294 Halticus bractatus 296 Helopeltis 293 Herdoniini  294, 295 Heterotoma planicorne 296 Hyalochloria 296 Hyalopeplini 295 Hyalopeplus pellucidus 295 Isometopinae 295 Leptopterna dolabrata  291, 295 Leucophoropterini 296 Lopidea davisi 296 Lygus  293, 295 Macrolophus melanotoma 294 Mecistoscelini 295 Melanotrichus virescens 296 Mirinae 295 Mirini 295 Monalocoris 294 Monoloniini 294 Myrmecophyes oregonensis 296 Notostira elongata 295 Odoniellini 294 Orthotylini 296 Phylinae 296

813

814

Index

Hemiptera: Miridae (contd.) Phytocoris 295 Pilophoropsidea 296 Pilophoropsis 296 Pilophorus 296 Poecilocapsus lineatus  291 Polymerus wheeleri 312 Psallopini 294 Pseudatomoscelis seriatus 293 Pycnoderes quadrimaculatus 294 Ranzovius 296 Renodaeus 296 Resthenia scutata 295 Restheniini 295 Rhinocapsus vanduzeei 296 Rhyparochromomiris femoratus 294 Sahlbergella singularis  293, 294 Schaffneria 296 Stenodemini 295 Stethoconus japonicus 295 Tenthecoris 294 Termatophylidea 295 Termatophylini 295 Trigonotylus caelestialium 295 Monophlebiidae Icerya purchasi  11, 251, 606, 664 Nabidae  282, 297, 312 Arachnocoris 297 Nabis americoferus  291 Pagasa fusca  291 Prostemmatinae 297 Naucoridae 209, 282, 288 Pelocoris carolinensis  286 Nepidae 209, 282, 289 Nepa apiculata  286 Nepomorpha  288–290, 312 Ninidae  284, 305 Notonectidae  282, 289 Notonecta undulata  286 Ochteridae  282, 289 Ochterus americanus  286 Omaniidae  282, 290 Ortheziidae 295 Oxycarenidae  284, 305 Oxycarenus 305 Oxycarenus hyalinipennis 305

Pachygronthidae  284, 306 Pachygronthinae 306 Phlegyas abbreviatus  298 Teracriinae 306 Pachynomidae  282, 297 Paraphrynoveliidae  281 Parastrachiidae. See Thyreocoridae–Parastrachiinae Peloridiidae 119 Pentatomidae  284, 309, 312 Aelia americana  307 Aelia furcula 309 Alcaeorrhynchus grandis  307 Asopinae 309 Biprorulus bibax 309 Edessa florida  307 Eurygaster integriceps 310 Euschistus 309 Murgantia histrionica  307 Nezara viridula  309, 312, 668, 670 Oebalus pugnax  307 Parabrochymena arborea  307 Pentatominae 309 Podisus 309 Pentatomoidea 306–310 Pentatomomorpha 301–311 Phloeidae  284, 309 Phylloxeridae  628, 632 Daktulosphaira vitifoliae  656, 658 Piesmatidae  284, 306 Parapiesma cinereum  298 Piesmatinae 306 Psamminae 306 Plataspidae  284, 309 Comptosoma 309 Libyaspis 309 Megacopta cribraria 309 Pleidae  282, 289 Neoplea striola  286 Plokiophilidae  282, 292 Embiophilinae 292 Plokiophilinae 292 Polyctenidae  282, 292, 312 Hesperoctenes eumops  291 Potamocoridae  282, 288 Pseudococcidae Antonina graminis 657

Index

Maconellicoccus hirsutus  659 Phenacoccus manihoti 613 Pseudococcus comstocki 603 Psylloidea 184 Psyllidae 664 Heteropsylla cubana 654 Livilla variegata 664 Psylloidea 120 Pyrrhocoridae  284, 311 Antilochus 311 Dysdercus 311 Raxa 311 Dysdercus lunulatus  307 Reduviidae  283, 299–300, 312 Apiomeris crassipes  298 Arilus 299 Arilus cristatus  298, 300 Berlandiana 299 Centraspis 299 Ectrichodiinae 299 Emesaya 299 Emesinae 299 Empicoris 299 Largus succinctus  307 Graptocleptes 300 Harpactorinae 299 Lophoscutus 300 Microtomus purcis  298 Phymata 300 Phymata pennsylvanica  298 Phymatinae  299, 300 Reduviinae 300 Reduvius personatus 300 Rodnius prolixus 300 Salyavata variegata 300 Salyavatinae 300 Stenopodainae 300 Triatoma 312 Triatoma sanguisuga  298 Triatominae 299 Rhopalidae  284, 302 Arhyssus lateralis  298 Boisea trivittata  298, 302 Jadera haematoloma 312 Niesthrea louisianica 302 Rhopalinae 302 Serinethinae 302

Rhyparochromidae 121, 284, 306, 654 Cleradini  306, 312 Drymini 306 Lethaeini 306 Myodocha serripes  298 Myodochini 306 Ozophorini 306 Plinthisinae 306 Pseudopachybrachius basalis  298 Rhyparochrominae 306 Rhyparochromini 306 Saileriolidae  284, 309 Saldidae 209, 282, 290 Saldula galapagosana  286 Schizopteridae  281, 285, 312 Corixidea major 312 Glyptocombus saltator  286 Scutelleridae  284, 310 Camirus porosus  307 Coleotichus blackburniae 668 Sphyrocoris obliquus  307 Stemmocryptidae 287 Stenocephalidae 303 Dicranocephalus bianchii 303 Dicranocephalus insularis  298, 303 Sternorrhyncha  3, 97, 147, 161, 168, 244, 609 Termitaphidae  284, 301 Tessaratomidae  284, 310 Musgraveia 310 Piezosternum subulatum  307 Oncomerinae 310 Tettigarctidae 120 Thaumastellidae  284, 310 Thaumastocoridae  283, 296 Thaumastocorinae 296 Xylastodorinae 296 Xylastodoris luteolus  291, 296 Thyreocoridae  284, 310 Corimelaena pulicaria  307 Corimelaeninae 310 Thyreocorinae 310 Parastrachiinae 310 Tingidae  283, 296–297, 312 Atheas mimeticus  291 Cantacaderinae 297 Corythucha ciliata  291, 297 Corythucha gossypii 297

815

816

Index

Hemiptera: Tingidae (contd.) Gargaphia 297 Kalama tricornis 654 Stephanitis pyrioides 295 Teleonemia scrupulosa 297 Tinginae 297 Vianaidinae 297 Urostylididae  284, 310 Veliidae  281, 287 Microvelia ashlocki  286 Velocipedidae  283, 300–301 Hymenoptera 2, 3, 50, 52, 54, 56, 69, 78, 80, 117, 120, 125, 147, 154, 155, 173, 206, 209, 212, 419–445 (chapter 12), 512, 579, 582–583, 606, 607, 608, 609 Aculeata  426, 443–446 Agaonidae  420, 424, 440, 788 Pleistodontes addicotti  442 Alvarommatidae (extinct)  425 Ampulicidae  420, 423, 446 Anaxyelidae  420, 423, 437 Andreneliidae (extinct)  425 Andrenidae  420, 423 Angarosphecidae (extinct)  423 Anomopterellidae (extinct)  425 Aphelinidae  420, 424, 608, 609, 616 Aphelinus albipodis  615 Aphelinus atriplicis  615 Aphelinus certus  615 Aphelinus hordei  615 Aphelinus kurdumovi  615 Aphelinus varipes 615, 615, 616, 617 Aphytis chrysomphali 788 Aphytis holoxanthus 613 Aphytis lingnanensis  613, 788 Aphytis melinus 788 Cales noacki  603, 615 Encarsia  614, 616 Encarsia sophia 614 Apidae  420, 423 Apis cerana 788 Apis mellifera  14, 24, 125, 644, 662, 788 Apis mellifera scutellata 659 Bombus  173, 582–583 Bombus terrestris  125, 666 Centris nitida 666 Liotrigona 582–583

Apocrita  147, 426 Apoidea  21, 23, 97, 120, 166, 666 Archaeocynipidae (extinct)  426 Argidae  420, 423, 437 Aulacidae  421, 425, 438 Austrocynipidae  421, 439 Austroniidae  422, 425, 439 Azotidae  420 Belytonymidae (extinct)  424 Bethylidae  421, 424, 444 Epyrini 444 Blasticotomidae  420, 423, 437 Braconidae  148, 187, 421, 425, 438, 607, 608, 609, 611 Aleiodes 427 Apanteles 427 Cotesia melitaearum 614 Heterospilus 427 Microgastrinae  438, 786 Bradynobaenidae  422, 444 Cephidae  420, 423, 437 Ceraphronidae  420, 440 Ceraphronoidea 440 Chalcididae  420, 424, 611 Chalcidoidea  13, 55, 97, 120, 154, 440–443, 606, 607 Chrysididae  421, 424, 443 Amiseginae 443 Chrysis 443 Loboscelidiinae 443 Chrysidoidea 443–444 Cimbicidae  420, 423, 437 Colletidae  420, 423 Colletinae 120 Crabronidae  420, 423, 446 Microstigmus 443 Cynipencyrtidae  420 Cynipidae  421, 424, 439 Cynipoidea  439, 606, 607 Daohugoidae (extinct)  423 Diapriidae  421, 425, 440 Belytinae 440 Diaprioidea 439 Diprionidae  420, 423, 437 Dryinidae  421, 424, 444 Electrotomidae (extinct)  423 Embolemidae  421, 424, 442

Index

Encyrtidae  420, 424, 608, 609, 611 Apoanagyrus lopezi  603, 613 Neodusmetia sangwani 603 Eostephanitidae (extinct)  426 Ephialtitidae (extinct)  425 Eriaporidae  420 Eucharitidae  421, 424, 440 Eulophidae  421, 424, 608, 609 Cirrospilus 611 Closterocerus utahensis 611 Pnigalio  611, 617 Quadrastichus erythrinae 654 Sympiesis 611 Zagrammosoma 611 Eupelmidae  421, 424, 611 Eurytomidae  421, 424, 440, 611 Bruchophagus 605 Evaniidae  421, 425, 438 Evanioidea 437–438 Falsiformicidae (extinct)  424 Figitidae  421, 424, 439 Formicidae  11, 12, 21, 79, 111, 120, 122, 123, 124, 128, 173, 245, 295, 349, 422, 425, 445–446, 465, 483, 577, 605, 646, 665– 666, 716 Anoplolepis gracilipes  125, 666, 757 Atta  21, 431 Campononotus nearcticus 295 Carebara 445 Dinoponera 445 Dorylus  431, 445 Eciton 431 Eciton burchellii 432 Formica subsericea 295 Lasius neoniger 295 Linepithema humile  125, 419, 429, 665 Messor barbarus 445 Myrmeciinae 120 Myrmecocystus 113 Pachycondylla chinensis 666 Paraponera clavata 431 Pheidole megacephala  125, 666, 757, 758 Rhoptromyrex transversiodis 285 Rhytidoponera 122 Solenopsis invicta  125, 608, 657, 659, 662, 663, 665, 674 Solenopsis geminata 4

Solenopsis richteri 663 Titanomyrma (extinct)  433 Wasmannia auropunctata  4, 124, 429, 666 Gallorommatidae (extinct)  425 Gasteruptiidae  421, 438 Hyptiogastrinae 438 Gerocynipidae (extinct)  424 Halictidae  420, 423 Halictinae 120 Heloridae  422, 425, 439 Heterogynaeidae 446 Heterogynaidae  420 Ibaliidae  421, 424, 439 Ichneumonidae  55, 155, 421, 425, 438–439, 607, 608, 609, 612 Agriotypinae 439 Agriotypus 439 Diplazontinae 439 Enicospilus 431 Exenterini 155 Megarhyssa atrata 438 Megarhyssa gloriosa 438 Ophion 431 Tryphoninae 438 Ichneumonoidea  606, 613 Iscopinidae (extinct)  425 Ismaridae  421, 439 Jurapriidae (extinct)  425 Karatavitidae (extinct)  423 Khutelchalcididae (extinct)  426 Kuafuidae (extinct)  426 Leucospidae  421, 424 Liopteridae  421, 425, 439 Maamingidae  421, 440 Maimetshidae (extinct)  425 Megachilidae  420, 423 Anthidium manicatum 666 Megachile rotundata 656 Megalodontesidae  420, 423, 437 Megalyridae  422, 425, 437 Megaspilidae  420, 424, 440 Melittidae  420, 423 Mellitosphecidae (extinct)  424 Mesoserphidae (extinct)  425 Monomachidae  421, 440 Mutillidae  422, 425, 444 Mymaridae  421, 424, 442, 616

817

818

Index

Hymenoptera: Mymaridae (contd.) Dicopomorpha echmepterygis  429, 442 Gonatocerus 615 Gonatocerus ashmeadi 617 Kikiki huna  430 Mymarommatidae  422, 425, 437 Ormyridae  421 Orussidae  420, 423, 426, 437 Paleomelittidae (extinct)  424 Pamphiliidae  420, 423, 437 Parasitica  426, 437–444 Paroryssidae (extinct)  423 Pelecinidae  422, 425, 439 Peradeniidae  422, 425 Pergidae  420, 437 Perilampidae  421, 424 Platygastridae  422, 425, 439 Amitus spinifrons 603 Scelioninae 439 Telenominae 439 Platygastroidea  439, 606, 607 Plumalexiidae (extinct)  424 Plumariidae  421, 442 Pompilidae 209, 422, 425, 444 Anoplius 209 Pepsis  431, 444 Praeaulacidae (extinct)  425 Praeichneumonidae (extinct)  425 Praesiricidae (extinct)  423 Proctorenyxidae  422, 439 Proctotrupidae 54, 422, 425, 439 Proctotrupoidea 439 Protimaspidae (extinct)  425 Protosiricidae (extinct)  423 Pseudosiricidae (extinct)  423 Pteromalidae  421, 424, 608, 609, 611, 616 Nasonia 431 Nasonia vitripennis 614 Radiophronidae (extinct)  424 Rhopalosomatidae  422, 426, 444 Roproniidae  422, 425, 439 Rotoitidae  421 Sapygidae  422, 426, 444 Sclerogibbidae  421, 424, 442 Scolebythidae  421, 424, 442 Scoliidae  422, 426, 444 Sepulcidae (extinct)  423

Serphitidae (extinct)  425 Sierolomorphidae  422, 426, 444 Signiphoridae  421 Sinosiricidae (extinct)  423 Siricidae  420, 423, 437, 647 Spathiopterygidae (extinct)  425 Sphecidae  420, 424, 446 Stenotritidae  420 Stephanidae  422, 425, 437 Stigmaphronidae (extinct)  424 Stolamissidae (extinct)  425 Symphyta  147, 426, 436–437 Tanaostigmatidae  421, 424 Tenthredinidae  154, 155, 420, 423, 437 Caliroa cerasi 648 Nematinae  70 Tetracampidae  421, 424 Tiphiidae  422, 426, 444 Torymidae  421, 424, 611 Megastigmus 605, 647 Megastigmus transvaalensis 617 Trichogrammatidae  421, 424, 442–443 Trichogramma  442, 613, 616 Trichogramma minutum 614 Trichogramma platneri 614 Trigonalidae  422, 425, 437 Vanhorniidae  422, 439 Vespidae  422, 426, 444–445 Eumenes 445 Eumeninae  120, 445 Masarinae 445 Polistes  606, 610 Polistes chinensis 125 Polistes humili 125 Polistes versicolor 666 Polistinae 445 Stenogastrinae 445 Vespinae 445 Vespula 429 Vespula germanica  125, 666 Vespula pensylvanica 666 Vespula vulgaris  125, 666 Vespoidea  173, 444 Xiphydriidae  420, 437, 438, 647 Xyelidae  420, 423, 437 Xyelotomidae (extinct)  423 Xyelydidae (extinct)  423

Index

i Isoptera. See Blattodea–Termitoidea

l

Lepidoptera 2, 3, 11, 16, 20, 21, 52, 69, 70, 78, 80, 117, 118, 120, 127, 146, 154, 155, 175, 179, 181, 206, 211, 212, 295, 463–489 (chapter 13), 578, 579, 582, 583, 606, 607, 646, 650 Acanthopteroctetidae  470, 477 Acanthopteroctetoidea  476 Adelidae  471, 478 Adeloidea  471, 476, 478 Aenigmatineidae  470, 478 Agathiphagidae  470 Agathiphagoidea  476 Aididae  474 Alucitidae  473 Alucitoidea  473, 479 Andesianidae  471, 476, 478 Angiospermivora 477 Anomosetidae. See Hepialidae Anthelidae  475, 485 Apatelodidae  475, 485 Apoditrysia 480–487 Argyresthiidae  472 Attevidae  472, 480 Autostichidae  472 Batrachedridae  472 Bedelliidae  472 Blastobasidae  472 Bombycidae  475, 485 Bombyx mori  21, 23, 24, 485 Bombycoidea  475, 479, 485–486 Brachodidae  473 Brahmaeidae  475, 485 Bucculatricidae  472 Callidulidae  474, 484 Calliduloidea  479 Carposinidae  473, 479, 484 Carthaeidae  475, 485 Castniidae  473, 481 Synemon plana 123 Cecidosidae  471 Cecidosiidae 478 Choreutidae  473 Choreutoidea  479, 480

Cimeliidae  474 Coleophoridae  472, 481 Copromorphidae  473, 484 Cosmopterigidae  472, 480 Hyposmocoma 481 Cossidae  473, 481 Cossoidea  473, 479, 481 Acentropinae 211 Crambidae  474 Arcola malloi 217 Sameodes albiguttalis 217 Scirpophaga incertula 218 Scirpophaga innotata 218 Cyclotornidae  473, 482 Dalceridae 57, 473, 482 Depressariidae  472 Doidae 469, 474 Douglasiidae  472 Drepanidae  474 Drepanoidea 469, 474, 479 Dryadaulidae  471, 478 Dudgeoneidae  473 Elachistidae  472, 480 Endromidae  475, 485 Epermeniidae  473 Epermenioidea  479 Epicopeiidae  475, 486, 488 Epipyropidae  473, 482, 610 Erebidae  475 Arctiinae  173, 487 Hyphantria cunea 670 Lymantria dispar  11, 466, 647 Lymantria monacha 176, 647 Lymantriinae  173, 487 Eriocottidae  471, 478 Eriocraniidae  470, 477 Eriocranioidea  476 Eupterotidae  475, 485 Euteliidae  475, 488 Exoporia 478 Galacticidae  473 Galacticoidea  479 Gelechiidae  472, 480 Gelechioidea 469, 472, 479, 480 Geometridae 173, 475, 486–487 Archiearinae 486 Asaphodes stinaria 127

819

820

Index

Lepidoptera: Geometridae (contd.) Biston betularia 18 Desmobathrinae 486 Ennominae 487 Geometrinae 487 Larentiinae 487 Nemoria 487 Oenochrominae 486 Operophtera bruceata 663 Operophtera brumata  251, 466, 487, 663 Orthostixinae 487 Sterrhinnae 487 Xanthorhoe bulbulata 127 Geometroidea  475, 479, 486–487 Glyphipterigidae  472, 480 Gracillariidae  472, 479, 610 Phyllocnistis citrella  603, 610–612, 611 Phyllonorycter blancardella 610, 611 Phyllonorycter messaniella 654 Gracillarioidea  471, 479, 479 Hedylidae  474, 482 Heliocosmidae Heliocosma 481 Heliodinidae  472 Heliozelidae  471, 478 Hepialidae  470, 477 Aoraia mairi 124 Hepialoidea  469, 470, 476, 477 Hesperiidae  474, 482 Astraptes fulgerator 583 Atalopedes campestris 23 Saliana severus 577 Heterobathmiidae  470 Heterobathmioidea  476, 477 Heterogynidae  473 Heteroneura 477 Himantopteridae  474 Hyblaeidae  474, 484 Hyblaeoidea  474, 479, 484 Immidae  473 Immoidea  479, 484 Incurvariidae  471, 478 Lacturidae  473 Lasciocampidae 486 Lasiocampidae  474 Dendrolimus pini 176 Malacosoma 486

Malacosoma disstria 250 Lasiocampoidea  479 Lecithoceridae  472, 480, 481 Limacodidae  474, 482 Lophocoronidae  470, 477 Lophocoronoidea  476 Lycaenidae 173, 474, 483 Paralucia pyrodiscus lucida 127 Paralucia spinifera 127 Lyonetiidae  472, 480 Lypusidae  472 Macrolepidoptera 123 Manidiidae 57 Meessiidae  471, 478 Megalopygidae  474, 482 Metarbelidae  473 Micropterigidae  470, 477 Micropterigoidea  476 Micropterygidae 122 Millieriidae  471, 478 Mimallonidae 469, 474 Mimallonoidea  479 Mnesarchaeidae 477 Mnesarchaeoidea 470 Momphidae  472 “Myoglossata” 477 “Neolepidoptera” 477 Neopseustidae  470 Neopseustoidea 470, 476 Nepticulidae  471 Nepticuloidea  476, 478 Noctuidae (see also Erebidae)  173, 475, 487–488 Agrotis infusa 113 Copitarsia 671 Euproctis chrysorrhoea 466 Euxoa auxiliaris 11 Helicoverpa 487 Orgyia thyellina 673 Noctuoidea 469, 475, 479, 487–488, 583 Notodontidae  475, 487 Dioptinae 465 Nymphalidae 114, 474, 483 Boloria 173 Danainae 483 Danaus plexippus  25, 483 Erebia 173

Index

Heliconiinae 483 Heliconius  465, 483 Ithomiini 483 Libytheinae 483 Limenitidinae 484 Morpho  24, 508 Nymphalinae 483 Oeneis 173 Satyrinae 483 Vanessa atalanta 483 Nolidae  475, 488 Obtectomera 482–487 Oecophoridae 120, 472, 480 Oenosandridae  475, 487 Opostegidae  471 Palaeosetidae. See Hepialidae Palaephatidae  471, 478 Azaleodes 478 Palaephatus 478 Ptyssoptera 478 Palaephatoidea 478 Papilionidae 114, 474, 483, 532 Ornithoptera alexandra  114, 115 Ornithoptera richmondia 116 Parnassius 171 Troidini 483 Papilionoidea 469, 474, 479, 482–483 Phaudidae  473 Phiditiidae  475, 485 Pieridae 114, 474, 483 Aporia crataegi 171 Colias 173 Dioryctria abietella 176 Plutellidae  472, 480 Plutella xylostella  218, 480 Praydidae  472 Prodidactidae  474, 484 Prodoxidae 465, 471, 478 Tegeticula 13 Prototheoridae. See Hepialidae Pseudobistonidae  475, 486 Psychidae  471, 478 Pterolonchidae  472 Pterophoridae 173, 473, 481 Pterophoroidea  479, 481 Pyralidae  474, 484 Cactoblastis cactorum  11, 466, 668

Chalcoela  606, 610 Crambinae 484 Diatraea 251 Ephestia elutella 484 Galleria melonella 484 Ostrinia nubilalis  484, 658, 659 Phycitinae 484 Plodia interpunctella 484 Pyraustinae 484 Spilomelinae 484 Sthenauge 610 Pyraloidea  474, 479, 480, 484 Ratardidae  473 Riodinidae  474, 483 Roeslerstammiidae  471 Saturniidae  11, 465, 475, 485, 583, 610 Coscinocera hercules 114 Gonimbrasia belina  93, 486 Satyridae. See Nymphalidae–Satyrinae Schistonoeidae  472 Schreckensteiniidae  473 Schreckensteinioidea  479 Scythrididae  472 Scythropiidae  472, 480 Sematuridae  475, 486 Sesiidae  473, 481 Simaethistidae  472 Simaethistoidea  479 Somabrachyidae  474 Sphingidae  475, 485, 583 Acosmeryx naga 172 Manduca quinquemaculata 486 Manduca sexta  486, 506 Stathmopodidae  472 Thyrididae  474, 482, 484 Thyridoidea  479 Tineidae  471, 478 Acrolophinae 478 Tineodidae  473 Tineoidea  471, 479 Tischeriidae  471, 478 Tischerioidea  476 Tortricidae (see also Heliocomidae)  473, 481 Choristoneura  439, 481 Cydia pomonella  481, 648, 652, 659 Epiphyas postvittana 481 Lobesia botrana 481

821

822

Index

Lepidoptera: Tortricidae (contd.) Olethreutinae 481 Tortricinae 481 Tortricoidea  479, 481 Tridentaformidae  471, 478 Uraniidae  475, 486 Urodidae  473 Urodoidea  479 Whalleyanidae  474 Whalleyanoidea  479 Xyloryctidae  472 Yponomeutidae 121, 472, 480 Yponomeuta 538 Yponomeutoidea  472, 479, 480 Ypsolophidae  472 Zygaenidae  474, 482 Chalcolsiinae 488 Zygaenoidea  473–474, 479, 482

m

Mantodea  3, 51, 56, 77, 80, 147, 148, 154, 184, 579, 581 Mantophasmatodea (= Notoptera– Mantophasmatodea)  3, 95, 118, 119, 512, 579, 581 Epiophlebiidae 179 Hemiphlebiidae 119 Hemiphlebia mirabilis 128 Hypolestidae 119 Petaluridae Petalura ingentissima 119 Platycnemididae Metacnemis valida  748 Synlestidae Chlorolestes umbratus  750 Mecoptera  3, 52, 120, 147, 155, 184, 210, 212, 579, 584 Boreus 152 Boreus hyemalis  153 Nannochoristidae  120, 210 Megaloptera  3, 51, 56, 97, 103, 147, 155, 184, 209, 212, 579, 583 Sialidae 156 Microcoryphia (Archaeognatha)  3, 51, 147, 580 Myriapoda  69

n

Neuroptera  3, 51, 97, 103, 209, 212, 579, 583, 606, 607 Ascalaphidae 184 Chrysopidae  18, 98 Hemerobiidae 184 Mantispidae  184, 610 Mantispinae 606 Myrmeleontidae 184 Palparini 104 Nemopteridae  104, 184 Nemoptera sinuata  149 Neurorthus 209 Climacia areolaris 209 Notoptera. See Grylloblattodea and Mantophasmatodea

o

Odonata  3, 15, 25, 50, 51, 55, 56, 69, 117, 147, 155, 207, 212, 218, 516, 579, 580 Aeshnidae 207 Cordulephyidae 119 Orthoptera  3, 11, 13, 20, 51, 80, 93, 121, 122, 147, 148, 152, 154, 173, 180, 182, 208, 212, 579, 580 Acrididae  77 Catantopinae 184 Chrysochraontini 154 Conophymatini 154 Dericorythini 184 Diexini 184 Egnatiini 184 Iranellini 184 Oedipodinae 184 Uvaroviini 184 Anostostomatidae 113 Ensifera 184 Gryllidae 18, 77 Grylloidea 177 Gryllotalpidae  646 Scapteriscus  659 Pamphagidae Pamphaginae  154, 184 Thrinchinae 154 Pyrgomorphidae Zonocerus variegatus 19

Index

Rhaphidophoridae 113 Stenopelmatidae Deinacrida heteracantha 113 Tettigoniidae  77 Deracanthinae 154 Drymadusini 154 Gampsocleidini 154 Glyphonotinae 154 Odonturini 154 Onconotinae 154 Poecilimon  149 Saga pedo  150

p

Phasmatodea  3, 77, 80 Heteronemiidae 300 Diapheromera femorata 300 Phasmatidae Acrophylla 114 Carausius morosus 19 Dryococelus australis  113, 114 Eurycnema goliath 114 Phthiraptera  3, 154, 209, 579, 581 Amblycera  51, 54, 147 Anoplura  51, 54, 147, 771 Echinophthiriidae 209 Haematopinidae Haematopinus oliveri 748 Menoponidae 209 Pediculidae Pediculus 13 Pediculus humanus 648 Plecoptera  3, 51, 69, 128, 147, 155, 173, 207, 212, 218, 579, 581 Antarctoperlaria 119 Austroperlidae 119 Capnia kolymensis 155 Euholognatha 155 Eustheniidae 119 Gripopterygidae 119 Leuctridae 207 Nemouridae 207 Nemoura 155 Notonemouridae 155 Perlidae 207 Perlodidae 207

Scopuridae 155 Taeniopterygidae 155 Protura  3, 558, 578–580, 579 Psocoptera  3, 51, 77, 80, 147, 579, 581, 654

r

Raphidioptera  3, 51, 146, 147, 184, 579, 583

s

Siphonaptera  3, 52, 56, 146, 154, 579, 584, 646 Pulicidae Ctenocephalides felis 584 Pulex 13 Xenopsylla 13 Xenopsylla chaeopis 662 Strepsiptera  3, 51, 118, 512, 579, 582, 605, 607 Mengenillidae  605, 610 Stylopidae 186

t

Thysanoptera  3, 51, 69, 97, 120, 147, 295, 579, 582, 605, 646, 647, 650 Phlaeothripidae 120 Amynothrips andersoni 217 Cartomothrips 654 Gynaikothrips ficorum 656 Thripidae Frankliniella occidentalis 660 “Thysanura”. See Microcoryphia and Zygentoma Trichoptera  3, 52, 69, 118, 146, 155, 173, 210, 213, 439, 579, 582, 607 Annulipalpia 211 Antipodoecidae 119 Chathamiidae 119 Conoesucidae 119 Glossosomatidae 211 Helicophidae 119 Hydrobiosidae 119 Hydroptilidae 211 Integripalpia 211 Orthotrichia 610 Kokiriidae 119 Limnephilidae Drusus annulatus 218 Limnephilus lunatus 218 Oeconesidae 119

823

824

Index

Trichoptera (contd.) Philopotamidae Chimarra 610 Plectrotarsidae 119 Rhyacophiloidea 211 Tasimiidae 119

z

Zoraptera  3, 51, 57, 118, 147, 578, 579 Zygentoma (see also “Thysanura”)  3, 147, 579, 580 Lepidotrichidae 512

825

Index of Arthropod Taxa Arranged Alphabetically. Page numbers in bold indicate table entries, and numbers in italic face indicate entries on figures and in figure captions.

a Abedus  208, 289 Acalles 177 Acalymma vittatum 359, 368 Acanthocephala femorata  298 Acanthocnemidae  340, 353 Acanthocnemus nigricans 353 Acanthopteroctetidae  470, 477 Acanthopteroctetoidea  476 Acanthoscelides A. obtectus  367 A. pallidipennis 182 Acanthosomatidae  283, 306–308 Acartophthalmidae  233 Acentropinae 211 Acidocerinae 348 Acmaeodera  186 Acmaeoderella  186 Acmaeoderini 162 Acosmeryx naga 172 Acrididae  77 Acroceridae 229, 231, 242 Acrolophinae 478 Acrophylla 114 Aculeata  426, 443–446 Adelges A. piceae  633, 667 A. tsugae 667 Adelgidae  351, 628 Adelidae  471, 478 Adeloidea  471, 476, 478 Ademosynidae (extinct)  358

Adephaga 346–347 Aderidae  342, 355, 387 Adoretus  363 Aedes  13, 247 A. aegypti  660, 662, 713, 726 A. albopictus  662, 733 A. campestris 19 A. seriatus 662 A. taeniorhynchus 19 Aegialites stejnegeri 169 Aelia A. americana  307 A. furcula 309 Aeloderma  186 Aenictopecheidae  281, 285 Aenigmatineidae  470, 478 Aeolesthes sarta  365 Aeoloides  186 Aepophilidae  290, 290 Aepophilus bonnairei 290 Aeshnidae 207 Aethina tumida 354, 364, 659 Agaonidae  420, 424, 440, 788 Agapanthia 182 Agapythidae  341, 354 Agasicles hygrophila 217 Agathidium laevigatum 167 Agathiphagidae  470 Agathiphagoidea  476 Agathon  238 Agelena orientalis 304 Agrilus  186, 363

A. (Xenagrilus) 182 A. planipennis  142, 360, 660, 667 Agriotes  186, 364 Agriotypinae 439 Agriotypus 439 Agromyzidae  233, 244, 246, 611 Agrotis infusa 113 Agyrtidae  338, 348, 383 Ahasverus 354 Aididae  474 Airaphilus  186 Akalyptoischiidae  341, 354 Alatavia 171 Alcaeorrhynchus grandis  307 Alcidodes A. dentipes  372 A. karelinii  159, 172 Aleiodes 427 Aleochara 349 Aleocharinae  157, 349 Aleurothrixus floccosus  603, 614 Alexiidae  341, 354 Aleyrodidae  294, 296, 608, 646, 652, 674 Alleculidae  181, 185, 187 Alnetoidia alneti 537 Alocypha bimaculata  368 Alphitobius diaperinus  165, 359 Alphitophagus bifasciatus  165

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

826

Index

Alticinae  81, 148, 152, 154, 182, 184 Alucitidae  473 Alucitoidea  473, 479 Alvarommatidae (extinct)  425 Alydidae  283, 301–302 Alydus 301 Amaurochrous cinctipes  307 Amblycera  51, 54, 147 Amblypelta 302 Ameletopsidae 119 Amiseginae 443 Amitermes 113 Amitus spinifrons 603 Ammobius rufus  165 Amorphocephala coronata 168 Ampedus nigrinus 391 Amphicerus cornutus  364 Amphicoma 181 Amphimallon  363 Amphizoidae 146, 338, 347, 383 Amphorophora 632 Ampulicidae  420, 423, 446 Amynothrips andersoni 217 Anamorphidae 354 Anaspis 393 Anastrepha 246 Anatolica 181 A. amoenula  185 A. cechiniae  185 A. mucronata  185 A. polita borealis  185 A. sternalis gobiensis  185 Anaxyelidae  420, 423, 437 Ancipitis punctatissimus  373 Andesianidae  471, 476, 478 Andreneliidae (extinct)  425 Andrenidae  420, 423 Anemia dentipes  185 Angarosphecidae (extinct)  423 Angiospermivora 477 Angustonicus 122 Anillini 346 Anisandrus  373 Anisolabis maritima 208 Anisopodidae  230

Annulipalpia 211 Anobium punctatum 352 Anomala sulcata  363 Anomopterellidae (extinct)  425 Anopheles  13, 247, 537, 575 A. coluzzii 732 A. crucians 717 A. filipinae 729 A. gambiae  575, 662, 717, 730, 732, 788 A. punctulatus 717 A. quadrimaculatus [complex]  726, 730 A. varuna 729 Anoplius 209 Anoplognathus chloropyrus 360 Anoplolepis gracilipes 125, 666, 757 Anoplophora A. chinensis  366, 660 A. glabripennis 360, 366, 652, 660, 673 Anoplura  51, 54, 147, 771 Anostostomatidae 113 Antarctoperlaria 119 Anthaxia  186 A. quadripunctata 177 Anthelidae  475, 485 Anthicidae  187, 342, 355, 387, 394 Anthicus  187 Anthidium manicatum 666 Anthocomus equestris 392 Anthocoridae  282, 290–292, 312 Anthocoris nemoralis 645 Anthomyiidae  234, 245, 249 Anthomyzidae  233 Anthonomini 177 Anthonomus 161, 370 A. (Anthonomidius) 181 A. grandis 357, 370, 659 Anthores leuconotus  366 Anthrenus  186, 359, 646 Anthribidae  153, 157, 176, 183, 187, 342, 356, 387, 394

Anthribus nebulosus 391 Anthypurinus kaszabi  151 Antilochus 311 Antipodoecidae 119 Antonina graminis 657 Aonidiella aurantii  613, 788 Aoraia mairi 124 Apanteles 427 Apatelodidae  475, 485 Aphanisticus 160 Aphelini 168 Aphelinidae  420, 424, 608, 609, 616 Aphelinus A. albipodis  615 A. atriplicis  615 A. certus  615 A. hordei  615 A. kurdumovi  615 A. varipes  615, 615–617 Aphelocheiridae 209, 281, 288 Aphididae 628 Aphidoidea  124, 154, 184, 236, 296, 608, 627–634 (chapter 20), 646, 647 Aphidoletes aphidimyza 250 Aphis A. citricidus  633, 660 A. fabae 632 A. glycines  615, 633, 657, 660 A. gossypii 632 A. sambuci 628, 629 Aphodius  167, 181, 186 A. fimetarius 392 A. holdereri 148 Aphthona  148, 161 A. coerulea  153 A. nonstriata 161 A. sarmatica 166 A. testaceicornis 170 Aphylidae  283, 308 Aphytis A. chrysomphali 788 A. holoxanthus 613 A. lingnanensis  613, 788 A. melinus 788

Index

Apidae  420, 423 Apioceridae 155, 231 Apiomeris crassipes  298 Apionidae  173, 182, 183, 187 Apioninae 357 Apis A. cerana 788 A. mellifera  14, 24, 125, 644, 662, 788 A. mellifera scutellata 659 Apoanagyrus lopezi  603, 613 Apocephalus  605, 608 Apocrita  147, 426 Apoditrysia 480–487 Apoidea  21, 23, 97, 120, 166, 666 Apomecyna binubila  366 Aporia crataegi 171 Apriona  366 Apsilocephalidae  231 Apsis albolineatus 160 Apystomyiidae  231 Arachnida  69, 80 Arachnida–Araneae (= Araneida) 48, 77, 292, 444, 609, 610, 665 Arachnida–Scorpiones 608 Arachnocampa 239 Arachnocampa luminosa  113, 239 Arachnocoris 297 Aradidae  121, 167, 283, 301 Aradus A. acutus  298 A. cimamomeus 301 Araecerus fasciculatus 357 Araphe 311 Araucoderus  235 Archaeocynipidae (extinct)  426 Archeocrypticidae  341, 355, 386 Archiearinae 486 Archostemata 344–345 Arcola malloi 217 Arctiinae  173, 487 Argidae  420, 423, 437

Argopus 176 Argyresthiidae  472 Arhaphe carolina  307 Arhopalus ferus  367 Arhyssus lateralis  298 Arilus 299 A. cristatus  298, 300 Arixyleborus  374 Aromia bungii  365 Arrhenodes minutus  369 Artematopodidae  339, 385 Artheneidae 303 Arthropterus wilsoni  344 Asaphodes stinaria 127 Ascalaphidae 184 “Aschiza” 242–243 Asias mongolicus  187 Asida lutosa  165 Asilidae  231, 234, 242 Asiocoleidae (extinct)  358 Asopinae 309 Aspidytes wrasei  175, 178 Aspidytidae 175, 338, 347 Asteiidae  233 Astraptes fulgerator 583 Atalopedes campestris 23 Atelestidae  231 Atheas mimeticus  291 Athericidae  213, 231, 241, 715, 718, 720–721 Atherix  238 Atomyria 166 Atrichops  716, 721 Atta  21, 431 Attagenus  186 A. smirnovi 168 Attelabidae  122, 183, 342, 356, 387 Attevidae  472, 480 Auchenorrhyncha  3, 147, 160, 161, 168, 182, 184, 208, 243 Augustinus koreanus 162 Aulacidae  421, 425, 438 Aulacigastridae  233 Aulacobaris A. coerulescens  158

A. picitarsus  157 Aulacophora  368 Aulacorthum solani 632 Australimyzidae  233 Austroconops 120, 716, 721 Austrocynipidae  421, 439 Austroleptidae  231 Austroniidae  422, 425, 439 Austroperlidae 119 Austrosimulium 113 Autostichidae  472 Axymyia  235, 236 Axymyiidae  213, 229, 230, 240 Azaleodes 478 Azotidae  420

b Bactrocera 246 B. cucurbitae  100, 101, 659 B. dorsalis  100, 101 B. invadens  100, 101 B. latifrons  100, 102 B. oleae 102–103 B. orientalis 244 B. papayae  659 B. zonata  100, 101 Bagoinae 160 Bagous 161 Baizongia pistaciae 628 Balta similis 648 Barberiella formicoides 295 Baridinae  152, 157, 160, 162, 166 Barypeithes pellucidus 656 Batocera rufomaculata  366 Batrachedridae  472 Batrachomyia 245 Bedelliidae  472 Belidae  342, 356, 387 Bellardia  238 Belohinidae  338, 350 Belostoma  208, 289 B. flumineum  286 Belostomatidae 209, 281, 289 Belvosia 614 Belytinae 440 Belytonymidae (extinct)  424 Bemisia tabaci  540, 582, 660

827

828

Index

Benedictus 161 Berendtimiridae (extinct)  358 Berlandiana 299 Berninelsonius hyperboreus 392 Berytidae  283, 304 Bessa remota 251 Bethylidae  421, 424, 444 Bibio  235 Bibionidae  230, 240 Biliranoides 296 Billaea claripalpis 251 Biphyllidae  340, 353, 385 Biprorulus bibax 309 Biston betularia 18 Bittacomorpha  238 Bixadus sierricola  366 Blaesoxipha 606 Blaps 181 B. femoralis medusula  185 B. halophila  165 B. kashgarensis gobiensis  185 B. kiritshenkoi  185 B. miliaria  185 Blasticotomidae  420, 423, 437 Blastobasidae  472 Blatta orientalis 648 Blattodea (= Blattaria, = Blattoptera + Isoptera)  51, 77, 80, 121, 147, 148, 154, 184, 208, 212, 579, 581, 646 Blepharicera  238 Blephariceridae  119, 128, 213, 230, 234, 240, 241, 255 Blepharidopterus angulatus 296 Blepharipa scutellata 610 Blissidae  283, 304 Blissus leucopterus  298, 304 Blosyrus asellus  370 Boganiidae  340, 354 Boisea trivittata  298, 302 Bolbomyiidae  231 Bolitophagus reticulatus 167 Bolitophilidae  230

Boloria 173 Bombus  173, 582–583 B. terrestris  125, 666 Bombycidae  475, 485 Bombycoidea  475, 479, 485–486 Bombyliidae  231, 234, 242, 246–247 Bombyx mori  21, 23, 24, 485 Boreus 152 B. hyemalis  153 Boridae  342, 355, 387 Bostrichidae  160, 185, 186, 340, 352, 385, 394 Bothrideridae  341, 354, 386 Bothynoderes punctiventris  371 Bothynotus modesus  291 Brachinini 346 Brachodidae  473 Brachycaudus helichrysi 632 Brachycera  231, 234, 241–245 Brachyceridae  160, 183, 343, 387 Brachycerus,369 Brachyderini 168 Brachypsectridae  339, 385 Brachypterus urticae 392 Brachysomus echinatus 163–164 Brachystomatidae  231 Braconidae  148, 187, 421, 425, 438, 607, 608, 609, 611 Bradynobaenidae  422, 444 Bradysia B. coprophila 246 B. impatiens 246 Brahmaeidae  475, 485 Braulidae  234 Brentidae  168, 176, 177, 185, 187, 343, 356, 387 Brevicoryne brassicae 627 Brontispa longissima  367 Broscosoma 169 Broscus 168 Bruchela 157, 187 B. albosuturata  158

B. anatolica  157 B. concolor  158 B. exigua  158, 183 B. fortirostris  158 B. hesperidis  158 B. kasparyani  158 B. kaszabi 183 B. medvedevi  158 B. muscula  157 B. orientalis  157, 183 B. parvula  157 B. rufipes  157 B. schusteri  157 B. sugonyaevi  158 B. suturalis  157 B. verae  158 Bruchidius 182, 187 Bruchinae  159, 184, 187 Bruchophagus 605 Bruchus 182, 367 Bryocorinae 294 Bryocorini 294 Bucculatricidae  472 Buprestidae  81, 154, 160, 174, 185, 186, 339, 345, 350, 351, 378, 384, 394, 437, 508, 647 Buprestis B. rustica 176 B. strigosa 177 Byrrhidae  339, 351, 384 Byrrhobolus 171 Byrrhus (Aeneobyrrhus) 170 Byturidae 156, 340, 353, 385 Byturus 353

c Cactoblastis cactorum 11, 466, 668 Caenorhinus marginellus  369 Calamobius 160 Cales noacki  603, 615 Caliroa cerasi 648 Callichilella grandis 295 Callidiellum  365 Callidulidae  474, 484 Calliduloidea  479

Index

Calliphora 252 Calliphoridae 234, 234, 245, 248, 584 Callipogon relictus 178 Callirhipidae  339, 385 Callisthenes 180 Callosobruchus  367 Calomicrus pinicola 160 Caloparyphus  236 Calosoma  141, 180 C. sycophanta  149, 347 Calyptratae 245 Camillidae 155, 234 Camirus porosus  307 Campononotus nearcticus 295 Campsicnemus 256 Campylomma verbasci 296 Canacidae  213, 233, 255 Canopidae  283, 308 Canopus C. burmeisteri 308 C. fabricii 308 Cantacaderinae 297 Cantharidae  185, 186, 340, 351, 385 Canthonini  104, 105 Canthyloscelidae 155, 230 Capnia kolymensis 155 Capnodis carbonaria  149 Carabidae  50, 76, 80, 81, 83, 173, 184, 185, 186, 338, 343, 345, 346, 383, 390, 394, 646, 656 Carabus  164, 170, 176, 784 C. auronitens 163 C. lopatini  156 C. variolosus 163 Carausius morosus 19 Cardiophorus  186 Carebara 445 Caridae  342, 356 Carnidae  233 Carnus  716 Carpophilus obsoletus  364 Carposinidae  473, 479, 484 Carthaeidae  475, 485 Cartomothrips 654

Caryedon serratus  367 Caryoborus  187 Cassidini 152 Castniidae  473, 481 Catantopinae 184 Cathartus 354 Catiniidae (extinct)  358 Catomus mongolicus  185 Catopinae 167 Cattarus 305 Caulophilus oryzae  369 Cavognathidae  341, 354 Cecidomyiidae  120, 154, 230, 241, 246, 251 Cecidosidae  471 Cecidosiidae 478 Celyphidae  232 Centorus tibialis  165 Centraspis 299 Centris nitida 666 Cephalocattarus 305 Cephidae  420, 423, 437 Cerambycidae  152, 160, 174, 176, 185, 187, 342, 343, 345, 356, 387, 390, 394, 437, 647 Cerambyx cerdo  365 Ceraphronidae  420, 440 Ceraphronoidea 440 Ceratitis 246 C. capitata  100, 102, 244, 659 C. cosyra 102 C. fasciventris 102 C. rosa 102 Ceratocanthinae  81, 82 Ceratocapsus 296 C. modestus  291 Ceratocombidae  281, 285 Ceratocombius vagans  286 Ceratopogonidae 154, 212, 229, 230, 240, 241, 252, 714, 715, 718, 720, 721, 727, 733 Cercyon 168 Cerophytidae  339, 385 Cerotoma bifurcata  368 Cerylonidae  341, 354, 386

Ceutorhynchinae 142, 142, 152, 154, 157, 160, 162, 166, 183 Ceutorhynchus  157, 162, 170 C. cakilis 168 C. chalibaeus  157 C. cochleariae 163 C. hamiltoni 168 C. inaffectatus  158 C. isatidis  158 C. pervicax 163 C. potanini 163 C. sophiae  157 C. tesquorum 163 Chacoela 610 Chaetocnema 160, 368 Chaetosomatidae  340, 353 Chalcididae  420, 424, 611 Chalcidoidea  13, 55, 97, 120, 154, 440–443, 606, 607 Chalcodryidae  342 Chalcoela 606 Chalcolsiinae 488 Chamaemyiidae  232, 244, 251 Chamaepsila hennigi 244 Chaoboridae  212, 229, 230, 239, 240, 250 Chaoborus edulis 250 Chathamiidae 119 Chauliopinae 305 Chauliops 305 Cheirolasia burkei  362 Chelidinea vittiger 302 Chelinidea vittiger  298 Chelonariidae  339, 384 Chiastocheta 252 Chilacis typhae 303 Chilocorus kuwanae  364 Chiloloba acuta  362 Chilopoda 608 Chimarra 610 Chinaola quercicola 293 Chioneosoma 164 Chironomidae  19, 57, 119, 126, 155, 173, 210, 212, 229, 230, 239, 240, 241, 250, 255, 716

829

830

Index

Chironomus 255 Chlamydopsinae 348 Chlamysini  176, 177 Chloridolum  365 Chlorolestes umbratus  750 Chlorophorus  365 C. obliteratus  187 C. ubsanurensis  187 Chloropidae 229, 233, 244, 245, 250 Chlorops pumilionis 245 Chnootriba similis  364 Choreutidae  473 Choreutoidea  479, 480 Choristoneura  439, 481 Chrysididae  421, 424, 443 Chrysidoidea 443–444 Chrysis 443 Chrysobothris C. affinis 177 C. femorata  363 C. pulchripes 177 Chrysochraontini 154 Chrysolina  151, 163, 171, 176, 182 C. (Pezocrozita) 182 C. caviger 163 C. convexicollis 163 C. jakovlevi 163 C. sauanica 163 C. subsulcata 163 C. tuvensis 163 C. urjanchaica 163 Chrysomelidae  70, 152, 154, 160, 173, 181, 184, 185, 187, 210, 342, 343, 345, 356, 361, 387, 390 Chrysomelinae  119, 151, 170 Chrysomeloidea  342 Chrysomphalus aonidum 613 Chrysomya 252 C. bezziana 249 C. rufifacies 656 Chrysopidae  18, 98 Chrysops  23, 725 Chyromyidae  233

Cicadellidae  54, 152, 209, 296, 444, 482, 539, 647 Cicadetta montana 539 Cicadidae  122, 177, 539 Cicindela  169, 663, 784 Ciidae 167, 342, 355, 386 Cimberis attelaboides  156 Cimbicidae  420, 423, 437 Cimeliidae  474 Cimex lectularius  291, 646, 648 Cimicidae  282, 292, 312 Cimicomorpha  209–301, 312 Cinara 633 Cionus zonovi  151 Cirrospilus 611 Cladotanytarsus lewisi 250 Clambidae  339, 384 Clavicornaltica 161 C. dali  153 Clavigralla gibbosa 302 Cleradini  306, 312 Cleridae 76, 81, 186, 340, 353, 380, 385 Cleroidea  394 Climacia areolaris 209 Clivinematini 294 Closterocerus utahensis 611 Clusiidae  233, 244 Clytrini  152, 182 Cneoglossidae  339 Cnestus mutilatus  374 Cobboldia russanovi 256 Coccina 154 Coccinella  187 C. septempunctata 664 Coccinellidae  173, 187, 341, 345, 355, 386 Coccoidea  119, 154, 295, 391, 482, 646, 647 Coccotrypes subcribrosus  374 Cochliomyia hominivorax  249, 657 Coelaenomenodera elaeidis  367 Coeliodes 162 Coelopidae  213, 232

Coelostomidiidae 125 Coenosia 251 Coleomegilla maculata  364 Coleophoridae  472, 481 Coleoptera 2, 3, 10, 12, 52, 56, 57, 59, 66–84, 70, 78, 80, 82, 84, 100, 117, 118, 119, 126, 147, 154, 173, 180, 206, 210, 212, 337–395 (chapter 11), 579, 582–583, 605, 606, 607, 609, 646, 650, 785 Coleorrhyncha 279 Coleotichus blackburniae 668 Colias 173 Collembola  3, 10, 69, 558, 578, 579 Colletidae  420, 423 Colletinae 120 Colobathristidae  283, 304 Colymbetinae 381 Colymbotethidae (extinct)  358 Compsilura concinnata 251, 466, 608, 668 Comptosoma 309 Conaliini  82, 83 Coniatus C. minutus  151 C. zaslavskii  151 Conoderinae 153 Conoderus rufangulus  364 Conoesucidae 119 Conophymatini 154 Conopidae  232, 244 Conorhynchus pulverulentus 150 Conotrachelus  372 Copelatinae 347 Copitarsia 671 Coprini 104 Coprinisphaeridae (extinct)  358 Copris 167 Copromorphidae  473, 484 Coptoclavidae (extinct)  358 Coptotermes formosanus  659

Index

Copturus aguacatae  369 Coquillettidia 240 Cordulephyidae 119 Cordylomera torrida  365 Coreidae  283, 302, 312 Coreinae 302 Coreoidea 301–303 Corethrellidae  212, 230, 715, 718, 721, 727 Coridromius 296 Corimalia reaumuriae  151 Corimelaena pulicaria  307 Corimelaeninae 310 Corixidae 209, 281, 288, 653 Corixidea major 312 Coroebina 180 Corylophidae  341, 354, 386 Corythucha C. ciliata  291, 297 C. gossypii 297 Coscinocera hercules 114 Cosmobaris scolopacea  151 Cosmopolites sordidus  369 Cosmopsaltriina 122 Cosmopterigidae  472, 480 Cossidae  473, 481 Cossoidea  473, 479, 481 Cossonus 161 Cossyphus tauricus  165 Costelytra zealandica  363 Cotesia melitaearum 614 Cotinus mutabilis 380 Crabronidae  420, 423, 446 Crambidae  474 Crambinae 484 Craspedonotus tibialis 168 Crioceris  368 Crosita 171 Crossotarsus  372 Crowsoniellidae  338, 345 Cryphalus latus  374 Crypticus quisquilius  165 Cryptocephalinae  151, 160, 170, 184 Cryptocephalini 152 Cryptocephalus  160, 182 C. duplicatus  149

C. ochroloma  153 C. pini 160 C. quadripustulatus 160 Cryptochetidae (= Cryptochaetidae) 155, 234, 603 Cryptochetum iceryae 250– 251, 603, 606 Cryptococcus fagisuga 660 Cryptolestes 354, 364 Cryptophagidae  157, 187, 341, 354, 386 Cryptorhamphidae  283, 304 Cryptorhynchus C. lapathi 175 C. mangiferae  370 Cryptostemma uhleri  286 Cryptoxyleborus subnaevus  374 Crypturgus cinereus  374 Ctenocephalides felis 584 Ctenostylidae  232 Cucujidae 186, 341, 354, 386, 394 Culex  235, 247 C. molestus 732 C. pipiens 732 C. quinquefasciatus 660 Culicidae  22, 55, 154, 166, 212, 218, 229, 230, 240, 255, 299, 584, 646, 714, 715, 718, 720, 721–722, 727 Culicoidea  230 Culicoides 250, 716, 717, 721, 733 C. imicola [complex]  730 C. variipennis  728, 729 C. sonorensis 729 Cupedidae 175, 338, 345, 383 Curaliidae 292 Curalium cronini 292 Curculio  162, 177, 370 Curculionidae  55, 152, 154, 173, 181, 182, 185, 187, 343, 343, 345, 357, 361, 387, 394 Curculioninae 183

Curculionoidea 356–357 Curtonotidae  234 Cuterebrinae  245, 248 Cybocephalidae  186, 354 Cychrini 346 Cyclaxyridae  341, 354 Cyclominae 153 Cyclorhipidion sexspinatum  374 Cyclotornidae  473, 482 Cydia pomonella  481, 648, 652, 659 Cydnidae  283, 308 Cylapinae 294 Cylapus 293 C. tenuis 294 Cylas  369 Cylindromorphus 160, 182, 186 Cylindrotomidae  230 Cyllodes ater 167 Cymidae 304 Cynipencyrtidae  420 Cynipidae  421, 424, 439 Cynipoidea  439, 606, 607 Cyphogenia intermedia  185 Cyphon 393 Cyphosoma 160 C. euphraticum  149 Cyphosthete mongolica  185 Cypselosomatidae  232 Cyrtocoridae  283, 308 Cyrtopeltocoris illini  291 Cyzenis albicans 251

d Dacillus elongatus 156 Dactylopius coccus  24, 787 Dactylotus globosus 170 Dacus 246 D. bivittatus 102 D. ciliatus 102 D. frontalis 102 D. vertebratus 102 Daktulosphaira vitifoliae  656, 658 Dalceridae 57, 473, 482

831

832

Index

Dalyat 346 Danainae 483 Danaus plexippus  25, 483 Daohugoidae (extinct)  423 Darinwinivelia fosteri  286 Dascillidae  339, 384 Dascilloidea 352 Dascillus cervinus 156 Dasyomma  716, 721 Dasytinae  181, 186, 353 Declinia relicta 178 Decliniidae  339 Dectes texanus  366 Deinacrida heteracantha 113 Delphacidae 539 Dendarus punctatus  165 Dendroctonus  374 D. frontalis 359 D. micans 360 D. ponderosae  13, 360, 361 D. valens 360 Dendrolimus pini 176 Depressariidae  472 Deracanthinae 154 Deracanthus faldermanni  151 Deraeocorinae 294 Deraeocoris 295 D. nebulosus 295 Dericorythini 184 Dermaptera  3, 51, 55, 147, 148, 154, 184, 206, 208, 578, 579 Dermatobia hominis  237, 248 Dermestes  167, 186, 359 D. lardarius 379 Dermestidae  186, 187, 340, 352, 380, 385 Derodontidae  340, 351, 385 Desmiphora hirticollis  366 Desmobathrinae 486 Deuterophlebia  236 Deuterophlebiidae  213, 230, 234, 240, 255 Diabrotica  368 D. virgifera  368, 642, 652 Diaclina testudinea  165

Diadocidiidae  230 Diapheromera femorata 300 Diaprepes  370 Diapriidae  421, 425, 440 Diaprioidea 439 Diapus  372 Diaspidiosus perniciosus  656, 658 Diastatidae  234 Diatraea 251 Dicerca furcata 176 Dichotomiini  104, 105 Dichotrachelus 177 Dicladispa  367 Dicopomorpha echmepterygis  429, 442 Dicranocephalus D. bianchii 303 D. insularis  298, 303 Dictyoptera aurora 391 “Dictyoptera” (see also Blattodea, Mantodea, Phasmatodea)  609 Dicyphini 294 Dicyphus agilis  291 Diexini 184 Dilamus mongolicus  185 Diloboderus abderus  362 Dinidoridae 308 Dinoderus 352 Dinodoridae  283 Dinoplatypus  372 Dinoponera 445 Diocalandra  369 Diopsidae  232, 244 Dioptinae 465 Dioryctria abietella 176 Diphlebiidae 119 Diphyllostomatidae 49, 339, 350, 384, 390 Diplazontinae 439 Diplopoda  346, 608 Diplura  3, 558, 578, 579 Diprionidae  420, 423, 437 Dipsocoridae  208, 285 Dipsocoromorpha  285–287, 312

Diptera 2, 3, 52, 55, 57, 69, 78, 79, 80, 97, 103, 117, 122, 126, 146, 154, 173, 179, 206, 211, 229–257 (chapter 9), 579, 584, 605, 606, 607, 609, 646, 650, 713–734 (chapter 22) Discolomatidae  341, 354 Distantiella theobroma  293, 294 Disteniidae  342, 356 Ditomyiidae  230 Diuraphis noxia  615, 633, 659, 659, 664 Dixidae  212, 230, 240 Doidae 469, 474 Dolichopodidae 122, 213, 231, 242, 255 Dolomedes 209 Dolurgus pumilus  374 Donacia  166, 210 Donaciinae 160 Dorcadion  152, 160, 180, 182, 356 Dorcatominae 167 Dorylus  431, 445 Dorytomus  166, 174, 176 Douglasiidae  472 Drasterius  186 Drepanidae  474 Drepanocerina 105 Drepanoidea 469, 474, 479 Drilini  340, 351 Drosophila  16–18, 23, 253–254, 256, 555 D. melanogaster  16–17, 20, 244, 506, 657 D. subobscura 657 Drosophilidae  234, 244 Drusus annulatus 218 Dryadaulidae  471, 478 Dryinidae  421, 424, 444 Drymadusini 154 Drymini 306 Dryococelus australis  113, 114 Dryocoetes  374

Index

D. autographus 391–392 Dryomyzidae  213, 232 Dryophthoridae  153, 160, 176, 182, 343, 387 Dryopidae  186, 210, 339, 384 Dudgeoneidae  473 Dundubiina 122 Dysdercus 311 D. lunulatus  307 Dytiscidae  119, 173, 186, 338, 347, 383, 394

e

Eccoptopterus spinosus  374 Eccritotarsini 294 Eccritotarsus 294 Echinophthiriidae 209 Eciton 431 E. burchellii 432 Ectrichodiinae 299 Edessa florida  307 Egnatiini 184 Elachistidae  472, 480 Elateridae  81, 173, 186, 339, 345, 351, 378, 385, 390, 394 Electrotomidae (extinct)  423 Elmidae 210, 339, 351, 384, 394 Elodophthalmidae (extinct)  358 Elytroteinus subtruncatus  370 Embiodea (= Embiidina, = Embioptera)  51, 118, 147, 292, 579, 581, 654 Embiophilinae 292 Embolemidae  421, 424, 442 Emesaya 299 Emesinae 299 Emmepus  186 Emperoptera 256 Empicoris 299 Empididae 119, 213, 231, 234, 239, 242 Empidinae 242 Empidoidea 242 Empis  235

Enaphalodes rufulus  365 Encarsia  614, 616 E. sophia 614 Enchenopa binotata 539 Encyclops caerulea  367 Encyrtidae  420, 424, 608, 609, 611 Endecatomidae  340, 352, 385 Endelus 161 Endomychidae 167, 341, 354, 386 Endromidae  475, 485 Enicocephalidae  281, 285 Enicocephalomorpha 312 Enicospilus 431 Ennominae 487 Ensifera 184 Entiminae  81, 82, 152, 158, 177, 183 Eodorcadion  160, 180 E. kozlovi  187 Eostephanitidae (extinct)  426 Epermeniidae  473 Epermenioidea  479 Ephemeroptera  3, 10, 51, 69, 93, 147, 155, 173, 206, 212, 516, 579, 580 Ephestia elutella 484 Ephialtitidae (extinct)  425 Ephydridae  213, 229, 234, 244, 245, 255 Epicopeiidae  475, 486, 488 Epilachna  364 Epilachninae 355 Epimetopinae 348 Epiophlebiidae 179 Epiphragma  236 Epiphyas postvittana 481 Epipyropidae  473, 482, 610 Episyrphus balteatus 243 Epitrichia intermedia  185 Epitrix 161, 368 Epuraea  167, 177 Epyrini 444 Erebia 173 Erebidae  475

Eremochorus E. inflatus  151 E. mongolicus  151 E. sinuatocollis 163 E. zaslavskii 163 Eremoxenus chan 168 Eriaporidae  420 Eriocottidae  471, 478 Eriocraniidae  470, 477 Eriocranioidea  476 Eriosoma lanigerum 634 Erirhininae  160, 173, 183 Eristalis 255 E. tenax  149 Erotylidae  81, 82, 167, 340, 354, 385, 394 Esperanza texana 301 Eucharitidae  421, 424, 440 Eucinetidae  339, 384 Eucnemidae  339, 385, 394 Eucraniini 104 Euholognatha 155 Eulichadidae  339, 384 Eulophidae  421, 424, 608, 609 Eumenes 445 Eumeninae  120, 445 Eumilada punctifera amaroides  185 Eumolpinae  152, 170, 184 Euops 122 Eupelmidae  421, 424, 611 Euplatypus  373 Euproctis chrysorrhoea 466 Eupsilobiidae 354 Eupterotidae  475, 485 Eurosta  236 Eurycnema goliath 114 Eurygaster integriceps 310 Eurygnathomyiidae 148 Euryphagus lundi  365 Eurysternini 104 Eurythyrea E. aurata 177 E. eoa 177 Eurytomidae  421, 424, 440, 611 Euscepes postfasciatus  370 Euschistus 309

833

834

Index

Eustheniidae 119 Euteliidae  475, 488 Eutrichapion viciae 392 Euwallacea  375 Euxestidae 354 Euxoa auxiliaris 11 Evaniidae  421, 425, 438 Evanioidea 437–438 Evocoidae  231 Exenterini 155 Exomala orientalis  363 Exoporia 478 Exosoma lusitanicum  368

f

Falsiformicidae (extinct)  424 Fanniidae  234, 245, 253 Feltiella acarisuga 250 Fergusonina turneri 237 Fergusoninidae 120, 233 Fidena 242 Figitidae  421, 424, 439 Fijipsalta 122 Forcipomyia  252, 253, 788 F. (Lasiohelea)  716, 721 Formica subsericea 295 Formicidae  11, 12, 21, 79, 111, 120, 122, 123, 124, 128, 173, 245, 295, 349, 422, 425, 445–446, 465, 483, 577, 605, 646, 665–666, 716 Formicomus  187 Frankliniella occidentalis 660 Fremuthiella vossi  151 Fulgoroidea 482 Fulvius 294 F. imbecilis  291

g

Galacticidae  473 Galacticoidea  479 Galeruca rufa 159 Galerucella 668 Galerucinae  151, 170 Galleria melonella 484 Gallorommatidae (extinct)  425

Gampsocleidini 154 Gampsocorinae 304 Gargaphia 297 Gasterophilinae  245, 248 Gasterophilus 237 G. intestinalis 19 Gasteruptiidae  421, 438 Gastrophysa 166 Gedoelstia 249 Gelastocoridae  281, 289 Gelastocoris oculatus  286 Gelechiidae  472, 480 Gelechioidea 469, 472, 479, 480 Geniocremnus chilensis  370 Genyocerus  373 Geocoridae  283, 304–305, 312 Geocorinae 305 Geocoris punctipes  298 Geometridae 173, 475, 486–487 Geometrinae 487 Geometroidea  475, 479, 486–487 Georyssidae  186 Geotrupes inermis 171 Geotrupidae 12, 338, 350, 361, 383, 383 Gerocynipidae (extinct)  424 Gerridae 209, 281, 287 Gerris marginatus  286 Gerromorpha  287–288, 312 Gigantometopus rossi 295 Gigantometra gigas 287 Glaphyridae  339, 350, 384 Glaphyrus 181 Glaresidae  339, 350, 384 Glossina  13–14, 728 Glossinidae  154, 234, 234, 245, 718, 722–723, 727 Glossosomatidae 211 Glyphipterigidae  472, 480 Glyphonotinae 154 Glypostenoda  82 Glyptocombus saltator  286 Gnathotrichus  375 Gobryidae  232

Goeldichironomus amazonicus 653 Golofa eacus  362 Gonatocerus 615 G. ashmeadi 617 Gonimbrasia belina  93, 486 Gonioctena fornicata  367 Goniops  716, 725 Gonipterus  370 Gonocephalum granulatum  165 Gracillariidae  472, 479, 610 Gracillarioidea  471, 479, 479 Grallipeza  235 Graptocleptes 300 Gratiana spadicea 380 Gripopterygidae 119 Gronops semenovi  151 Gryllidae 18, 77 Grylloblattodea (= Notoptera– Grylloblattodea)  3, 51, 57, 95, 118, 147, 579, 581 Grylloidea 177 Gryllotalpidae  646 Grypus 161 Gymnopleurini 104 Gynaikothrips ficorum 656 Gyrinidae  186, 338, 347, 380, 383 Gyrostigma G. rhinocerontis 256 G. sumatrensis 256

h Habroloma 182 Haematobia H. exigua 248 H. irritans  248, 660, 723 Haematopinus oliveri 748 Halictidae  420, 423 Halictinae 120 Haliplidae  186, 338, 383 Hallodapini 296 Halobates 209 Halticini 296 Halticotoma valida 294 Halticus bractatus 296

Index

Harmonia axyridis  141, 355, 364, 664 Harpactorinae 299 Harpalini 346 Hebridae  281, 287 Hebrus concinnus  286 Hedylidae  474, 482 Heilipus lauri  372 Helcomyzidae  232 Heleomyzidae  213, 233 Heliconiinae 483 Heliconius  465, 483 Helicophidae 119 Helicoverpa 487 Helictopleurina 105 Heliocosma 481 Heliodinidae  472 Heliozelidae  471, 478 Helodidae  157, 186 Helopeltis 293 Helophoridae  186 Helophorinae 348 Helophorus lapponicus 148 Heloridae  422, 425, 439 Helosciomyzidae  232 Helotidae 175, 340, 354 Helotrephidae  281, 289 Hemerobiidae 184 Hemipeplus 355 Hemiphlebia mirabilis 128 Hemiphlebiidae 119 Hemiptera  3, 11, 51, 69, 117, 119, 122, 147, 208, 279–313 (chapter 10), 579, 582, 646, 647, 650, 785–786 Hemipyrellia  235 Hemitrichapion reflexum 163 Henicocoridae  283, 303 Henosepilachna  364 Hepialidae  470, 477 Hepialoidea  469, 470, 476, 477 Herdoniini  294, 295 Hermatobatidae  281, 287 Hermetia illucens 252 Hesperiidae  474, 482 Hesperinidae  230

Hesperoctenes H. eumops  291 H. campestris  365 Hetaeriinae 348 Heterobathmiidae  470 Heterobathmioidea  476, 477 Heterobostrychus aequalis  364 Heteroceridae  186, 339, 384 Heterocheilidae  213, 233 Heterogastridae  283, 305 Heterogynaeidae 446 Heterogynaidae  420 Heterogynidae  473 Heteromyzidae  233 Heteronemiidae 300 Heteroneura 477 Heteronychus arator  362 Heteropsylla cubana 654 Heteroptera  3, 54, 77, 80, 147, 168, 184, 212, 279–313 (chapter 10), 609, 646 Heterospilus 427 Heterostylum robustum 247 Heterotoma planicorne 296 Hilarimorphidae  231 Himalusa 349 Himantopteridae  474 Hippelates 250 Hippoboscidae 154, 234, 245, 715, 716, 718, 720, 723 Hippoboscoidea  229, 237 Hippuriphila 161 Hispini  81, 160 Histeridae  167, 168, 186, 338, 348, 380, 383, 383–390 Hobartiidae  341, 354 Holcocranum saturejae 303 Holotrichia  363 Homalocnemidae  231 Homalodisca H. coagulata  20, 642, 664–665 H. vitripennis 617 Homomorpha cruciata  187 Homoptera  77, 80 Hoplia praticola 163 Hoplinus 304

Horaia  236 Huttoninidae  233 Hyalochloria 296 Hyalopeplini 295 Hyalopeplus pellucidus 295 Hyblaeidae  474, 484 Hyblaeoidea  474, 479, 484 Hybosoridae  339, 350, 384 Hybotidae  231 Hydraenidae  186, 210, 338, 348, 383 Hydrobiosidae 119 Hydrobius fuscipes 380 Hydrochinae 348 Hydrometra martini  286 Hydrometridae  281, 288 Hydrophilidae 167, 186, 338, 347, 348, 383 Hydrophiloidea 347–348 Hydrophilus 141 Hydroporinae 347 Hydroptilidae 211 Hydroscaphidae 57, 338, 346, 383 Hydrotaea irritans 248 Hygrobiidae  338, 347 Hylastes ater  375 Hylesinus  375 Hylobius 161, 372 Hylotrupes bajulus  365 Hylurgopinus rufipes  375 Hylurgops  375 Hylurgus ligniperda  375 Hymenoptera 2, 3, 50, 52, 54, 56, 69, 78, 80, 117, 120, 125, 147, 154, 155, 173, 206, 209, 212, 419–445 (chapter 12), 512, 579, 582–583, 606, 607, 608, 609 Hyocephalidae  283, 302–303 Hypera postica  371, 659 Hyperaspis  187 Hyperinae  152, 153, 170 Hyperoscelis 155 Hyphantria cunea 670 Hypocassida 159

835

836

Index

Hypoderma  237, 249 H. bovis 248 Hypodermatinae 245 Hypohypurini 154 Hypolestidae 119 Hypolixus truncatulus  371 Hypomeces squamosus  371 Hyposmocoma 481 Hypothenemus hampei  375 Hypsipterygidae  281, 287 Hyptiogastrinae 438

i

Ibaliidae  421, 424, 439 Icerya purchasi  11, 251, 606, 664 Ichneumonidae  55, 155, 421, 425, 438–439, 607, 608, 609, 612 Ichneumonoidea  606, 613 Idiostolidae  283, 303 Immidae  473 Immoidea  479, 484 Inbiomyiidae  233 Incurvariidae  471, 478 Inopeplidae 175 Integripalpia 211 Ips 176, 375 I. typographus  359, 360 Iranellini 184 Ironomyia 243 Ironomyiidae  232 Ischaliidae 175 Ischnopterapion I. loti 392 I. virens  369 Iscopinidae (extinct)  425 Ismaridae  421, 439 Isometopinae 295 Isonycholips gotoi 168 Iteaphila group  231 Ithomiini 483 Ivalia 161 Ixodes scapularis 12

j

Jacobsoniidae  340, 348, 351, 385

Jadera haematoloma 312 Jaxartiolus 166 Joppeicidae  282, 292 Joppeicus paradoxus 292 Julodella 180 J. abeillei  150 Julodis 180 J. variolaris  150 Jurapriidae (extinct)  425 Jurodidae (including Sikhotealiniidae)  338, 345

k Kalama tricornis 654 Karatavitidae (extinct)  423 Kateretidae  341, 354, 386 Keroplatidae  230, 239 Keroplatus 239 Kerria lacca 24 Khutelchalcididae (extinct)  426 Kikihia 122 K. convicta 121 Kikiki huna  430 Kiskeya 161 K. baorucae  153 Kleidocerys resedae 305 Kokiriidae 119 Kuafuidae (extinct)  426 Kytorhinoides thermopsis  182 Kytorhinus K. kergoati 182 K. pectinicornis 182

l Labradorocoleidae (extinct)  358 Lacturidae  473 Laemophloeidae  386 Laemophloeidae (including Propalticidae)  341, 354 Laena starcki  165 Lagocheirus araneiformis  366 Lamia textor 175 Lamingtoniidae  341, 354

Lamprodila L. amurensis 177 L. rutilans 177 Lamprosominae 177 Lampyridae 177, 340, 351, 381, 385 Larentiinae 487 Largidae  283, 311 Larginae 311 Largus 311 L. succinctus  307 Laricobius 351 Larinus planus 668 Lasciocampidae 486 Lasiocampidae  474 Lasiocampoidea  479 Lasiochilidae  282, 292 Lasiochilus 292 Lasioderma 168 L. serricorne 352 Lasiosynidae (extinct)  358 Lasius neoniger 295 Latridiidae 157, 341, 354, 386 Lauxaniidae  232, 244 Lebiinae 346 Lecithoceridae  472, 480, 481 Leichenum pictum  165 Leiodidae  167, 185, 186, 338, 349, 383, 394 Lema decempunctata 161 Lepiceridae  338, 346 Lepicerus inaequalis  344 Lepidonotaris petax 183 Lepidoptera 2, 3, 11, 16, 20, 21, 52, 69, 70, 78, 80, 117, 118, 120, 127, 146, 154, 155, 175, 179, 181, 206, 211, 212, 295, 463–489 (chapter 13), 578, 579, 582, 583, 606, 607, 646, 650 Lepidosaphes ulmi 648 Lepidotrichidae 512 Leptinotarsa decemlineata  367, 381, 652 Leptoconops  716, 721 Leptocorisinae 301

Index

Leptodirus 349 Leptoglossus phyllopus  298, 302 Leptophlebiidae 119 Leptopodidae  282, 290 Leptopodomorpha 209, 290, 312 Leptopterna dolabrata  291, 295 Lepyrus 170 Lestonia haustorifera 308 Lestoniidae  283, 308 Lethaeini 306 Leucopholis  363 Leucophoropterini 296 Leucopis tapiae 251 Leucospidae  421, 424 Leuctridae 207 Liadytidae (extinct)  358 Libyaspis 309 Libytheinae 483 Lilioceris lilii  368 Limacodidae  474, 482 Limenitidinae 484 Limnephilus lunatus 218 Limnichidae  339, 384 Limnobaris 160 Limoniidae  230 Limonius californicus  364 Linepithema humile  125, 419, 429, 665 Liopteridae  421, 425, 439 Liotrigona 582–583 Lioxyonychini 154 Lipsothrix 240 Liriomyza L. brassicae 246 L. huidobrensis 246 L. sativae 246 L. trifolii 246 Lissorhoptrus L. oryzophilus 218 L. oryzophilus  369 Listroderes  370 Listronotus  370 Livilla variegata 664 Lixinae  152, 153, 162, 166, 183

Lixophaga diatraeae 251 Lixus  157, 161 L. incanescens  151 L. juncii  371 Lobesia botrana 481 Loboscelidiinae 443 Lonchaeidae  232 Lonchoptera bifurcata 243 Lonchopteridae  213, 232, 243 Longitarsus  152, 157, 159, 170, 179 Lophocoronidae  470, 477 Lophocoronoidea  476 Lophoscutus 300 Lopidea davisi 296 Lucanidae  339, 350, 384, 394 Lucilia  236 L. cuprina 249, 659, 660 Luperomorpha xanthodera  368 Luperus longicornis 160 Lutrochidae  339, 384 Lutzomyia 724 L. longipalpis 728 Lycaenidae 173, 474, 483 Lycidae  340, 385 Lyctocoridae  282, 292 Lyctocoris 292 L. campestris  291 Lyctus 352 Lydella minense 251 Lygaeidae  283, 305 Lygaeinae 305 Lygaeoidea 303–306, 312, 646 Lygaeus 305 L. kalmii  298 Lygistorrhinidae  230 Lygus  293, 295 Lymantria L. dispar  11, 466, 647 L. monacha 176, 647 Lymantriinae  173, 487 Lymexylidae  340, 352–353, 385 Lyonetiidae  472, 480 Lypusidae  472

Lyrosoma 168 Lytta vesicatoria 379

m

Maamingidae  421, 440 Maconellicoccus hirsutus  659 Macrolepidoptera 123 Macrolophus melanotoma 294 Macropogon pubescens 156 Macrosiagon  187 Macrosiphum rosae  629 Macrotarrhus kiritshenkoi  151 Macroveliidae  281, 287 Madurasia obscurella  368 Magdalini 177 Magdalis 174 Magnocoleidae (extinct)  358 Maimetshidae (extinct)  425 Malachiinae  181, 353 Malacosoma 486 M. disstria 250 Maladera castanea  363 Malaya  716 Malcidae  284, 305 Malcinae 305 Mallochiola gagates 293 Mallosia armeniaca  150 Manduca M. quinquemaculata 486 M. sexta  486, 506 Manidiidae 57 Manobia 161 Mansonia 240 Mantispidae  184, 610 Mantispinae 606 Mantodea  3, 51, 56, 77, 80, 147, 148, 154, 184, 579, 581 Mantophasmatodea (= Notoptera– Mantophasmatodea)  3, 95, 118, 512, 579, 581 Maoricicada 122 Margarinotus kurbatovi  153 Marginidae  233 Masarinae 445 Mastotermes darwiniensis 120

837

838

Index

Mauroniscidae  340, 353 Mayetiola destructor  644, 648, 657, 659, 713 Mecistoscelini 295 Mecoptera  3, 52, 120, 147, 155, 184, 210, 212, 579, 584 Mecysmoderes  157, 176 Mecysolobini 176 Medocostes lestoni 297 Medocostidae  282, 297 Medythia quaterna  368 Meessiidae  471, 478 Megabruchidius M. dorsalis  172, 182 M. tonkineus  172, 182 Megachile rotundata 656 Megachilidae  420, 423 Megacopta cribraria 309 Megalodontesidae  420, 423, 437 Megalopodidae  342, 356, 387 Megalopodinae  176, 177 Megaloptera  3, 51, 56, 97, 103, 147, 155, 184, 209, 212, 579, 583 Megalopygidae  474, 482 Megalyridae  422, 425, 437 Megamerinidae 155, 233 Megaplatypus mutatus  373 Megarhyssa M. atrata 438 M. gloriosa 438 Megarididae  284, 309 Megaselia  243, 608 M. scalaris 247 Megaspilidae  420, 424, 440 Megastigmus 605, 647 M. transvaalensis 617 Melaloncha  247, 608 Melandryidae  342, 355, 376 Melanesthes 181 M. czikii  185 M. heydeni  185 Melanimon tibialis  165 Melanobaris 157 M. atramentaria  157

M. gloriae  158 M. hochhuthi  157 M. nigritarsis  157, 158 Melanophila fulvoguttata  363 Melanotrichus virescens 296 Melanotus communis  364 Meligethes 177 M. aeneus  364 Melittidae  420, 423 Melittomma insulare  364 Mellitosphecidae (extinct)  424 Meloidae  187, 342, 355, 357–359, 378, 387 Melolontha  363 Melophagus ovinus 723 Melyridae  340, 345, 353, 385 Membracidae 539 Mengenillidae  605, 610 Menoponidae 209 Meromyza americana 245 Meruidae  338, 347 Meschiidae  284, 305 Mesembrinellinae  229, 237 Mesocinetidae (extinct)  358 Mesoplatys cincta  367 Mesoptiliinae 183 Mesoserphidae (extinct)  425 Mesovelia mulsanti  286 Mesoveliidae  281, 288 Messor barbarus 445 Metacanthinae 304 Metacanthus annulosus 304 Metacnemis valida  748 Metamasius  369 M. callizona 664 Metarbelidae  473 Metaxina ornata 353 Metaxinidae  340, 353 Metcalfa pruinosa  141, 655 Metopia  238 Microacmaeodera 180 Microcerella bermuda 256 Microcoryphia (= Archaeognatha)  3, 51, 147, 580 Microdera kraatzi  185 Microgastrinae  438, 786

Micromalthidae  338, 345, 383 Micromalthus debilis 346, 381, 507 Micropezidae  232, 234 Microphysidae  282, 293 Micropterigidae  470, 477 Micropterigoidea  476 Micropterygidae 122 Microsania 242 Microstigmus 443 Microtheca ochroloma  367 Microtomus purcis  298 Microvelia ashlocki  286 Milichiidae  233 Millieriidae  471, 478 Miltogramminae  229, 245 Mimallonidae 469, 474 Mimallonoidea  479 Miquihuana 346 Miridae  282, 293–296, 311, 312, 664 Mirinae 295 Mirini 295 Mitrastethus baridioides  370 Mnesarchaeidae 477 Mnesarchaeoidea 470 Mniophila muscorum  153, 161 Moegistorhynchus longirostris 242 Momphidae  472 Monalocoris 294 Monarthrum  376 Monatrum prescotti  185 Mongolocleonus gobianus  151 Monochamus  366 Monoloniini 294 Monomachidae  421, 440 Monomminae 175 Mononychini 160 Mononychus punctumalbum 161 Monotomidae  341, 354, 385 Montandoniola moraguesi 656 Mordella  82 Mordellidae 80–82, 81, 82, 83, 187, 342, 355, 386 Mordellini  82, 83

Index

Mordellistena  82 Mordellistenini 82 Morellistena  187 Mormotomyia hirsuta 256 Mormotomyiidae  233 Morpho  24, 508 Murgantia histrionica  307 Murmidiidae 354 Musca M. autumnalis  248, 714 M. crassirostris  716, 723 M. domestica  16, 250, 348, 646, 648, 714 M. sorbens 248 M. vetustissima 112, 249, 789 Muscidae  213, 229, 234, 245, 253, 715, 719, 723 Musgraveia 310 Mutillidae  422, 425, 444 Mycetaeidae 354 Mycetophagidae  341, 355, 386, 394 Mycetophilidae  79, 154, 230, 241 Mycteridae  342, 355, 387 Mycteromyiini  716, 725 Mycterus curculionoides 157 Mydidae  231 Mymaridae  421, 424, 442, 616 Mymarommatidae  422, 425, 437 Myodocha serripes  298 Myodochini 306 “Myoglossata” 477 Myraboliidae  341, 354 Myriapoda  69 Myriophora 608 Myrmeciinae 120 Myrmecocystus 113 Myrmecophyes oregonensis 296 Myrmeleontidae 184 Mystacinobiidae  234 Myxophaga 345–346 Myzus M. antirrhinii 633 M. persicae 632

n

Nabidae  282, 297, 312 Nabis americoferus  291 Nacerdes melanura 355 Nalassus 164 N. faldermanni  165 Nannochoristidae  120, 210 Nannodastiidae  233 Nanophyidae 182 Nasonia 431 N. vitripennis 614 Nastus 161 Nasutitermes 300 Natalimyzidae  233 Naucoridae 209, 282, 288 Naupactus  371 Nausibius 354 Nebria 170 Necatapion bruleriei 159 Necrobia  167, 186 N. rufipes  186 Necrophorus argutor 185 Nematinae  70 “Nematocera” 239–241 Nemestrinidae  231, 234, 242 Neminidae  233 Nemonychidae 182, 342, 356, 387 Nemoptera sinuata  149 Nemopteridae  104, 184 Nemoria 487 Nemoura 155 Nemouridae 207 Neochetina N. bruchi 217 N. eichhorniae 217 Neodusmetia sangwani 603 “Neolepidoptera” 477 Neophytobius 170 Neoplatygaster venustus 162 Neoplea striola  286 Neopseustidae  470 Neopseustoidea 470, 476 Nepa apiculata  286 Nephrocerus 243 Nepidae 209, 282, 289 Nepomorpha  288–290, 312

Nepticulidae  471 Nepticuloidea  476, 478 Neriidae  232 Nerthra 289 Nesameletidae 119 Nesotes 381 Neurochaetidae  233 Neuroptera  3, 51, 97, 103, 209, 212, 579, 583, 606, 607 Neurorthus 209 Nezara viridula  309, 312, 668, 670 Nicrophorus 349 N. americanus 53 Niesthrea louisianica 302 Nilaparvata lugens 13, 537, 539 Ninidae  284, 305 Nipponobuprestis 180 Nitidulidae  167, 185, 186, 341, 354, 386 Noctuidae (see also Erebidae) 173, 475, 487–488 Noctuoidea 469, 475, 479, 487–488, 583 Nolidae  475, 488 Nosodendridae  340, 351, 385 Notaris 170 N. dauricus 183 Noteridae  338, 347, 383 Nothybidae  232 Notodontidae  475, 487 Notonecta undulata  286 Notonectidae  282, 289 Notonemouridae 155 Notoptera. See Grylloblattodea; Mantophasmatodea Notostira elongata 295 Notoxus  187 Nycteribiinae 245 Nymphalidae 114, 474, 483 Nymphalinae 483 Nymphomyia  236, 238 Nymphomyiidae  213, 230, 237 Nysius 305

839

840

Index

o

Oberea  366 O. erythrocephala 161 Oborocoleidae (extinct)  358 Obrieniidae (extinct)  358 Obtectomera 482–487 Ochlerotatus japonicus 662 Ochodaeidae  339, 350, 384 Ochteridae  282, 289 Ochterus americanus  286 Ochthebius figueroi 148 Odiniidae  233 Odoiporus longicollis  369 Odonata  3, 15, 25, 50, 51, 55, 56, 69, 117, 147, 155, 207, 212, 218, 516, 579, 580 Odoniellini 294 Odontota dorsalis  367 Odonturini 154 Oebalus pugnax  307 Oeconesidae 119 Oecophoridae 120, 472, 480 Oedemeridae  185, 187, 342, 355, 378, 387 Oedipodinae 184 Oedoparena glauca 237–238 Oemona hirta  365 Oeneis 173 Oenochrominae 486 Oenosandridae  475, 487 Oestridae  154, 229, 234, 234, 245, 248 Oestrinae 245 Oestrus ovis 249 Olethreutinae 481 Olibrus 354 Omalisidae  340, 351 Omaniidae  282, 290 Omethidae  340, 385 Ommatidae  338, 345 Oncomerinae 310 Onconotinae 154 Oncopeltis 305 O. fasciatus 19 Onesia  238 Oniscigastridae 119

Oniticellina 104 Onitini 104 Onthophagini 104 Onthophagus  167, 181, 186 Onycholips 168 Oodescelis polita  165 Ootheca  369 Opatrum sabulosum  165, 181 Operophtera O. bruceata 663 O. brumata  251, 466, 487, 663 Opetiidae  232 Opetiopalpus sabulosus  186 Ophion 431 Opomyzidae  233 Opostegidae  471 Oprohinus  160, 161 Opsius stactagalus 657 Orchestes O. alni 172, 370 O. mutabilis 172 Oreogetonidae  231 Oreoleptidae  213, 231 Oreomela  169, 171 Orfelia fultoni 239 Orgyia thyellina 673 Orius insidiosus  291 Ormyridae  421 Ornidia obesa 252 Ornithoptera O. alexandra  114, 115 O. richmondia 116 Orobitis 155 Orphilus 352 Orsillinae 305 Orsodacnidae  342, 356, 387 Ortheziidae 295 Orthoptera  3, 11, 13, 20, 51, 80, 93, 121, 122, 147, 148, 152, 154, 173, 180, 182, 208, 212, 579, 580 “Orthorrhapha” 241–242 Orthostixinae 487 Orthotomicus  376 Orthotrichia 610 Orthotylini 296

Orussidae  420, 423, 426, 437 Oryctes  362 Oryzaephilus 354 Oscinella frit 245 Ostoma ferrugineum 156 Ostrinia nubilalis 484, 658, 659 Othniidae 175 Otibazo 168 Otidocephalinae 79, 81, 82 Otiorhynchus  158–159, 161, 166, 169, 177, 371 O. aurifer 172 O. ovalipennis 172 Oulema melanopus  368, 657 Oxoplatypus quadridentatus  373 Oxycarenidae  284, 305 Oxycarenus 305 O. hyalinipennis 305 Oxyonychini  159, 161 Oxyonyx kaszabi  151 Oxypeltidae  342, 356 Ozopemon 381 Ozophorini 306

p

Pachnoda  362 P. marginata 380 Pachycondylla chinensis 666 Pachygronthidae  284, 306 Pachygronthinae 306 Pachyneuridae  230 Pachynomidae  282, 297 Paederidus 378 Paederus 378 Pagasa fusca  291 Pagiocerus frontalis  376 Palaephatidae  471, 478 Palaephatoidea 478 Palaephatus 478 Paleomelittidae (extinct)  424 Pallichnidae (extinct)  358 Pallopteridae  233 Palparini 104 Pamphaginae  154, 184 Pamphantinae 305

Index

Pamphiliidae  420, 423, 437 Panesthia lata 120 Pangoniinae 241–242 Pantomorus cervinus  371 Pantophthalmidae  231, 241 Papilionidae 114, 474, 483, 532 Papilionoidea 469, 474, 479, 482–483 Papuana  362 Parabrochymena arborea  307 Paracantha culta 668 Paracylindromorphus 160, 186 Parahygrobiidae (extinct)  358 Paralucia pyrodiscus lucida 127 Paralucia spinifera 127 Paraminota 161 Paraminotella 161 Parandrexidae (extinct)  358 Paraphrynoveliidae  281 Parapiesma cinereum  298 Paraponera clavata 431 Pararaphe 311 Parasitica  426, 437–444 Parastrachiinae 310 Parnassius 171 Parnops 166 Paropsidis charybdis 360 Paropsis atomaria 360 Parorobitis 155 P. gibbus  156 Paroryssidae (extinct)  423 Passalidae  338, 350, 383 Passandridae  341, 354, 386 Patapius spinosus  286, 290, 654 Paussinae 346 Pediciidae  230 Pediculus 13 P. humanus 648 Pedinus  164, 181 P. femoralis  165 Pelecinidae  422, 425, 439 Pelecorhynchidae  213, 231, 234 Pelocoris carolinensis  286 Peloridiidae 119

Peltis 156 Pemphigus 633 P. populivenae 245 Pentadon 141 Pentaria  187 Pentatomidae  284, 309, 312 Pentatominae 309 Pentatomoidea 306–310 Pentatomomorpha 301–311 Penthicus 181 P. lenczyi  185 Pepsis  431, 444 Peradeniidae  422, 425 Perapion myochroum  151 Pergidae  420, 437 Pericoma  236 Perilampidae  421, 424 Periscelididae  233 Perissommatidae  230 Perkinsiella saccharicida 658 Perlidae 207 Perlodidae 207 Permocupedidae (extinct)  358 Permosynidae (extinct)  358 Perotis cuprata 161 Petalura ingentissima 119 Phaedon  166, 218 P. brassicae  367 Phaelota 161 Phaenops guttulatus 177 Phaeomyiidae 148, 233 Phalacridae 186, 341, 354, 386 Phaleria pontica  165 Phaleriini 168 Phanaeini 104 Pharoscymnus  187 P. auricomus 161 Phasiinae 614 Phasmatodea  3, 77, 80 Phaudidae  473 Pheidole megacephala 125, 666, 757, 758 Phenacoccus manihoti 613 Phengodidae  340, 385 Phiditiidae  475, 485 Philernus gracilitarsis  151 Philoliche 242

Philopedon plagiatus 168 Philornis downsi  4, 249, 660 Philus antennatus 356 Phlaeothripidae 120 Phlebotominae 247, 716, 724 Phlebotomus 724 P. perniciosus 728 Phlegyas abbreviatus  298 Phloeidae  284, 309 Phloeosinus  376 Phloeostichidae  341, 354 Phloeotribus  376 Phloiophilidae  340, 353 Phloiophilus edwardsii 353 Phlyctinus callosus  371 Phoracantha  365 P. recurva 172 P. semipunctata  172, 664 Phoridae  213, 232, 237, 243, 246, 249, 251, 253, 606, 607, 608, 610 Photuris 15 Phreatodytes 347 Phthiraptera  3, 154, 209, 579, 581 Phtora reitteri  165 Phycitinae 484 Phycosecidae  340, 353 Phycosecis 353 Phylinae 296 Phyllobius thalassinus 163 Phyllocnistis citrella 603, 610–612, 611 Phyllonorycter P. blancardella 610, 611 P. messaniella 654 Phyllophaga  363, 390 Phyllotreta  369 Phylloxeridae  628, 632 Phymata 300 P. pennsylvanica  298 Phymatinae  299, 300 Physopeltinae 311 Phytalmia 122 Phytocoris 295 Phytoecia 182 Piazomias  150

841

842

Index

Pieridae 114, 474, 483 Piesmatidae  284, 306 Piesmatinae 306 Piezosternum subulatum  307 Pilipalpidae 175 Pilophoropsidea 296 Pilophoropsis 296 Pilophorus 296 Pimelia subglobosa  165 Piophila casei  244, 252 Piophilidae  232, 244, 253 Pipunculidae 229, 232, 235, 243, 251 Pissodes  372 Pissodini 177 Pityoborus comatus  376 Pityogenes 176, 376 Pityophthorus juglandis  376 Placosternus difficilis  365 Plagionotus arcuatus  365 Planolinoides borealis 48 Plastoceridae  339 Plataspidae  284, 309 Platycoelia lutescens 378 Platygasteronyx humeridens  151 Platygastridae  422, 425, 439 Platygastroidea  439, 606, 607 Platyninae 123 Platyope mongolica  185 Platypezidae  232, 242 Platypodidae 177 Platypodinae  357, 359 Platypsyllus castor 349 Platypus  373 Platystomatidae  232 Plecoptera  3, 51, 69, 128, 147, 155, 173, 207, 212, 218, 579, 581 Plectrotarsidae 119 Pleidae  282, 289 Pleistodontes addicotti  442 Pleocomidae 49, 338, 349, 383, 390 Plinthini 177 Plinthisinae 306 Plinthus 177

Plodia interpunctella 484 Plokiophilidae  282, 292 Plokiophilinae 292 Plumalexiidae (extinct)  424 Plumariidae  421, 442 Plutella xylostella  218, 480 Plutellidae  472, 480 Plyapomus longus 304 Pnigalio  611, 617 Pocadius 167 Podabrocephalidae  339 Podischnus agenor  362 Podisus 309 Poecilimon  149 Poecilocapsus lineatus  291 Polistes  606, 610 P. chinensis 125 P. humili 125 P. versicolor 666 Polistinae 445 Pollenia 239 Polyctenidae  282, 292, 312 Polyctesis 179 Polydrusus P. corruscus 391 P. impressifrons 391 Polygraphus 176, 376 Polymerus wheeleri 312 Polypedilum nubifer 653 Polyphaga  342, 347–357 Pompilidae 209, 422, 425, 444 Popillia  363 Potamocoridae  282, 288 Praeaulacidae (extinct)  425 Praeichneumonidae (extinct)  425 Praelateriidae (extinct)  358 Praesiricidae (extinct)  423 Praydidae  472 Premnotrypes  371 Priasilphidae  341, 354 Prionoceridae  340, 353 Prionolabis  235 Prionus  367 Prisistus 160 Proctacanthus  235 Proctorenyxidae  422, 439

Proctotrupidae 54, 422, 425, 439 Proctotrupoidea 439 Prodidactidae  474, 484 Prodoxidae 465, 471, 478 Promecheilidae  342, 355 Promecotheca cumingii  367 Promelittomma insulare 353 Pronotacantha 304 P. annulata  298 Prosodes 164 Prostemmatinae 297 Prostephanus 352 P. truncatus 348 P. truncatus  364 Prostomidae  342, 355, 387 Protaetia  362 Protimaspidae (extinct)  425 Protocalliphora 713 Protocoleoptera (extinct)  358 Protocucujidae  340, 354 Protopiophila litigata 244 Protosiricidae (extinct)  423 Protura  3, 558, 578–580, 579 Psacothea hilaris  367 Psallopini 294 Psamminae 306 Psammoestes dilatatus  185 Pselaphinae  120, 185, 186, 349 Psephenidae 210, 339, 384 Pseudacteon 608 Pseudatomoscelis seriatus 293 Pseudips concinnus  376 Pseudobistonidae  475, 486 Pseudocneorhinus bifasciatus  371 Pseudococcus comstocki 603 Pseudohylesinus granulatus  376 Pseudohypocera kerteszi 247 Pseudomorphini 346 Pseudopachybrachius basalis,298 Pseudopityophthorus  376 Pseudorchestes  151, 152 P. convexus 180 P. furcipubens  151

Index

P. tschernovi 180 Pseudosiricidae (extinct)  423 Pseudostyphlus leontopodi 170 Psila rosae 244 Psilidae  232, 244, 249 Psocoptera  3, 51, 77, 80, 147, 579, 581, 654 Psychidae  471, 478 Psychoda 255 P. phalaenoides 246 Psychodidae 154, 213, 218, 229, 230, 240, 249, 299, 584, 715, 719, 724 Psyllidae 664 Psylliodes  160, 161 P. valida  170, 171 Psylloidea  120, 184 Pterocoma reitteri  185 Pterogeniidae  342, 355 Pterolonchidae  472 Pteromalidae  421, 424, 608, 609, 611, 616 Pterophoridae 173, 473, 481 Pterophoroidea  479, 481 Ptiliidae  338, 349, 383 Ptiliolum 393 Ptilodactylidae  339, 384 Ptinidae  160, 174, 186, 340, 352, 385, 394 Ptochus P. daghestanicus 164 P. porcellus 164 Ptomaphagus hirtus  344 Ptosima 179 Ptychopteridae  213, 230 Ptyssoptera 478 Pulex 13 Pulvinaria urbicola 757, 758 Pycnoderes quadrimaculatus 294 Pyralidae  474, 484 Pyraloidea  474, 479, 480, 484 Pyraustinae 484 Pyrgotidae  232, 244 Pyrochroidae  342, 355, 387 Pyrrhalta viburni  369

Pyrrhocoridae  284, 311 Pythidae  342, 355, 387

q Quadrastichus erythrinae 654

r Radiophronidae (extinct)  424 Rallidentidae 119 Rangomaramidae  231 Ranzovius 296 Raphidioptera  3, 51, 146, 147, 184, 579, 583 Ratardidae  473 Raxa 311 Reduviidae  283, 299–300, 312 Reduviinae 300 Reduvius personatus 300 Renodaeus 296 Resthenia scutata 295 Restheniini 295 Rhabdoscelus obscurus  369 Rhadalinae 353 Rhadine 346 Rhaebus  187 Rhagionidae  231, 241, 715, 719, 720, 724 Rhagoletis 246 Rhagophthalmidae  340 Rhamphini  152, 162, 177 Rhamphus choseniae 175 Rhaphidophoridae 113 Rhaphiomidas terminatus abdominalis 256 Rhiniidae  234, 245 Rhinocapsus vanduzeei 296 Rhinocyllus conicus 668 Rhinophoridae  234, 245 Rhinorhipidae  339 Rhinostomus barbirostris  369 Rhipiceridae  339, 351, 384 Rhipsideigma raffrayi  344 Rhizophagus 354 Rhodopsalta 122 Rhombocoleidae (extinct)  358 Rhopalidae  284, 302 Rhopalinae 302

Rhopalomeridae  233 Rhopalosiphum maidis 633 Rhopalosiphum padi  615 Rhopalosomatidae  422, 426, 444 Rhoptromyrex transversiodis 285 Rhyacophiloidea 211 Rhynchitidae 183 Rhynchophorus  369 Rhyparochromidae 121, 284, 306, 654 Rhyparochrominae 306 Rhyparochromini 306 Rhyparochromomiris femoratus 294 Rhysodinae  338, 346, 383 Rhyssemus germanus 392 Rhythirrinini 153 Rhytidoponera 122 Richardiidae  232, 244 Riodinidae  474, 483 Ripiphoridae 187, 342, 355, 383, 386 Risidae 148 Rivacindela 583 Rodnius prolixus 300 Rodolia cardinalis  11, 14, 250, 603, 669 Roeslerstammiidae  471 Rolstonus rolstoni  307 Roproniidae  422, 425, 439 Rotoitidae  421

s Saga pedo  150 Sahlbergella singularis  293, 294 Saileriolidae  284, 309 Saldidae 209, 282, 290 Saldula galapagosana  286 Saliana severus 577 Salpingidae  342, 355, 387 Salyavata variegata 300 Salyavatinae 300 Sameodes albiguttalis 217 Sapaia 180

843

844

Index

Saperda  367 Saperda populnea 175 Sapygidae  422, 426, 444 Sarcophaga  235 S. aldrichi 250 Sarcophagidae  170, 229, 234, 237, 245, 248, 253, 584, 606 Sasajiscymnus tsugae  365 Saturniidae  11, 465, 475, 485, 583, 610 Satyrinae 483 Scaphidema metallicum  165 Scaphoideus titanus 660 Scapteriscus  659 S. castaneus  307 Scarabaeidae  12, 49, 50, 81, 99, 104, 120, 185, 186, 244, 339, 343, 345, 350, 361, 378, 384, 394, 663 Scarabaeinae  105, 789 Scarabaeini 104 Scarabaeoidea  97, 181 Scarabaeus 167 S. sacer 23 S. zambesianus 380 Scarites 169 Scatella stagnalis 246 Scathophaga  235 Scathophagidae 234, 234, 245 Scatopsidae  213, 230, 240 Scelioninae 439 Scenopinidae  231 Scepsidinae  716, 725 Schaffneria 296 Schistonoeidae  472 Schizocoleidae (extinct)  358 Schizophora  232, 233, 234 Schizophoridae (extinct)  358 Schizopodidae  343, 384 Schizopteridae  281, 285, 312 Schlechtendalia chinensis 628 Schreckensteiniidae  473 Schreckensteinioidea  479 Sciaridae  231, 241, 246, 252 Sciomyzidae  213, 233, 244, 251

Scirpophaga S. incertula 218 S. innotata 218 Scirtidae  339, 384, 390 Sclerogibbidae  421, 424, 442 Scleropterus 170 Scolebythidae  421, 424, 442 Scoliidae  422, 426, 444 Scolytinae  21, 160, 174, 357, 359, 647 Scolytus 183, 376 S. multistriatus 660 S. schevyrewi 660 Scopuridae 155 Scraptia straminea  187 Scraptiidae  187, 342, 355, 387, 390 Scutelleridae  284, 310 Scydmaeninae 348 Scydosella musawasensis 349 Scymnus  187 Scyphophorus acupunctatus  369 Scythis 181 Scythrididae  472 Scythropiidae  472, 480 Sematuridae  475, 486 Senotainia tricuspis 247 Sepsidae  233, 252 Sepulcidae (extinct)  423 Sergentia koschowi 240 Serica 390 Serinethinae 302 Serphitidae (extinct)  425 Sesiidae  473, 481 Sialidae 156 Sibinia sp. pr. beckeri  151 Sierolomorphidae  422, 426, 444 Sigara hubbelli  286 Signiphoridae  421 Sikhotealinia zhiltzovae (extinct) 177 Silphidae  167, 185, 338, 349, 380, 383, 383, 394 Silvanidae 186, 341, 354, 386 Simaethistidae  472

Simaethistoidea  479 Simuliidae  18, 154, 155, 212, 218, 230, 234, 240, 247, 584, 714, 715, 719, 720, 724–725, 733 Simulium (Wilhelmia)  537 Simulium S. arcticum  731 S. damnosum  717, 726, 730, 731, 732 S. metallicum  717 S. ochraceum  726 S. sirbanum  732 S. vampirum  731 Sinisilvanidae (extinct)  358 Sinosiricidae (extinct)  423 Sinoxylon unidentatum  364 Siphlaenigmatidae 121 Siphonaptera  3, 52, 56, 146, 154, 579, 584, 646 Siricidae  420, 423, 437, 647 Sisyphini 104 Sisyphus 167 Sitona 170, 371 Sitonini 152 Smaragdesthes africana  362 Smicripidae  341, 354, 386 Solenopsis S. geminata 4 S. invicta  125, 608, 657, 659, 662, 663, 665, 674 S. richteri 663 Somabrachyidae  474 Somatiidae  232 Spaniopsis  716, 724 Spathiopterygidae (extinct)  425 Speonomus 349 Spercheinae 348 Spermophagus  159, 182, 187 S. sericeus 182 Sphaeridiinae 348 Sphaeritidae 146, 338, 348, 383 Sphaeriusidae  338, 346, 383 Sphaeroceridae 229, 233, 244–245

Index

Sphecidae  420, 424, 446 Sphenophorus venatus  369 Sphenoptera 182, 186 S. gossypii  363 Sphindidae  340, 354, 385 Sphingidae  475, 485, 583 Sphyrocoris obliquus  307 Spilogona 57 Spilomelinae 484 Spilostethus 305 Spondyliaspinae 121 Stackelbergomyiinae 148 Staphylinidae  50, 55, 157, 168, 173, 176, 181, 185, 186, 338, 343, 345, 349, 380, 383, 516, 646 Staphylinoidea 348–349 Stathmopodidae  472 Stegobium paniceum 352 Steirastoma breve  367 Stelidota geminata  364 Stemmocryptidae 287 Stenocephalidae 303 Stenodemini 295 Stenogastrinae 445 Stenopodainae 300 Stenosis punctiventris  165 Stenotrachelidae  342, 355, 387 Stenotritidae  420 Stenus  157, 380 Stephanidae  422, 425, 437 Stephanitis pyrioides 295 Stephanocleonus  170, 180 S. excisus  151 S. inopinatus  151 S. paradoxus  151 S. persimilis  151 S. potanini  151 Sternocera 180 Sternochetus  370 Sternoplax mongolica  185 Sternorrhyncha  3, 97, 147, 161, 168, 244, 609 Steropes latifrons  187 Sterrhinnae  487 Stethoconus japonicus 295 Stethorus punctatum  365

Sthenauge 610 Sthereus ptinoides 168 Stigmaphronidae (extinct)  424 Stolamissidae (extinct)  425 Stomoxyinae  646, 716 Stomoxys calcitrans 648, 660, 723 Stonemyia  716, 725 S. velutina 256 Stratiomyidae  213, 231, 235, 241, 253 Streblinae 245 Strepsiptera  3, 51, 118, 512, 579, 582, 605, 607 Stromatium barbaratum  365 Strongyliini  82 Stylogaster  235 Stylogastrinae 244 Stylopidae 186 Suragina  716, 721 Suraginella  716, 721 Sycoracinae  716, 724 Symphoromyia  716, 724 Symphyta  147, 426, 436–437 Sympiesis 611 Synchroidae  342, 355, 387 Synemon plana 123 Synteliidae  175, 178, 338, 348 Syringogastridae  232 Syrphidae 170, 213, 229, 232, 243, 255 Syrphus  236 Systelloderes biceps  286

t

Tabanidae  154, 170, 213, 229, 231, 234, 241, 247, 584, 714, 715, 719, 720, 725 Tabanomorpha  231, 241–242 Tabanus T. conterminus 729 T. nigrovittatus 729 Tachinidae  148, 170, 229, 234, 237, 245, 251, 437, 584, 606, 607, 610, 612, 786 Tachiniscidae  232

Taeniopterygidae 155 Taldycupedidae (extinct)  358 Tanaostigmatidae  421, 424 Tanyderidae  213, 230 Tanymecini 168 Tanymecus dilaticollis  371 Tanypezidae  232 Tanysphyrus lemnae 392 Tasimiidae 119 Tasmosalpingidae  341, 354 Tegeticula 13 Telegeusinae  340, 351, 385 Telenominae 439 Teleonemia scrupulosa 297 Teleopsis  235 Teloganodidae 119 Temnoshoita nigroplagiata  369 Tenebrio obscurus  165 Tenebrioides mauritanicus 156 Tenebrionidae  164, 173, 184, 185, 187, 342, 345, 355–356, 386, 394, 506 Tenthecoris 294 Tenthredinidae  154, 155, 420, 423, 437 Tentyria nomas  165 Tephritidae  97, 229, 232, 244, 246, 251, 646, 647 Teracriinae 306 Teratomyzidae  233 Teredidae 354 Teretrius nigrescens 348 Termatophylidea 295 Termatophylini 295 Termitaphidae  284, 301 Termitoidea  11, 12, 21, 93, 97, 118, 120, 237, 245, 349, 351, 577, 579, 581, 647, 745 Termitophilomya  238 Termitoxeniinae 237 Tessaratomidae  284, 310 Tetanocera  236 Tetracampidae  421, 424 Tetranychidae 250 Tetratomidae  342, 355, 386

845

846

Index

Tetropium  367 T. fuscum 660 Tetrybrachys 152 Tettigarctidae 120 Tettigoniidae  77 Thamnurgus T. caucasicus 183 T. pegani 187 T. russicus 183 Thanasimus 353 Thanatophilus 167 Thanerocleridae  340, 353 Thaumaglossa 352 Thaumaleidae 119, 212, 230, 234, 241 Thaumastellidae  284, 310 Thaumastocoridae  283, 296 Thaumastocorinae 296 Thaumatomyia T. glabra 245 T. notata  239, 249 Thaumatoxena  238 Theca  186 Theophilea 160 Therevidae  231, 255 Thorictus 168 Thrinchinae 154 Throscidae  339, 385, 390 Thylodias 359 T. contractus 187 Thymalus 156 Thyreocoridae  284, 310 Thyreocorinae 310 Thyreophora cynophila 256 Thyreophorini 229 Thyrididae  474, 482, 484 Thyridoidea  479 Thysanoptera  3, 51, 69, 97, 120, 147, 295, 579, 582, 605, 646, 647, 650 “Thysanura”. See Microcoryphia; Zygentoma Tineidae  471, 478 Tineodidae  473 Tineoidea  471, 479 Tingidae  283, 296–297, 312 Tinginae 297

Tiphiidae  422, 426, 444 Tipulidae  173, 179, 229, 230, 240 Tipuloidea  213, 230, 241 Tischeriidae  471, 478 Tischerioidea  476 Titanomyrma (extinct)  433 Tomarus gibbosus 50 Tomicus  377 T. piniperda 359 Torridincolidae  338, 345 Tortricidae (see also Heliocomidae)  473, 481 Tortricinae 479 Tortricoidea  479, 481 Torymidae  421, 424, 611 Tournotaris 170 T. bimaculata 391 Toxorhynchites  716 Trachelostenini  342, 355 Trachypachinae  338, 346, 383 Trachyphloeus 158 Trachys 182 Trachyscelis aphodioides  165 Trechini  169, 346 Trechus 170 Treptoplatypus solidus  373 Triadocupedidae (extinct)  358 Triaplidae (extinct)  358 Triatoma 312 T. sanguisuga  298 Triatominae 299 Tribolium T. castaneum  20, 356, 359, 381 T. confusum 20 Trichispa sericea  367 Trichoceridae  230 Trichoferus campestris  365 Trichogramma  442, 613, 616 T. minutum 614 T. platneri 614 Trichogrammatidae  421, 424, 442–443 Trichoptera  3, 52, 69, 118, 146, 155, 173, 210, 213, 439, 579, 582, 607

Trichosirocalus barnevillei 163 Tricoleidae (extinct)  358 Trictenotomidae 175, 342, 355 Tridentaformidae  471, 478 Trigonalidae  422, 425, 437 Trigonoscelis T. schrencki  150 T. sublaevigata granicollis  185 Trigonotylus caelestialium 295 Trirhithrum T. coffeae 103 T. nigerrimum 103 Tritarsusidae (extinct)  358 Trixagus 393 Trogidae 167, 338, 350, 384 Trogoderma granarium  364, 646 Trogossitidae 156, 340, 353, 385, 394 Trogoxylon 352 Troidini 483 Truncaudum agnatum  377 Tryphetus incarnatus  373 Tryphoninae 438 Trypodendron domesticum  377 Tshekardocoleidae (extinct)  358 Tychius  153, 159 Tymbopiptus valeas 124 Typophorus nigritus  368

u

Ulidiidae  232 Ulodidae 124, 342, 355 Ulomoides dermestoides 379 Ultracoelostoma 666 Ulyanidae (extinct)  358 Upis ceramboides 355 Uraniidae  475, 486 Urodidae  473 Urodoidea  479 Urodontidae  162, 183 Urophora 669

Index

Urostylididae  284, 310 Uvaroviini 184

v

Valeseguyidae  230 Vanessa atalanta 483 Vanhorniidae  422, 439 Varroa V. destructor 788 V. jacobsoni 788 Veliidae  281, 287 Velocipedidae  283, 300–301 Vermeleonidae  231 Vermileonidae  229, 239 Vesperidae  342, 356 Vespidae  422, 426, 444–445 Vespinae 445 Vespoidea  173, 444 Vespula 429 V. germanica  125, 666 V. pensylvanica 666 V. vulgaris  125, 666 Vianaidinae 297

w Wasmannia auropunctata 4, 124, 429, 666 Whalleyanidae  474

Whalleyanoidea  479 Wohlfahrtia 249

Xylotrechus  365 Xylotrupes gideon  362 Xystrocera globosa  366

x

y

Xanthorhoe bulbulata 127 Xenasteiidae 155, 233 Xenomela 170 Xenopsylla 13 X. chaeopis 662 Xiphydriidae  420, 437, 438, 647 Xyelidae  420, 423, 437 Xyelotomidae (extinct)  423 Xyelydidae (extinct)  423 Xylastodorinae 296 Xylastodoris X. luteolus  291–296 Xyleborus  377 Xyleborus glabratus 660 Xyletinus  186 Xylomyidae  231, 241 Xylophagidae  231 Xylophagomorpha  231 Xyloryctidae  472 Xylosandrus  377 Xyloterinus politus  377 Xyloterus lineatus  377

Yponomeuta 538 Yponomeutidae 121, 472, 480 Yponomeutoidea  472, 479, 480 Ypsolophidae  472

z Zabrini 346 Zabrus tenebrioides  362 Zagrammosoma 611 Zelandochlus 121 Zonocerus variegatus 19 Zopheridae 176, 342, 355, 386 Zoraptera  3, 51, 57, 118, 147, 578, 579 Zorochrus  186 Zygaenidae  474, 482 Zygaenoidea  473–474, 479, 482 Zygentoma (see also “Thysanura”)  3, 147, 579, 580

847

849

Index of Non‐Arthropod Taxa Arranged Alphabetically. Includes non‐arthropod animals, plants, fungi, protists, bacteria and viruses. Page numbers in bold indicate table entries, and numbers in italic face indicate entries on figures and in figure captions.

a Abies  160, 174, 176 A. balsamea 667 A. fraseri 667 Abutilon theophrasti 302 Acacia  21, 119, 437 Acer  175 A. negundo  141, 302 Adelina tribolii 20 Aesculus hippocastanum  175 Agathis 121 alfalfa  13, 246, 359, 656 Allium 161 almond 101 Alternanthera philoxeroides 217 Amorpha fruticosa 182 Amphibia  10, 721, 722, 724, 725 Amygdalus 183 Anabasis brevifolia  151 Angraecum sesquipedale 486 anteater 11 Apiaceae 82, 142, 162, 483 Apicomplexa 723 apple 252 Araucaria  121, 439 Arecaceae  73, 361, 480 Aristolochia A. diehlsiana 115 A. elegans 116 Aristolochiaceae 483 Artemisia  161, 164, 181, 182

A. pauciflora 181 Artiodactyla 105 Artocarpus 252 Asclepiadaceae 483 Asteraceae 82, 142, 152, 162 Astragalus 159 Atraphaxis  171, 182 Aves 529 avocado 101

b Baccaurea motleyana 102 Bacteria  215, 247 Anaplasma 250, 726 Bacillus anthracis (anthrax)  719, 722 Bacillus thuringiensis  667, 732 Bartonella (verruga peruana)  718, 723 Borrelia burgdorferi (Lyme disease)  11‐12, 667 Campylobacter 359 Corynebacterium pyogenes 248 Dermatophilus congolensis (streptothrichosis)  719 Erwinia tracheiphila 359 Francisella tularensis (tularaemia) 248, 718, 719, 725 Rickettsia (typhus)  13 Salmonella 359

Streptomyces 21 Wolbachia 432 Xylella fastidiosa 665 Yersina pestis (plague)  13, 662, 767 badger 11 bamboo 295 bat  292, 583, 723 beans  101, 246, 294, 305, 355 beets 246 Besnoitia  719 Betula 174, 175 black bear  11 Bolboschoenus 160 Bombacaceae 73 Boraginaceae  142 162 Bovini 105 Brassicaceae  142, 162, 183 bromeliad  207, 208, 211, 664 Bryophyta  161, 207, 287, 288, 293, 295, 303 buffalo 723 Burseraceae 73

c Cacao  252, 294, 302, 612, 788 Cajanus cajan 302 Cakile C. euxina 167 C. maritima 167 Callitris 309 Calluna vulgaris  175 camel  98, 248

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

850

Index

Camelina  158 Cannabaceae 162 Capsicum annuum 102 Caragana 171, 175, 182, 183 Cardueae 162 Carduus  183, 251 Carex 161 carrot 246 cashew  101, 252 cassava  252, 302 Castanea dentata 667 Casuarinaceae 119 cat  123, 128 cattle  12, 98‐99, 248, 661, 663, 723, 724, 725, 731 cauliflower 252 Cecropiaceae  73, 74 Cedrus 174 celery 246 Celtis schippii 73 Centaurea 251 C. stoebe 669 Cerasus vulgaris  175 Chenopodiaceae  142 Chosenia arbutifolia 175 Cirsium 251 C. arvense 668 C. canescens 668 C. undulatum 668 Clematis 176 Cobresia 170 cocoa beans  357 coconut palm  302, 353 coffee plant  103, 357 Convolvulaceae 159 Convolvulus arvensis  159, 172 Corylus avellana  175 Cotoneaster  175 cotton  13, 311, 359 Crataegus  175, 538 Cucurbitaceae  101, 103, 142, 159, 359 Cuscutaceae 159 cycad  354, 357 Cynoglossum officinale 361 Cyperaceae  182, 304

d Daedaleopsis confragosa 167 date palm  101 Descurainia sophia  157 donkey  98, 248 duck 208

e Eichhornia crassipes 217 emu 359 Ephedra 161 E. major 159 E. przewalskii  151 159 E. sinica 159 Ephedraceae  142 162 Equisetum 161 Ericaceae  142 Erodium 182 Erwinia tracheiphila 359 E. canescens  157 E. pulchellum  157 Eucalyptus  119, 124, 126, 172, 296, 360, 437, 664 Euonymus  175 Euphorbia 161 E. characias 665 Euphorbiaceae  73, 162, 187

f

Fabaceae 73, 142, 162, 301, 305, 308, 309, 605 Fagaceae  142, 162 Fagus  178 F. grandifolia 660 Fergusobia quinquenerviae 237 fern  161, 294, 357 Ficus  114, 118, 440 F. macrophylla 114 F. microcarpa 656 filarial nematodes  252, 584, 721, 722, 725 Dirofilaria  247, 253 Loa loa  248, 725 Mansonella 247, 718, 719 Mansonella ozzardi 725 Onchocerca 247, 718, 719, 726, 730

Onchocerca lienalis 725 Onchocerca lupi 725 Onchocerca volvulus  725, 731 Parafilaria bovicola 248 Stephanofilaria  719 723 Frangula alnus  175 Fraxinus  175  360, 667 F. excelsior 664 F. pennsylvanica  172, 183 frog  245, 721, 724 European green frog  247 fungus  167, 215, 242, 301, 354, 359, 660 bracket fungus  56, 292, 352 Gossmannia (blue‐stain fungus) 361 giraffe 723

g Gleditsia triacantha 172 goat  98‐99, 123, 248, 359 goose 208 Gossmannia (blue‐stain fungus) 361 granadilla 101 grizzly bear  11 Grossularia 183 ground squirrel  181 Guarea pterorhachis 73 guava  100, 101, 302

h

Habronema  718, 723 Halorhagaceae  142 Haloxylon ammodendron  151, 184 Helicostylis 73 Heracleum 161 Herpestes javanicus  123, 663 Hesperis bicuspidata  158 horses  98, 248, 359

i Icosella neglecta 247 Iljinia regelii  151 Iriartea deltoidea 73 Iris pseudacorus 161

Index

Iryanthera 73 Isatis  158

j Jacaratia 73 jackfruit 101 Juglans regia 172 Juncus 160 Juniperus 160 J. virginiana 293

l Laburnum 664 Lamiaceae  142, 162, 182, 305 Lantana camara 297 Larix  160, 171, 174, 175, 176, 177, 301 Lauraceae 73 Lecythidaceae 73 leek 252 Leersisa hexandra 539 Leishmania 248, 718, 724, 727, 728 Leontopodium 170 Lepidium L. draba  144, 159 L. vesicarium  158 Leptographium wageneri 360 lettuce 246 Leucocytozoon 247, 718, 719, 725, 733 lichen  293, 295, 309 Liliaceae  142 162 Lindackeria 73 lizard  10, 124 Lonicera  175 Luehea seemanni 785 Lythrum salicaria  361, 668

m Magnoliophyta 160 Malus  175, 538 M. domestica 101, 175 Mangifera indica (mango)  100, 101, 103, 252 marmot 181 martin [bird]  11 Matisia malacocalyx 73

Matthiola  158 Melaleuca M. howeana 115 M. quinquenervia 237 Meliaceae 73 melons 246 Metarhizum 359 Mimosaceae 119 Moraceae  73, 162 mouse (See also Peromyscus)  11, 12 Myristacaceae 75 Myrtaceae  119, 354

n Nasturtium nasturtium‐ aquaticum 218 Nectria 660 Nestor meridionalis 666 Nitraria sphaerocarpa  151 Nothofagus  119, 121, 122, 125, 303, 666

o oak. See Quercus Odocoileus virginianus (white‐ tailed deer)  11 Olea 103 Oleaceae  142 Onagraceae  142 onions  246, 252 Opuntia  11, 302, 466, 485, 668, 670 O. corallicola 668 otter 208

p pangolin 11 papaya  101, 302 Paramecium 20 Pararistolochia 116 Passiflora 483 Passifloraceae 465 peach 101 peas 246 Peganum harmala 187 Perissodactyla 105

Peromyscus 669 P. leucopus 11 P. maniculatus 669 Persea borbonia 661 Phragmites australis 160 Phylloscopus 529 Picea  160, 174, 175, 176 P. abies 176 pig  98, 380, 723 Pinophyta  160, 357 Pinus 301 P. contorta  13, 361 P. pumila 174 P. sibirica 174 P. sylvestris 174, 175, 176 P. taeda 359 Pistacia 628 pitcher plant  211, 243 Plasmodium (malaria)  13, 247, 253, 575, 584, 661, 662, 718, 722, 726, 730, 732, 733, 767 avian malaria  249, 718 Platanus 297 Poaceae  142, 160, 162, 182, 301, 304, 479, 480, 484, 539 podocarps 121 Polygonaceae  142 Populus 174, 175 P. tremula 174, 175 potato 246 Potentilla 181 Pourouma minor 73 Primulaceae  142 Proboscidea 105 Protea nitida 665 Proteaceae  119, 665 Prunus 174 P. spinosa 183 Pteridophyta  161, 294, 357 pumpkin 246

q Quercus  11, 161, 162, 174, 175, 175, 486, 487, 663, 667 Q. garryana 663 quince 101

851

852

Index

r Rafflesia arnoldii 252 Rattus  113, 120, 123, 128, 662 Reaumuria soongorica  151 reptiles 721 Reseda lutea  157 Restionaceae 304 rhinoceros 723 Rhus 617 R. javanica 628 Ribes  175, 437 rice 539 rodent 12 Rosa  175, 437 Rosaceae  142, 162, 175 Roystonea 296 Rubiaceae  142, 605 Rubus  175, 353, 437 R. idaeus  175

s

Salicaceae  142 Salix 174‐175, 175, 391, 437 S. interior 668 S. udensis 175 S. schwerinii 175 S. viminalis 175 Sambucus  175 Sapotaceae 73 Schinus 617 S. terebinthifolius  466, 656 Schistosoma (bilharzia) Sclerocarya birrea  101 Scrophulariaceae  142, 162 sea lion  208 seal 208 sheep  98‐99, 248, 359, 661, 723 Sisymbrium S. loeselii  157 slime‐mold 354 sloth bear  11 Solanaceae  142, 162 Solanum S. esculentum  100, 102, 246 S. incanum 102 S. melongena 102 S. nigrum 102

S. sisymbriifolium 102 S. torvum 102 Sorbus 174, 175 S. aucuparia  175 soybean 660 sparrow 12 spinach 246 Spiraea 183 spirurid nematodes  723 sponges  209, 379 squash 355 Sterigmostemum  158 Strigosella  158 Strychnos 101 sun bear  11 suslik 181 swallow (bird)  11 swift (bird)  11 Sympegma regelii  151 Symphoricarpus  175 Syringa  175

t tea  252, 294 Thelazia 248 Tilia  175 Tillandsia 664 toad, cane  128, 242, 724 tree tomato  101 Trillium 665 Trollius T. asiaticus 170 T. europaeus 252 trout 10 Trypanosoma T. brucei (sleeping sickness)  13, 248, 584, 718, 723 T. cruzi (Chagas disease)  13, 300, 312 T. equiperdum 248 T. evansi 248 T. nagana  718, 723 Tsuga T. canadensis 667 T. caroliniana 667 Typha 664

u

Ulmus 174, 175 U. americana 660 U. pumila  172, 183 Urticaceae 305

v Vaccinium V. myrtillus  175 V. uliginosum  175 Viburnum  175 Vincetoxicum 466 Viola 155 Violaceae 155 viruses African horse sickness  247, 718, 721, 730 Akabane  718 avian pox  661, 718 Barmah forest disease  718 blue‐tongue  248, 721, 729, 730, 733 bovine ephemeral fever 247, 718 bovine herpes  719 Bovine leukemia  719 Cache Valley disease  718 chikungunya fever  663, 718, 722, 726 citrus tristeza  661 dengue  248, 661, 664, 718, 722, 726 encephalitis 248 encephalitis, eastern equine 247, 718 encephalitis, Japanese  718 encephalitis, La Crosse  662 encephalitis, Rocio  718 encephalitis, Venezuelan equine  718 encephalitis, western equine  718 encephalitis, West Nile  13, 247, 513, 718, 732 equine infectious anemia  719 geminiviruses 661

Index

hantavirus 669 Human Inmunodeficiency (HIV) 248 Jamestown Canyon disease  718 O’nyong‐nyong  718 Oropouche fever  718, 721 Palyam disease  718 plant viruses (unspecified) 628, 633, 661 polydnavirus 432

Rift Valley fever  718, 719 Rocio encephalitis  718 Ross River virus  718, 726 sand fly fever  248, 719, 724 Schmallenberg  718, 721, 733 tomato spotted wilt  661 tospovirus 661 Wesselsbron  718 vesicular stomatitis  719 yellow fever  13, 248, 653, 665, 718, 722, 726

Zika  718 Vitaceae  142

w walrus 208 Warscewiczia coccinea 73 watermelon 101

y yellow‐headed blackbird  11 Yucca  13, 294, 465

853

855

Subject Index Page numbers in bold indicate table entries, and numbers in italic face indicate entries on figures and in figure captions.

a

abundance  67, 69, 77, 79, 89, 99, 214, 215, 241, 255, 356, 381, 604, 606, 612, 663, 757, 772 acoustic communication  208, 380, 465, 483, 484, 487, 538–539 adaptive radiation. See radiation adventive species of insects  4, 12, 14, 24, 49, 100–102, 107, 121, 123–126, 128, 141, 142, 183, 249, 290, 292, 297, 302, 303, 305, 306, 360, 390–392, 487, 633, 634, 641–675 (chapter 21), 757, 758, 777 adventive species of plants  116, 123, 172, 183, 217, 297, 302, 357, 361, 466, 481, 485, 748 aesthetics  468, 508, 713, 725, 755 African Arachnid Database (AFRAD) 97 aestivation  113, 210 Africa  12, 14, 93–107 (chapter 5), 144, 155, 168, 175, 184, 188, 242, 247–250, 256, 287, 293, 297, 303, 305, 347, 348, 354, 431, 444, 478, 485, 575, 581, 582, 612, 615, 617, 655, 658, 665, 717, 721–723, 725, 730, 732, 751, 769, 788

African Fruit Fly Initiative (AFFI) 100–101 Afrotropical region  93–107 (chapter 5), 146, 155, 175, 185, 188, 304, 308, 310, 353, 439, 487, 715–716, 723 agamospecies  531, 534–536 agriculture  13–14, 246–247, 344, 357–359, 647, 648, 653, 658–660, 750, 754, 788 agroecosystems  23, 99, 123, 293, 427, 505, 606, 612, 654, 658 Alaska [USA]  49, 392, 652, 768 alien species. See adventive species allelochemicals  483, 486, 488, 665 allergic reactions  218, 246, 250, 379, 662 allochronic speciation. See speciation alpine insects  20, 144, 152, 169–171, 252 Altai mountains  146, 163, 169, 170, 181 amber  432, 436 American Samoa  297 anaplasmosis 250, 719 Anatolia  158, 174, 180, 184 Andrews Experimental Forest [Oregon, USA]  10 Angola  94, 106

anholocyclic populations  631 Antarctica  229, 345, 580, 655 anticancer properties. See medicinal properties of insects Antipodes Islands [New Zealand] 117 Aotearoa (New Zealand)  113, 117 aposematism  295, 379, 464, 465, 482, 484, 486, 488 Appalachian mountains  218, 237, 667 apterous insects. See flightless insects aquatic insects  10, 56, 82, 119, 121, 123, 128, 155, 160, 173, 186, 205–220 (chapter 8), 241, 242, 250, 255, 287–290, 312, 348, 351, 380, 481, 484, 653, 721, 724–725 Argentina  119, 120, 296, 303 aridization  148, 169, 180 Aristotle 528 Arizona [USA]  47, 49, 58, 594 Armenia  149, 179 Arrente people  113 art, literature and religion, insects in  13, 67, 217, 248, 256–257, 378, 419, 463, 464, 616, 658, 661 asexual reproduction. See parthenogenesis

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

856

Index

Asia  13, 101, 102, 143–187, 213, 216, 293, 297, 303, 305, 310, 360, 379, 381, 477, 482, 483, 532, 537, 539, 575, 583, 651–653, 724, 788 Auckland Islands [New Zealand] 117 Australasian region  104, 111–129 (chapter 6), 112, 210, 481, 483, 537, 715–716 Australia 11–13, 70, 98, 111, 113, 116–117, 118–121, 123, 126–128, 216, 243, 245, 248, 249, 251, 279, 280, 281–284, 296, 297, 302–311, 337, 345, 347, 348, 353, 354, 360, 361, 429, 431, 437, 440, 477, 478, 480–481, 485, 487, 539, 583, 653, 654, 658, 659, 659, 661, 665, 666, 789 Australian Biological Resources Study (ABRS)  128 Australian Entomological Society 113 Austria, 94  183, 255, 256, 650, 652, 660 autoparasitism 605 Azerbaijan 170 Azores  144, 180

b backyard biodiversity  767–777 (chapter 24) Bali (Indonesia)  112 ballast 645–646, 646, 648, 649 Banks Peninsula [New Zealand] 123 Barcode Index Number (BIN), 382, 383, 388–389 771 Barcode of Life Project 382–393, 578, 775

Barcode of Life Data Systems (BOLD) 4, 338–343, 382, 387, 388–389, 390–393, 577–585 barcoding, DNA  79, 82, 85, 382–394, 436, 465, 467, 489, 508, 516, 521, 548–549, 551, 554, 575–585 (chapter 17), 614–617, 616, 629, 633, 634, 673, 714, 727–729, 771, 775, 786 barcoding, specimen labels 596–597 Basic Local Alignment Search Tool (BLAST)  576, 578 Beard, Dan  787 Belarus  143, 160, 162 Belgium 93, 94, 251, 664 Benin 101 Bering Island [Russia]  167 Bermuda 256 Bhutan, 149, 179 binomial nomenclature. See nomenclature bioassessment. See biological assessment biochemistry  381, 531 biocontrol. See biological control biodiversity assessment  128, 548, 549, 768, 773, 775 Biodiversity Information Standards 598 Biodiversity Institute of Ontario 390 bioengineering  15, 380, 789 biogeography  22, 97, 99, 113, 114, 121, 381, 507, 508, 646 bioindicators  99, 246, 254–255 bioinformatics  488, 507, 554–556, 559–560, 593–601 (chapter 18), 775 biological assessment  72, 214, 215–217, 254, 255, 749

biological control of insects  11, 14, 16, 25, 97, 244, 250–251, 292, 295, 297, 311, 312, 351, 352, 355, 391, 432, 434, 437–441, 603–618 (chapter 19), 645, 652, 669, 788 biological control of plants  124, 144, 297, 302, 361, 463, 466, 480, 481, 485, 656, 665, 667–670 biological race  536 biological species concept (BSC). See species concepts bioluminescence  113, 239, 349, 351, 379–381 biomonitoring. See biological assessment bioprospecting 107 biosecurity  100, 125, 128, 246, 466, 582, 583, 616, 646, 649, 651, 658, 671 biosensors 381 bioterrorism  501, 513, 674 biotype 536–540 biting by insects (other than flies)  217, 288–289, 296, 299–300, 347, 430–431 blood feeding  154, 155, 208, 234, 241, 245, 247, 254, 299, 306, 713–734 (chapter 22) Borneo  112, 218 Botswana  101, 103 Bounty Islands [New Zealand] 117 brachypterous insects  209, 293, 299, 301 brackish (saline) habitat. See salt‐water habitats Brazil  4, 70, 75, 248, 349, 428, 576, 612, 622, 722, 725 Britain  50, 144, 148, 255, 427, 430, 529, 644, 648, 652

Index

British Columbia [Canada]  11, 13, 57, 361, 651, 652, 663, 673, 674 Buller, Walter  124 butterfly houses  114, 247

c California [USA]  11, 14, 48, 57, 168, 245, 251, 256, 361, 393, 610, 611, 611, 612, 648, 650, 651, 653, 654, 658, 659, 659, 664, 669, 788 Cambodia 717 camouflage  104, 210, 300, 313, 463, 487 Campbell Island [New Zealand] 117 Canada  13, 49, 54–59, 216, 354, 360, 361, 382, 383–387, 388, 390–393, 581–583, 612, 651–652, 656, 660–663, 668, 673, 731 Canadian National Collection of Insects, Arachnids and Nematodes  49, 548 Canary Islands  180, 381, 429, 627, 656, 666 canopy, forest  68–70–85, 156, 428 canopy fogging  9, 69, 73, 74, 85, 280 cantharidin  359, 378, 379 Cape Verde  144, 179 Carboniferous Period  15 Caribbean  651, 662, 721, 722 carrion insects  84, 167, 244, 245, 247, 252, 253, 256, 349, 352, 354 case‐making 211 caste determination  21, 577 catalogs  54, 96, 97, 103, 144, 279, 289, 290, 293, 306, 632 Caucasus  141, 147, 152, 154, 157, 159, 162, 164, 169, 170, 172, 173, 180–183 cave‐dwelling insects  245, 256, 349

Celebes. See Sulawesi Central America  47, 67, 249, 427 Central Asian subregion  147, 184 Centre for Agriculture and Biosciences International (CABI) 143 Chatham Islands [New Zealand] 117 checklists  2, 288, 292, 305, 309, 436, 444, 516, 652 Chile  119, 121, 290, 303, 354 China  23, 102, 144, 145, 146, 155, 158, 169, 170, 174, 175, 179, 180, 182, 183, 216, 287, 289, 308–310, 356, 360, 437, 486, 582, 583, 615, 633, 652, 655, 768 Christmas Island [Australia]  112, 666, 757 chromosomes  16, 159, 303, 381, 537, 551, 632, 727, 731 Circumpolar region  147, 172, 173 classification  56, 230, 244, 245, 279, 281–284, 285, 289, 290, 293, 296, 297, 299, 302, 303, 338–343, 344, 347, 351, 356, 362–377, 420–422, 422, 436–438, 444, 445, 464, 466, 467, 469, 476, 478, 480, 487, 488, 490, 499, 500, 506, 509, 512, 513, 521, 530, 552, 560, 586, 627, 629, 630, 634, 721, 770, 777 climate change  9, 14, 22–24, 49, 59, 65, 96, 121, 123, 126, 127, 172, 280, 312, 313, 356, 513, 593, 604, 634, 641–643, 662, 670, 672, 733, 747, 756, 757, 759, 772, 776, 777

clones  531, 536 coarse particulate organic matter (CPOM)  206, 214, 215 coevolution  440, 464, 465, 483, 484, 508 COI gene (cytochrome c oxidase subunit I gene)  382, 390, 393, 548, 577, 583–586, 613–617, 615 collections  49, 50, 53, 54, 59, 93, 94, 95–98, 103, 106, 143, 359, 378, 435, 465, 489, 501, 503, 504, 506, 508, 513, 515, 517, 518, 521, 523, 528, 585, 593, 595–597, 599, 601, 613, 731, 776 Colombia  724, 725 Colorado [USA]  381, 652, 722 cleptoparasitic. See kleptoparasitism commensals  296, 313, 355 community ecology  22, 465, 727, 770–772, 775 Comores Islands  101 competition  20, 23, 378, 380, 464, 663, 665, 666, 748, 773 competitive displacement  664, 665 Congo, Democratic Republic of  103, 106, 205, 516, 654 conjunctivitis  248, 250 Connecticut [USA]  787 conservation  9, 10, 17, 25, 50, 53, 65, 68, 80, 96, 97, 104, 106, 113, 114, 116, 127–129, 142, 255, 256, 280, 312, 313, 343, 346, 350, 356, 359, 395, 432, 437, 445, 464, 465, 502–505, 509, 527, 576, 577, 587, 604, 641, 644, 665, 669, 725, 726, 747, 749–759, 771–787

857

858

Index

Convention on Biological Diversity (CBD)  128, 777 Convention on International Trade in Endangered (CITES)  116, 483 coprophagous insects  12, 84, 164, 167, 181 Costa Rica  252, 427, 430, 438, 585, 586, 608, 612, 771, 786 courtship. See reproductive behavior Cretaceous Period  432, 433, 468 Crimea 170 Critical Zone  65, 67–69, 71, 85 crop losses from insects  100, 311, 633, 649, 658 crop pests. See pests crypsis. See camouflage cryptic species. See sibling species Cuba 296 culture, insects in human. See art, literature and religion Cyberinfrastructure for Phylogenetic Research (CIPRES) 520 cybertaxonomy  517, 521 cyclical parthenogenesis  631 cytochrome c oxidase. See COI gene cytochrome oxidase. See COI gene cytochromes, discovery  19 cytoforms  717, 730 cytotaxonomy  724, 727, 730 Czech Republic  392

d Daghestan  164, 172 Darwin Core (DwC)  598, 599 Darwin, Charles  18, 486, 529, 641

databases  96, 97, 126, 520, 586, 603–618 (chapter 19), 613, 616, 617, 649, 730, 731, 774, 776 defenses, insect  351, 379, 431, 465, 483, 612 defenses, plant  161, 360 defoliation  11, 486, 538, 667 deforestation  65, 67, 123, 142, 218, 506, 776 dermatitis and dermatosis 378, 719 deserts  49, 57, 105, 150, 161, 166, 174, 180, 183, 184, 229, 356, 443, 507 detritivores 12, 84, 127, 211, 215, 343, 350, 608 Devonian period  15, 768 diabetes  253, 254 diapause  206, 207, 210, 464, 468, 488 dichlorodiphenyltrichloroethane (DDT)  466, 726, 732 diseases of animals, arthropod borne  13–14, 247–249, 312, 360, 662, 667, 713–733 (chapter 22), 769, 788 African horse sickness  247, 718, 721, 730 Akabane viral disease  718 anthrax  718, 719 arbovirus  662, 722 avian pox  661, 718 Barmah forest disease, 718 bartonellosis  718–719, 723, 724 besnoitiosis, 719 bilharzia 251 Black Death  662 bluetongue 247, 718, 721, 729–730, 733 bovine ephemeral fever 247, 718 bovineleukosis  719 Cache Valley viral disease  718

California encephalitis  718 Chagas disease  13, 300, 312 Chandipura virus disease  719 Changuinola fever  719 chikungunya 662, 718, 722, 726, 733 dengue  247, 661, 662, 718, 722, 726 dirofilariasis  718 dog heartworm  247, 718 eastern equine encephalitis 247, 718 encephalitis  718 equine encephalosis  718 equine infectious anemia, 719 elaeophorosis  719 filariasis  247, 586, 718, 719, 722 habronemiasis  719, 723 hemorrhagic disease, 718 722 hog cholera  719 Ilheus fever  718 Jamestown Canyon viral disease  718 Japanese encephalitis  718 leishmaniasis 247, 719, 724, 727, 728 Lyme disease  11, 12, 667 leucocytozoonosis  718, 719 loiasis 248, 719, 725 mal de caderas  719 malaria  13, 14, 247–249, 575, 586, 661, 662, 718, 722, 726, 732, 733, 767, 788 mansonelliasis  718, 719, 725 mastitis  248, 250 Mayaro fever  718 Murray Valley encephalitis  718 nagana  718, 723 onchocerciasis  718, 719, 725, 726, 730, 767 Oropouche fever  718, 721 Oroya fever  719

Index

Palyam viral disease  718 plague  13, 648, 662, 730, 767 Rift valley fever  718, 719 Ross River fever  718, 726 Saint Louis encephalitis, 718 sand fly fever  247, 719, 724 Semliki Forest encephalitis  718 stephanofilariasis  719, 723 streptothrichosis  719 surra  719 Tahyna fever  718 tularemia  718, 719, 725 typhus 13 Venezuelan equine encephalitis  718 verruga peruana  719 vesicular stomatitis  719 Wesselsbron disease  718 West Nile encephalitis  13, 247, 513, 662, 718, 719, 722, 732 western equine encephalitis  718 yellow fever  13, 247, 248, 653, 661, 662, 713, 718, 722, 726 diseases of plants  13, 660 bacterial wilt  359, 360 citrustristeza 661 Dutch elm disease  660, 671 tomato spotted wilt  661 dispersal  12, 22, 121, 312, 381, 391, 394, 479, 486, 642, 643, 651, 665, 769 displacement of species  664, 665 disruptive selection  18, 464, 535, 538 dissolved organic matter (DOM), 206 215 Distributed Generic Information Retrieval (DiGIR)  598 DNA hybridization  584 DNA sequencing. See sequencing of DNA

Dobzhansky, Theodosius  18, 502, 530 drugs from insects. See medicinal properties of insects drumming. See acoustic communication dung (see also coprophagous insects)  12, 93, 98–100, 104–106, 167, 181, 242, 243, 245, 249, 252, 348, 350, 352, 361, 378–381, 392, 663, 723, 750, 789

e East Scythian subregion, 147  180, 183 ecology  9, 14, 16, 20, 25, 55, 58, 85, 99, 129, 143, 436, 438, 464, 502–504, 513, 531, 536, 547, 548, 550, 552, 575, 577, 587, 595, 641, 642, 649, 669, 670, 714, 752, 753, 771, 776, 777 ecosystem engineers  12, 726 ectoparasites (and ectoparasitoids) 53, 208, 292, 437, 438, 442, 443, 605, 610, 644, 648, 652, 661, 723, 771, 788 Ecuador  71–73, 75, 85, 378, 585, 724, 725 edible insects. See entomophagy education  25, 59, 116, 128, 143, 220, 515, 521, 731, 775, 777 eggs of insects  16, 116, 206–211, 237, 244, 245, 252, 289, 296, 351, 352, 355, 359, 379, 437, 440–442, 577, 586, 604, 605, 627, 717, 721, 730 Egypt  100, 101, 292, 378, 419, 713 El Niño  126, 642 electrophoresis  586, 728

Encyclopedia of Life  515 endangered species  25, 127, 313, 464 Endangered Species Act  256 endemic species. See precinctive species endemism  99, 100, 114, 118, 119, 121–123, 154, 155, 169 endoparasitoids  243, 438, 439, 605, 788 endosymbionts  548, 583, 604, 665 England. See Britain Entomological Collections Network (ECN)  596 Entomological Society of Canada 53 Entomological Society of Washington 784 entomophagy, by humans  124, 239, 247, 378, 440, 486 eradication  124, 249, 357, 575, 644, 657–659, 673, 726 ethics 504 Ethiopia  101, 106 Ethiopian region. See Afrotropical region Europe  24, 49, 93, 95, 97, 101, 103, 141, 144, 146, 148, 154, 155, 158, 164, 168, 169, 174, 176, 177, 183, 219, 245, 249, 256, 297, 301, 345, 356, 360, 378, 392, 393, 427, 432, 442, 445, 465, 515, 537–539, 633, 634, 648, 649, 651–653, 655, 656, 658, 660, 662, 664, 667, 721, 733, 757, 772 Evolutionary Synthesis  529 exclusion of species  673 excretion 19 exotic species. See adventive species

859

860

Index

extinction  24, 114, 115, 120, 121, 123, 124, 171, 214, 255, 256, 356, 394, 467, 468, 489, 499, 506, 507, 511, 603, 604, 663, 668, 670, 726, 747, 748, 752, 755, 757, 760, 769, 770, 773, 777, 789, 789 extirpation  664, 668

f Far East of Russia  143, 146, 148, 162, 166–168, 172, 174–177, 179, 182, 345 Fauna Europaea  595 Fiji  111, 118, 122, 123, 251, 381, 444 filter feeding  727 fine particulate organic matter (FPOM)  206, 215 Finland 154 fire  58, 123, 125, 239, 251, 346, 359, 429, 556, 608, 642, 657, 659, 662–666, 674, 747 First Order Biota  65 Fitch, Asa  558, 627, 629, 630, 633 flight muscles  19, 229, 237, 253, 380 flight, insect  15, 19, 20, 126, 164, 173, 207, 229, 253, 254, 380, 434, 441, 469, 512, 553, 595, 642 flightless insects  124, 159, 209 Florida [USA]  47, 49, 58, 251, 292, 296, 611, 613, 643, 648, 651, 653, 656, 664, 666, 668, 775 Florissant shales  722 flower visitation  13, 243 fogging. See canopy fogging folklore, insects in  419 food webs  10, 22, 205, 212, 214, 215, 356, 432, 548, 665, 726, 757, 758

forensic entomology  23, 352, 584, 656 forestry  124, 246, 344, 346, 353, 357, 360, 395, 432, 445, 646, 647, 658, 671, 674, 771 fossils  22, 119, 357, 358, 423–426, 432–433, 426–433, 436, 468, 506, 507, 512, 517, 721, 769 fowlpox  718 Fox Glacier [New Zealand]  121 France, 94  162, 256, 653 Franz Joseph glacier [New Zealand] 126 fungivores 68, 84, 167, 243, 343, 350, 606

g Galápagos Islands  249, 303, 606, 648, 664, 726 galls, plant, 84  120, 164, 168, 229, 237, 246, 250, 252, 352, 419, 428, 430, 432, 439, 440, 481, 605, 628, 654 GenBank  549, 559, 577, 578, 586, 617 gene flow  531, 532, 535, 663 generalists, insect  158, 160, 174, 183, 246, 252, 297, 300, 479, 537, 610–612, 632, 663, 666, 668, 669, 725, 786 genetics  9, 14, 16, 18, 21, 244, 253, 254, 359, 381, 502, 504–506, 512, 514, 529, 535, 645, 727, 771, 777 genome sequencing. See sequencing of DNA genomes  507, 547, 551, 554, 555, 559, 730 georeferencing  596, 597, 599 Georgia [USA]  58, 653 Georgia, Republic of, 615 German Barcode of Life Network 578

Germany  94, 255, 256, 391, 392, 585, 653 Glacier National Park [USA] 11 glaciers  121, 127, 169, 229, 747 Global Biodiversity Assessment 96 Global Biodiversity Information Facility (GBIF)  97, 518, 599 Global Invasive Species Program (GISP) 673 global warming. See climate change Gobi Desert  150, 151, 152, 167, 181, 184–186, 185–186 Gondwanaland  104, 105 grasslands  12, 105, 121, 123, 152, 157, 170, 428, 439, 468 greenhouses  246, 250, 251, 294, 652 Greenland  436, 648 Guanacaste Conservation Area  427, 438, 584, 595 guilds 83, 84, 85, 772, 773 Guyana  582, 725

h habitat alteration  14, 218, 726 habitat destruction  24, 104, 256, 642, 670, 772, 777 habitat fragmentation  22, 218, 346, 603, 604 haematology. See blood feeding Haldane, J.B.S.  10, 16, 583 Hawaii [USA]  102, 244, 249, 251, 256, 295, 297, 510, 643, 648, 651, 653, 654, 656, 658, 661–664, 666, 668, 673 Hennig, William  19, 499–501, 503, 505, 509–511, 513, 514, 517, 533, 560 herbivores. See phytophagous insects

Index

Hesperian (evergreen forest) region, 147  172, 174, 179, 184 hilltopping  170, 242, 243 Himalayan mountains  144, 161, 169, 170, 174, 179 Hispaniola 627 human immunodeficiency virus (HIV)  248, 379 Holarctic region  243 holomorphology  500, 517 homeobox genes  17 homeotic mutations  17 homosequential sibling species  717, 727, 729, 734 honeydew  12, 124, 125, 234, 434, 444, 628, 656, 657, 666 Hong Kong  613 host race  536–539 host specificity  54, 58, 68, 70, 85, 118, 586, 733, 785, 786 hot springs  209, 240, 243, 346 Howard, Leland O.  670, 784, 786 human evolution  248, 713 Hungary, 94 hybridization  528, 531, 532, 535, 539, 550, 663, 730, 732, 734 hyperparasitoids  437–439, 605

i idiobionts 605 Illinois 629 imaginal discs  16, 17 immature stages of insects (larvae and pupae)  10–12, 19, 22, 47, 54, 56, 78, 82, 85, 103, 113, 116, 119, 120, 127, 152, 155, 157, 158, 160, 161, 166–168, 177, 181, 182, 206–208–212, 214, 217, 218, 229, 237,



239–253, 255, 256, 285, 288, 292, 295, 296, 300, 344–350, 352–360, 379, 380, 426, 430, 434, 436–440, 443, 463, 469, 476, 479–486, 507, 538, 577, 580, 605, 610, 611, 662, 664, 666, 669, 713, 717, 721–727, 730, 734, 757, 771 immigrant species. See adventive species incipient speciation. See speciation India  102, 161, 183, 293, 301, 302, 305, 575, 717, 768 individual insects, number of  1, 2, 9, 10, 427–428 Indonesia  304, 428, 714, 754, 788 Industrial melanism  18 Industrial Revolution  256 informatics. See bioinformatics inquilines  237, 354, 439 Insect Farming and Trading Agency (IFTA)  116 insect trade  378 insecticides. See pesticides Integrated Biodiversity Assessment Center (IBAC)  775, 776 Internal Transcribed Spacer regions (ITS1 and ITS2)  551, 557, 613–617 International Barcode of Life Project (IBOL)  382, 578 International Code of Zoological Nomenclature 598 International Convention on Biodiversity 93 International Nucleotide Sequence Database Collaborative 578 International Rice Research Institute (IRRI)  537, 538

intertidal zones. See salt‐water habitats intrinsic value of insects  749 introduced species. See adventive species invasive species. See adventive species Invasive Species Specialist Group 128 inventories  85, 96, 504, 514, 582, 634, 649, 772–775, 777, 786 Iran  144, 158 Irano‐Turanian subregion, 147  179, 184 Irian Jaya [Indonesia]  717 island biogeography  22, 727 isolating mechanisms  530, 535 Israel  148, 157, 161, 172, 292, 613, 615, 653 Italy  94, 143, 149, 345, 648, 653, 660

j Japan  144, 146, 168, 174, 176, 177, 179, 180, 237, 297, 312, 378, 540, 615, 648, 653, 659, 670 Java 112 jewelry, insects in  24 Jurassic Period  432

k Kamchatka Peninsula  160, 164 karyotypes  392, 435 Kazakhstan  18, 164, 166, 171, 172, 180 Kentucky, 344 Kenya  94, 100–102, 256, 653 keys, identification  4, 55, 83, 143, 148, 285, 292, 293, 295–297, 300–305, 308, 309, 348, 356, 430, 438–440, 442–444, 521, 577, 616, 630, 772 keystone species  13, 603, 666, 726, 749, 760

861

862

Index

kin selection  21 Kirby, William  783, 784, 786–789 kleptoparasitism 304, 442, 605 Kolyma River  155 Korea  174, 176, 179, 297, 615 Krasnodar [Russia]  141, 164, 172 Kyoto Convention  126

l La Crosse encephalitis 662, 718 Lady Glanville  787 Lake Baikal  163, 240 lakes  58, 70, 105, 205–212, 216, 240, 241, 250, 285, 287, 288–290, 347, 513, 721, 722 Laos 102 larvae. See immature stages of insects Latin America  429, 431, 717 Laurasia 148 leaf mining  351 Lebanon 148 lekking 244 life cycles  49, 210, 216, 312, 344, 381, 634, 769 Lincoln, Abraham  50 Linnaeus, Carolus (Carl von Linné)  528, 529, 627, 630, 631, 770, 783 livestock  13, 98, 99, 218, 247–249, 253, 256, 359, 361, 432, 586, 648, 661, 721, 723, 725, 729, 733, 789 logging  123, 218, 747, 768 Lombok 111 longevity, insect  56, 467 Lord Howe Island [Australia]  113–115, 120, 124 Lord of the Flies 257 lotic habitats. See streams

Louisiana [USA]  58, 247, 292 luciferases  379, 381

m Macaronesian subregion, 147 179 Macquarie Island [Australia] 117 macroinvertebrates  209, 212, 215, 216, 722, 724 Madagascar  104, 105, 119, 218, 353, 437, 484, 582 Madeira 179 maggot therapy  253 Malaise traps  300, 427, 433 Malaysia  102, 112, 516, 540, 585, 722, 788 Malpighian tubules  19, 728 Maori  113, 128 Maryland [USA]  630 Massachusetts [USA]  360, 667 maternal care  297, 308– 310, 349 mating. See reproductive behavior Mauritius 100–102 Mayflower 648 Mayr, Ernst  18, 510, 527, 529, 530, 532, 535, 770 medicinal properties of insects  23, 352, 379, 381, 725, 732 Mediterranean region  12, 168 megafauna  93, 256, 576, 722 Melanesia  121, 123 Mesozoic Era  432, 468 metapopulation dynamics  22 Mexico  47, 48, 285, 427, 582, 668, 725, 788 Michigan [USA]  360 microsatellites  614, 633 microscopy  219, 435, 510, 560, 630, 632 Middle Ages  430 Middle East  295, 310 migration  22, 25, 237, 468, 671, 776

military history  13, 248, 254 mimicry  21, 243, 300, 351, 443, 463–465, 481–484, 487 Minnesota [USA]  11, 382, 630 misidentification  612, 613, 729, 772 mitochondrial DNA (mtDNA)  381, 393, 467, 549, 552, 577 modeling  68, 96, 126, 128, 513, 657 Moldova 181 molecular techniques  122, 445, 500, 553, 614, 633, 663, 726, 728, 729 Mongolia, 150  151, 152, 158, 159, 161, 163, 166, 171, 172, 179–183, 185 monitoring 100 monocultures  24, 604, 610 monophagy. See host specificity monophyletic groups  426, 722 Montana [USA]  11 Morgan, Thomas Hunt  16, 632 Morocco 179 MorphBank 617 morphology  55, 312, 345, 348, 351, 390, 393, 428, 436–438, 440, 469, 481, 500, 501, 503, 507, 512–514, 517, 519, 528, 531, 536, 537, 548, 550, 552, 560, 576, 577, 587, 630, 632 morphospecies  68, 76, 79, 80, 82, 83, 85, 124, 528, 529, 531, 614, 717, 723, 733, 771, 774, 786 Moses 713 mountains  47, 57, 106, 144, 146, 154, 158, 159, 161, 164, 166, 169–171, 173, 180, 184, 394, 714 Mozambique, 94  101, 106 muscles. See flight muscles

Index

museum collections  96, 359, 390, 504, 613 mutualisms  21, 237, 252, 666, 757, 773 Myanmar 717 mycophages. See fungivores myiasis  248, 249, 661 myrmecochores 665 myrmecophiles 390 mythology, insects in  378

n Namib Desert  381 Namibia, 94  101, 103, 104, 152 Natal, 94 102 National Center for Biotechnology Information (NCBI) 578 National Invasive Species Council 673 National Invasive Species Information Center 653 natural enemies  11, 346, 361, 603, 604, 616, 649, 656, 659, 664, 665, 667, 669, 671, 729, 732 Nearctic region  47–59 (chapter 3), 243, 285, 392, 664, 715–716, 725 nectar  210, 211, 234, 242, 251, 256, 350, 486, 612 neighbor‐joining tree  551 neoteny  351, 478 Neotropical region  47, 210, 251, 430, 652, 721, 725 Nepal  149, 179, 182 nests of Hymenoptera  125, 209, 241, 245, 346, 429, 431, 442–445, 665 Netherlands  255, 313, 653, 748 Nevada [USA]  49 New Caledonia  111, 113, 118–124, 353, 354, 381

New England [USA]  251, 391, 653, 667, 673 New Guinea  69, 70, 104, 111, 112, 114, 116, 118, 121–123, 287, 301 New Jersey [USA]  360, 391, 662 New Mexico [USA]  54 New South Wales Threatened Species Conservation Act 120 New Systematics  514, 770 New York [USA]  94, 294, 360, 582, 597 New Zealand  111–114, 117–119, 121–129, 155, 216, 239, 348, 351, 353, 354, 356, 360, 429, 439, 477, 483, 648, 653, 655, 656, 658, 666, 672, 673 Newfoundland [Canada]  645, 651, 652 Nobel Prize  657 nomenclature  489, 509, 521, 528, 540, 549, 613, 770 nontarget species  14, 669 Norfolk Island [Australia] 120–121 North America  11, 12, 14, 23–25, 47–59 (chapter 3), 82, 83, 102, 121, 146, 168, 172, 209, 247, 279, 285, 293, 295, 297, 302–304, 306, 308, 309, 312, 345, 347, 355, 360, 361, 378, 381, 382, 389–393, 429, 439, 440, 442–445, 465, 466, 477, 486, 515, 539, 580, 585, 586, 612, 627–631, 633, 634, 641, 642, 644–646, 648, 651, 652, 654, 655, 657, 660, 661, 663–671, 674, 717, 724, 729–731, 771, 772, 788 Norway 155

Nova Scotia [Canada]  583, 651, 652, 660 nuclear genes  613 nucleotide sequencing. See sequencing of DNA nuisance insects  217, 246, 249–250, 289, 302, 305, 306, 349, 355, 432, 661, 721, 722, 724 number of individual insects. See individual insects, number of number of species. See species, number of nuptial gifts  242 nutrient spiraling (nutrient cycling)  12, 205, 206, 654, 663, 667

o oceans, insects on  144, 205, 289, 344, 645 oceans, scarcity of insects in  144, 205, 645 Ohio [USA]  360, 654 old‐growth forests  255 oligarchy hypothesis  72, 85, 86 omnivores  605, 606 Onchocerciasis Control Programme  731, 732 Ontario [Canada]  47, 58, 360, 382, 390–392, 610, 611, 612 oothecae 438 operational taxonomic unit (OTU) 587 optical character recognition (OCR) 597 Oriental region  144, 162, 169, 170, 179, 213, 243, 309, 445, 651 ornamental pests  295, 297 Orthrian (evergreen forest) region  147, 172, 174, 176, 179, 180 ouabain 19

863

864

Index

oviposition  116, 237, 242, 466, 478, 486, 538

p paedogenesis 237 Pakistan  102, 585, 717 palaeospecies 535 Palearctic region  47, 49, 104, 106, 141–187 (chapter 7), 281–284, 285, 537, 660, 715–716, 724 paleolimnology  9, 14 Panama, 70  248, 280, 346, 427, 725 Panama Canal  248 Papua New Guinea (PNG)  114–116, 118, 717 parasites  12, 14, 20, 68, 72, 98, 155, 167, 215, 229, 243, 245, 247, 337, 379, 426, 508, 535–537, 603–605, 611, 613, 616, 713, 721, 723–725, 767, 769 parasitoids  11, 14, 20, 24, 68, 164, 209, 211, 229, 241–246, 346, 349, 355, 390, 426, 434, 437–442, 463, 465, 466, 483, 536, 586, 603–618 (chapter 19), 628, 643, 665, 668, 670, 672, 757, 786 parataxonomists 771, 775–777 parthenogenesis  18, 159, 237, 344, 349, 507, 511, 534, 536, 576, 581 Patagonia 121 Paterson, Hugh  530, 535, 561 pathogens  14, 246, 247, 250, 359, 360, 655, 660–663, 674, 713, 721–725, 732, 733, 776 pederin  378, 379 Perú  69, 72, 73, 75, 294, 724 pest management  250, 603, 606, 608, 613, 614, 669, 768, 776

pesticides  14, 24, 25, 359, 381, 657, 730, 788 pests  14, 16, 22, 23, 49, 100–103, 124, 128, 129, 142, 160, 176, 218, 244, 246–251, 253, 293–295, 297, 302, 304–306, 308, 311, 312, 352–357, 359–361, 362–377, 419, 426, 432, 439–441, 445, 463, 464, 466, 480, 481, 484–487, 504, 513, 540, 575, 582, 583, 587, 603, 608, 610–612, 614, 616, 627, 628, 641, 644–646, 648, 649, 651–658, 660, 664, 665, 667, 672–674, 723–725, 729, 732, 734, 750, 769, 776, 777 pharmaceuticals  506, 789 phenetics 521 pheromones  21, 211, 360, 381, 537–539, 614, 657 Philippines 729 Phillip Island  121 phoresy  12, 21, 381 PhyloCode 521 phylogenetic species concept. See species concepts phylogenies  381, 436, 437, 501, 517, 533, 552, 555, 558, 559 physiology  9, 14, 16, 19, 21, 22, 254, 300, 312, 464, 486, 506, 670 phytophagous insects  11–13, 22, 54, 58, 68, 82, 84, 86, 114, 118, 119, 121, 122, 127, 142, 144, 148, 152, 154, 157–162, 164, 168, 170, 172–174, 176, 181, 182, 211, 214, 215, 217, 243–245, 296, 303, 304, 308, 309, 311, 312, 343, 346, 348–350, 356, 359, 361, 381, 436, 438, 439, 466, 508, 535–537, 539,



605, 606, 608, 633, 645, 654, 660, 663, 664, 667, 668, 748, 776, 786 phytotelmata  240, 241, 664, 721 pitfall traps  239, 433 Planetary Biodiversity Inventory (PBI)  512, 514, 517, 518 plastron. See respiration Pleistocene glaciations  111, 126, 179 Poland  164, 360 polarized light  380 pollination  12–14, 24, 65, 93, 97, 125, 251, 252, 357, 361, 432, 486, 660, 665, 666, 714, 757 pollution  70, 206, 215–219, 255, 346, 361, 655, 747, 772, 776, 777 polymerase chain reaction (PCR)  553–555, 558, 577, 617, 633 Polynesia  20, 664, 722 polyphyletic groups  714 polytene chromosomes  717, 728 Popper, Karl  509 population bottlenecks  16 Poulton, Edward  529, 530 Precautionary Principle  749, 753 precinctive species  18, 49, 100, 103–105, 112–115, 118–123, 125, 127–129, 143, 146, 148, 152, 154, 155, 158, 160, 162–164, 166, 168–170, 173, 174, 177, 179, 182–184, 249, 255, 256, 293, 353, 354, 360, 381, 390, 392, 477, 478, 481, 484, 487, 644, 653, 661, 663, 665, 666, 759 predators  10–12, 14, 20, 24, 25, 68, 72, 84, 124, 167, 181, 207–209, 211, 215,

Index



239, 241–243–246, 250, 256, 289, 292, 294–297, 299, 300, 311–313, 343, 347–351, 353–355, 379, 391, 431, 438, 440, 443–445, 463, 465, 476, 603, 605, 606, 628, 629, 643, 647, 656, 657, 665, 668, 672, 721, 725, 726, 757, 788 provisioning  12, 349, 444, 445, 605, 606 public health  247, 674, 783 pupation  116, 209, 211, 348, 378

q quarantine. See biosecurity Quebec [Canada]  360 Queen Elizabeth Islands [Canada] 56

r radiations  113, 114, 119–123, 148, 343, 468, 510 rainforests  67, 69, 72, 86, 99, 105, 114, 239 Ray, John  2, 783, 787 Red List of Threatened Species  114, 255, 383, 394, 749, 759, 789 refugia 169 Relational Database Management Systems (RDBMS) 96 relict taxa  105 religion, insects in  378 reproductive behavior  18, 21, 208, 209, 237, 239, 242, 244, 251, 288, 443, 477, 478, 530, 536, 538–540, 604, 729 reproductive isolation  18, 164, 467, 530–534, 536, 538, 539, 550–552, 576, 617, 729 resilin protein  15

resistance  360, 381, 537, 539, 641, 645, 661, 722, 730, 732, 758 respiration  205, 209, 210, 240, 288, 290 restriction fragment length polymorphisms (RFLP)  586, 632, 633 Réunion  101, 102 Rhode Island [USA]  58 ribosomal DNA  614 Riley, Charles Valentine  784 Rio Declaration of Biological Diversity and Sustainable Development 774 Rio Negro  71 Romania 585 Roosevelt, Theodore  504 Rosen, Warren G.  1 Ross, Ronald  245 Ruahine Range  124 Russia (see also Far East)  141, 142, 147, 149, 155, 157, 159, 167, 168, 171–173, 175, 176, 180–183, 667 Ryukyu Islands [Japan]  144

s Sahara Desert  144 Saharo‐Arabian subregion, 147 184 Saint Helena  304 saliva  23, 234, 253, 299 salivary glands  301, 728 salt‐water habitats  19, 166, 168, 207, 209, 211, 240, 241, 245, 250, 287, 288, 344, 347, 722, 728 sap‐feeding 479 saprophagy  349, 605 Saudi Arabia  722 savanna  100, 105, 106, 123 Say, Thomas  49 Sayan mountains  163, 170 Scandinavia 148 scarabiasis 379 scavenging  241, 296, 654

scent glands  209, 279 Scientific Committee on Problems of the Environment (SCOPE)  641, 673 Scythian (Steppe) region  147, 164, 172, 180 seashores 168 Second Order Biota  66 postmortem interval (PMI)  23, 379, 380, 586, 656 seed dispersal  10, 12, 350, 432, 665 seed predation  84, 170, 182, 243, 252, 302, 303, 306, 352, 354, 432, 440, 444, 605, 645, 654, 669 seepages (seeps)  115, 119, 205, 207, 209, 211, 240, 241 Senegal, 94 101 sequencing of DNA  4, 254, 382, 392, 482, 507–508, 519, 521, 547–561 (chapter 16), 575–585 (chapter 17), 601, 614, 616, 617, 633, 728, 730, 786 Serbia and Montenegro  653 Sethian (desert) region, 147  172, 183 sex determination  56, 381 sex ratios  56, 432 sexual dimorphism  443, 512 sexual selection  244, 464 Shannon index  772 Sharp, David  784 shellac 656 Siberia  146, 148, 163, 167, 172, 176, 180–183, 768 sibling species  2, 18, 20, 124, 219, 391–394, 467, 531, 534, 536–540, 575, 580–584, 604, 614–617, 633, 717, 724–734 sickle‐cell anemia  248 Sindbis fever, 718

865

866

Index

single nucleotide polymorphisms (SNPs)  555, 559, 560 sleeping sickness  13, 248, 586, 718, 723 Snares Islands [New Zealand] 117 social insects  120, 167, 348, 349, 381 soil arthropods  580 South Africa  12, 93, 94, 95–97, 99, 101, 103–107, 119, 175, 249, 296, 348, 354, 583, 655, 658, 665 South African National Biodiversity Institute (SANBI)  97, 107 South America  116, 119, 155, 217, 249, 345, 353–356, 436, 442, 444, 477, 478, 612, 613, 648, 657, 666, 721, 725, 726, 769 South Carolina [USA]  293, 661 South Korea. See Korea Southeast Asia  13, 114, 121, 122, 176, 353, 379, 381, 483, 532, 769, 788 Spain  148, 179, 256, 427, 653, 665 specialist insects  68, 72, 80, 84, 100, 101, 126, 295, 346, 359, 466, 535, 536, 538, 604, 610, 667, 670, 747, 748, 754, 758 speciation  18, 68, 69, 104, 381, 390, 463, 464, 467, 507, 510, 511, 528, 530, 532, 534–538, 550–552, 556, 617, 727, 732, 770, 771 Species 2000  96, 117 species complexes  540, 551, 614, 616, 633, 661, 717, 726, 728, 759 species concepts  18, 510, 511, 527–540 (chapter 15), 532, 534, 540, 550, 576, 587, 631, 633, 777

species richness  10, 49, 69, 70, 73, 99, 100, 117, 122, 148, 157, 158, 173, 229, 230, 348, 393, 464, 466, 467, 478, 483, 484, 576, 583, 603, 604, 606, 608, 612, 722, 733, 757, 758, 772–774, 786 species turnover  75, 76, 85 species, number of  1, 2, 3, 50, 51–52, 53, 55, 57, 98, 118, 144, 145–146, 186–187, 212–213, 280, 281–284, 337, 338–343, 420–422, 426–427, 597, 605, 631, 631–632, 715–716, 771, 783–790 (chapter 25) specific mate‐recognition system (SMRS)  529–532, 535, 538, 539 Spence, William  783, 784, 786, 787, 789 spermatophore 207 spontaneous generation  713 Sri Lanka  101, 102 stasipatric speciation. See speciation Stenopean region  147, 166, 172, 174–177, 180, 183 steppe  146, 148, 149, 152, 160, 161, 163, 164, 166, 170–174, 177, 180– 184, 653 stored‐product pests  355, 379, 443, 466, 646 streams  70, 71, 119, 123, 144, 146, 163, 180, 205–212, 216, 218, 219, 237, 240, 241, 243, 245, 250, 285, 287–290, 346, 438, 580, 721, 724 Stroganov Palace (Russia)  168 subsocial behavior (see maternal care) Sudan 292 Sulawesi (Celebes)  111, 112, 428, 616, 785

Sumatra 295 supercooling 20 superspecies 532 surveys, taxonomic  69, 100, 101, 103, 104, 114, 116, 118, 120, 172, 184, 254, 427, 548–550, 587, 614, 649, 664, 770 swarms, mating  237, 239, 242, 250, 627 Sweden, 94 359 swimming  207, 210, 211, 240, 288, 289, 380 Switzerland  143, 427, 652, 654, 664 symbiosis 381 sympatric speciation. See speciation synanthropic arthropods  769 synonymies  435, 631, 632, 785, 786 Systema Naturae  528, 770, 785 systematics  19, 50, 58, 59, 80, 280, 293, 299, 311, 348, 438, 467, 489, 500, 507, 508, 510, 522, 529, 533, 535, 547, 554, 560, 593, 601, 613, 617, 629, 631, 632, 671, 728–730, 770, 775–777

t taiga  146, 147, 156, 159, 160, 166, 167, 172–176 Taiga (Euro‐Siberian)  147, 176 Taiwan  102, 144, 310, 722 Tajikistan 166 Tanzania  100, 101 Tasmania  102, 111, 121, 125, 666 taxon pulse model  85 Taxonomic Databases Working Group (TDWG)  598 taxonomic impediment  129, 467, 500 taxonomy  50, 85, 86, 96, 97, 127, 143, 214, 285, 346,

Index



382, 390, 393–395, 435, 436, 444, 445, 464, 467, 489, 499–510, 512–515, 522, 523, 529, 536, 540, 547, 549, 551–554, 556, 559–561, 578, 582, 585, 599, 601, 607, 627, 630–632, 634, 671, 673, 713, 714, 717, 721, 725, 727–730, 733, 768, 770–772, 775–777, 786 termitophiles 390 Texas [USA]  47, 58, 98 Thailand  102, 287, 378, 427 Third Order Biota  66 threatened species  127, 773 Tibet  145, 169, 170 Tien Shan mountains  146, 155, 169, 170 Tonga  111, 122 Total Perspective Vortex  67 toxic shock  724 toxicity testing  215, 254 monitoring 673 Transcaucasia  148, 170, 172 transdetermination 17 transgenic arthropods  727 transposable elements  16 trapping 125 traumatic insemination  290, 292, 296 Trinidad and Tobago  659 Tristan da Cunha  648, 653 trophic levels  216, 604, 665, 670, 757 tropics  68, 105, 106, 154, 207, 213, 218, 248, 249, 285, 288, 299, 305, 308, 348, 353, 379, 428, 432, 444, 482, 487, 515, 612, 722, 726, 748 trypanosomiasis (see also nagana; sleeping sickness) 300, 718, 719 tundra  47, 146, 147, 157–159, 166, 167, 170, 171, 173, 177, 183, 722 Turkey  157, 788

Turkmenistan 187 Tuva [Russia]  163, 164, 170, 171, 180, 181, 183 type specimens  98, 560, 730

u

Uganda, 94 100 Ukraine  172, 180 undescribed species  9, 117, 152, 242, 246, 285, 337, 355, 393, 502, 515, 608, 616, 731, 771 United Kingdom (UK)  111, 216, 360, 583 United Nations  777 United States Department of Agriculture (USDA)  93, 101, 144, 250, 354, 357, 360, 627, 645, 775 United States of America (USA)  285, 382, 391, 393, 553, 554, 612, 659 Universal Earth Ethic  753 Ural mountains  163 urban environments  142, 168, 175, 250, 360, 361, 504, 655, 660, 769 urticaria 662

v Vanuatu (New Hebrides)  111, 118, 122, 123, 353 vectors of diseases  95, 154, 212, 214, 218, 219, 248, 249, 312, 347, 350, 355, 359, 584, 587, 660–662, 714, 717, 719, 723–726, 729–734, 769, 788 vectors (means of transport) 646–647 Venezuela  653, 661, 725 venom, insect  431 Vietnam  176, 180, 729 Virginia  293, 391 viviparity  237, 292, 381 Volga River  163 voucher  513, 550, 577, 578, 730, 731

w Waitomo 113 Wales [UK]  115, 120, 125, 360 Wallace, Alfred Russell  111, 114, 486, 529, 532, 535 Wallacea  112, 217 waterfalls  119, 240, 346, 348 weeds (plants)  24, 124, 125, 143, 144, 208, 214, 217, 251, 297, 356, 357, 361, 651, 656, 668, 669 West Indies  653, 668 West Scythian  147, 180 Westwood  249, 786 Western Hemisphere Immigrant Arthropod Database (WHIAD) 674 wildlife  13, 25, 245, 659, 661, 723, 726, 733, 750 Wilson, Edward O.  657, 714 wings of insects  15, 24, 104, 187, 208, 237, 239, 250, 253, 254, 279, 292, 293, 309, 311, 343, 349, 437, 438, 440, 442, 443, 465, 468, 469, 477, 481, 483, 484, 486, 487, 503, 508, 512, 583, 585, 630 wood borer  352, 353, 360, 660 World Conservation Monitoring Centre 770 World Health Organization  722, 724, 725, 731 World Heritage List  114 Wrangel Island [Russia]  160, 173

y Yakutia 163 Yemen 725 Yenisei River  146, 163, 180

z Zambia  101, 106 Zanzibar 100 Zimbabwe  94, 101

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Figure 4.12  Coleoptera taxa examined in Yasuni from 1994 to 2006. Images were taken with the EntoVision extended focus photography system (Alticinae and Cleridae not figured). For each taxon, the number of observed morphospecies (as of 2008) is listed, as well as predicted numbers of species based on accumulation curves and ICE (incidence‐based coverage estimator) calculations (Erwin et al. 2005).

Insect Biodiversity: Science and Society, Volume I, Second Edition. Edited by Robert G. Foottit and Peter H. Adler. © 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.

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Figure 7.2  Palearctic insects in natural habitats. (a) Calosoma sycophanta (L.) (Coleoptera: Carabidae) (Turkey) (photo A. Konstantinov). (b) Nemoptera sinuata Olivier (Neuroptera: Nemopteridae) (Turkey) (photo M. Volkovitsh). (c) Eristalis tenax L. (Diptera: Syrphidae) (Turkey) (photo A. Konstantinov). (d) Cryptocephalus duplicatus Suffrian (Coleoptera: Chrysomelidae) (Turkey) (photo A. Konstantinov). (e) Poecilimon sp. (Orthoptera: Tettigoniidae) (Turkey) (photo M. Volkovitsh). (f ) Capnodis carbonaria (Klug) (Coleoptera: Buprestidae) (Turkey) (photo M. Volkovitsh). (g) Cyphosoma euphraticum (Laporte and Gory) (Coleoptera: Buprestidae) (southern Russia) (photo M. Volkovitsh).

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Figure 7.3  Palearctic insects in natural habitats. (a) Julodis variolaris (Pallas) (Coleoptera: Buprestidae) (Kazakhstan) (photo M. Volkovitsh). (b) Julodella abeillei (Théry) (Coleoptera: Buprestidae) (Turkey) (photo M. Volkovitsh). (c) Mallosia armeniaca Pic (Coleoptera: Cerambycidae) (Turkey) (photo M. Volkovitsh). (d) Trigonoscelis schrencki Gebler (Coleoptera: Tenebrionidae) (Kazakhstan) (photo M. Volkovitsh). (e) Saga pedo Pallas (Orthoptera: Tettigoniidae) (Kazakhstan) (photo M. Volkovitsh). (f ) Piazomias sp. (Coleoptera: Curculionidae) (Kazakhstan) (photo M. Volkovitsh).

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Figure 9.1  Adult Diptera. (a) Tanyderidae (Araucoderus) habitus, dorsal view. (b) Axymyiidae (Axymyia), lateral view. (c) Limoniidae (Prionolabis) mating pair, oblique-dorsal view. (d) Bibionidae (Bibio) habitus, oblique-lateral view. (e) Culicidae (Culex) feeding on ranid frog. (f ) Empididae (Empis) habitus, lateral view. (g) Pipunculidae taking flight, oblique-lateral view. (h) Micropezidae (Grallipeza) habitus, lateral view. (i) Diopsidae (Teleopsis) head, frontal view. (j) Conopidae (Stylogaster) mating pair, lateral view. (k) Asilidae (Proctacanthus) feeding on dragonfly, oblique-dorsal view. (l) Sarcophagidae (Sarcophaga) habitus, dorsal view. (m) Scathophagidae (Scathophaga) habitus, oblique-lateral view. (n) Stratiomyidae habitus, lateral view. (o) Calliphoridae (Hemipyrellia) habitus, frontolateral view. Images by G.W.C. (a–c, h, i, m), S. Marshall (e–g, j, k), M. Rice (d), and I. Sivec (l, n, o).

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Figure 9.2  Larval Diptera. (a) Tipulidae (Epiphragma) habitus, dorsal (top) and ventral (bottom) views. (b) Axymyiidae (Axymyia) habitus dorsal view. (c) Nymphomyiidae (Nymphomyia) habitus lateral view. (d) Deuterophlebiidae (Deuterophlebia) habitus, dorsal view. (e) Psychodidae (Pericoma) habitus, lateral view. (f ) Blephariceridae (Horaia) habitus, dorsal (left) and ventral (right) views. (g) Calliphoridae (Lucilia) habitus, dorsal view. (h) Tephritidae (Eurosta) habitus, ventral view. (i) Syrphidae (Syrphus) feeding on aphids, dorsal view. (j) Syrphidae (Microdon) on glass, lateral view. (k) Sciomyzidae (Tetanocera) habitus, lateral view. (l) Stratiomyidae (Caloparyphus) habitus, dorsal view. Images by G.W.C. (a–c, e, f, h, k, l) and S. Marshall (d, g, i, j).

Figure 11.1  Examples of lesser‐known representatives of the four suborders of Coleoptera (clockwise from top left): Ptomaphagus hirtus (Tellkampf ) (Polyphaga) is found only in caves in Kentucky, USA; Lepicerus inaequalis Motschulsky (Myxophaga) lives in moist sand from Mexico to Venezuela; Arthropterus wilsoni (Westwood) (Adephaga) is associated with ants under bark and logs in southeastern Australia; and Rhipsideigma raffrayi (Fairmaire) (Archostemata) is found in rotten logs in the drier forests of Madagascar.

Figure 12.4  Lateral habitus views of representative families of Chalcidoidea (Hymenoptera). Images by Klaus Bolte. Top row: Tanaostigma stanleyi LaSalle (Tanaostigmatidae), Encyrtus fuscus (Howard) (Encyrtidae), Signiphora sp. (Signiphoridae). Second row: Brachymeria tibialis (Walker) (Chalcididae), Leucospis affinis Say (Leucospidae), Rotoita sp. (Rotoitidae). Third Row: Ormyrus vacciniicola Ashmead (Ormyridae), Kapala sulcifacies (Cameron) (Eucharitidae), Perilampus hyalinus Say (Perilampidae). Bottom Row: Elasmus atratus Howard (Eulophidae), Eulophus orgyiae (Fitch) (Eulophidae), Epiclerus nearcticus Yoshimoto (Tetracampidae).

Figure 23.1  The Kubusi stream damsel Metacnemis valida, a narrow‐range endemic in South Africa that is Red Listed as Endangered, as its stream habitats are being shaded out by invasive alien trees such as Acacia spp.

Figure 23.2  Non‐consumptive instrumental value can be the viewing of insects that delight us, such as this rare, paleoendemic white malachite Chlorolestes umbratus in the Harold Porter Nature Reserve, South Africa.

Figure 23.3  A significant approach to insect conservation is the use of set‐aside land in agro‐ forestry production landscapes. Shown here is a grassland ecological network in a pine plantation in South Africa. This remnant set‐aside land has great conservation value for a whole range of biodiversity while maintaining ecosystem processes such as the historic hydrology.