Acarology : proceedings of the 10th International Congress, [celebrated in Canberra, Australia, July 5-10, 1998) 9780643066588, 0643066586

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ACAROLOGY PROCEEDINGS OF THE 10TH INTERNATIONAL CONGRESS

R.B. Halliday, D.E. Walter, H.C. Proctor R.A. Norton, & M.J. Colloff [Editors]

ACAROLOGY PROCEEDINGS OF THE 10TH INTERNATIONAL CONGRESS

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ACAROLOGY PROCEEDINGS OF THE 10TH INTERNATIONAL CONGRESS

Editors R. B. Halliday

R. A. Norton

CSIRO Entomology GPO Box 1700 Canberra ACT 2601 Australia

SUNY–College of Environmental Science & Forestry 1 Forestry Drive Syracuse, New York USA 13210

D. E. Walter

M. J. Colloff

Department of Zoology & Entomology University of Queensland St Lucia Queensland 4072 Australia

CSIRO Entomology GPO Box 1700 Canberra ACT 2601 Australia

H. C. Proctor Australian School of Environmental Studies Griffith University Nathan Queensland 4111 Australia

All rights reserved. Except under the conditions described in the Australian Copyright Act 1968 and subsequent amendments, 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, duplicating or otherwise, without the prior permission of the copyright owner. Contact CSIRO PUBLISHING for all permission requests. National Library of Australia Cataloguing-in-Publication entry International Congress of Acarology (10th : 1998 : Canberra, Australia) Acarology : proceedings of the 10th International Congress Bibliography. Includes index. ISBN 0 643 06658 6 (hardback). ISBN 0 643 06980 1 (eBook). 1. Acarology – Congresses. I. Halliday, R. B. (Robert Bruce), 1950–. ACAROLOGY: PROCEEDINGS OF THE II. Title.

10TH INTERNATIONAL CONGRESS

595.42 Available from:

CSIRO PUBLISHING

150 Oxford Street (PO Box 1139) Collingwood VIC 3066 Australia Tel: Fax: Email: Web site:

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Set in Adobe Garamond and Adobe Gill Sans Cover photograph: Epicriopsis walteri Halliday (Ameroseiidae), from leaf litter at Lamington National Park, Queensland (photo D. E. Walter) Typeset by Desktop Concepts P/L, Melbourne Printed in Australia by Ligare This publication was generously supported by The Schlinger Foundation and ANIC fund.

CONTENTS

CONTENTS

Introduction: Past, Present and Future Acarology

1

250 years of Australian acarology

3

R. B. Halliday

Poising for a new century: diversification in acarology

17

Evert E. Lindquist

Taxonomy of New Zealand Prostigmata: Past, Present, and Future

35

Ting-Kui Qin and Rosa C. Henderson

Acarine Systematics and Phylogeny

41

The body segmentation of oribatid mites from a phylogenetic perspective

43

Gerd Weigmann

Phylogenetic relationships of Hypozetes (Acari: Tegoribatidae)

50

Valerie M. Behan-Pelletier

Systematic relationships of Nothrolohmanniidae, and the evolutionary plasticity of body form in Enarthronota (Acari: Oribatida) 58 Roy A. Norton

Historical ecology of the Acaridae (Acari): phylogenetic evidence for host and habitat shifts

76

Barry M. OConnor

Organismal patterns causing high potential for adaptive radiation in Parasitengonae (Acari: Prostigmata)

83

Andreas Wohltmann, Harald Witte and Ronald Olomski

Assessment of the usefulness of ribosomal 18S and mitochondrial COI sequences in Prostigmata phylogeny 100 Jürgen C. Otto and Kate J. Wilson

Acarine Biogeography and Biodiversity

111

Achilles and the mite: Zeno’s Paradox and rainforest mite diversity

113

David Evans Walter

Closely related species of Parasitengonae (Acari: Prostigmata) inhabiting the same areas: features facilitating coexistence 121 Andreas Wohltmann

Aquatic mites as bioindicators, with an Australian example

136

J. E. Growns

V

CONTENTS

Study of the diversity of Ptyctima (Acari: Oribatida) and quest for centres of its origin: the fauna of the Oriental and Australian regions

143

Wojciech Niedbala

Genetic markers and mite population biology

149

Maria Navajas

Evolutionary Ecology of Acarine Reproduction

153

Coercion and deceit: water mites (Acari: Hydracarina) and the study of intersexual conflict

155

Heather Proctor and Karen Wilkinson

Thelytokous reproduction in the family Acaridae (Astigmata)

170

Kimiko Okabe and Barry M. OConnor

Morphological adaptations associated with mate-guarding behaviour in the genus Hericia (Acari: Algophagidae) 176 Norman J. Fashing

Reproductive behaviour of the semi-aquatic mite Homocaligus cf. amphibius Wainstein, 1975 (Acari: Homocaligidae)

180

A. V. Tolstikov

Acarine Morphology and Ultrastructure

183

New morphological analysis of the bat wing mites of the genus Periglischrus (Acari: Spinturnicidae)

185

Juan B. Morales-Malacara

Functional morphology and fine structure of the female genital system in Typhlodromus spp. (Acari: Phytoseiidae)

196

G. Nuzzaci, A. Di Palma and P. Aldini

Anatomy and ultrastructure of the female reproductive system of Sarcoptes scabiei (Acari: Sarcoptidae) 203 Clifford E. Desch

The use of autofluorescence of the pharyngeal pump system in Pygmephoridae (Acari: Heterostigmata) as a new taxonomic aid

213

S. H. Coetzee and A. M. Camerik

Functional morphology of some leg sense organs in Pediculaster mesembrinae (Acari: Siteroptidae) and Phytoptus avellanae (Acari: Phytoptidae)

217

Enrico de Lillo and Pasquale Aldini

Ultrasonication, a tool for microdissection of astigmatic mites investigated by SEM

226

M. G. Walzl

Fine structure and mineralisation of cuticle in Enarthronota and Lohmannioidea (Acari: Oribatida) 230 Gerd Alberti, Roy A. Norton and Jörn Kasbohm

VI

CONTENTS

The leg chaetotaxy of Caligonellidae (Prostigmata: Raphignathoidea)

242

Sabina Fajardo Swift

An alarm pheromone function of the secretion from the nymphal stage of the oribatid mite Nothrus palustris (C. L. Koch) (Acari: Nothridae)

250

Satoshi Shimano, Tomoyo Sakata, Yoshikatsu Mizutani, Yasumasa Kuwahara and Jun-ichi Aoki

Ecology and Biology of Soil Mites

253

Reproductive and nutritional biology of Tectocepheus velatus (Acari: Tectocepheidae) in different biotopes

255

Martina Hajmová and Jaroslav Smrz

Feeding habits of the Indian oribatid mites Hoplophthiracarus rimosus (Phthiracaridae) and Lohmannia n. sp. (Lohmanniidae) and their role in decomposition

262

N. Ramani and M. A. Haq

Effects of moisture regime on the nutritional biology of saprophagous soil mites (Oribatida and Acaridida)

266

Jaroslav Smrz

Talus formations – remarkable biotopes for acarological research, with examples from the Rhagidiidae (Acari: Prostigmata) 269 Miloslav Zacharda

Myriad Mesostigmata associated with log-inhabiting arthropods

272

Owen Seeman

Soil Acari response to deforestation and fire in a Central Amazon forest

277

Lucille M. K. Antony

Niche segregation and can-openers: Scydmaenid beetles as predators of armoured mites in Australia 283 Freerk Molleman and David Evans Walter

Interactions between Mites and Plants

289

The false spider mite Brevipalpus obovatus Donnadieu (Acari: Tenuipalpidae): host-related biology, seasonal abundance, and control

291

Hussien A. Rezk

Comparison of feeding damage by redlegged earth mite Halotydeus destructor (Tucker) (Acari: Penthaleidae) to different grain legume species as an indicator of potentially resistant lines

295

A. Liu and T. J. Ridsdill-Smith

Densities of Panonychus ulmi (Acari: Tetranychidae) and Aculus schlechtendali (Acari: Eriophyidae) on three apple cultivars in western Norway

300

Mofakhar S. Hossain and Torstein Solhøy

Physiological and biochemical responses of plants to spider mite feeding

306

Anna Tomczyk

VII

CONTENTS

Host plant resistance in cotton to spider mites

314

L. J. Wilson and V. O. Sadras

Resistance in pasture legumes to redlegged earth mite Halotydeus destructor (Tucker) (Acari: Penthaleidae)

328

S. F. Wang, T. J. Ridsdill-Smith and E. L. Ghisalberti

Host plant susceptibility to eriophyid mites used for weed biological control

342

J. M. Cullen and D. T. Briese

Effect of nutrients and salinity on the incidence of Petrobia latens (Müller) (Prostigmata: Tetranychidae)

349

Ashok Sharma and Mahendra Sharma

The life history and population development of Rhyncaphytoptus negundivagrans Farkas (Acari: Diptilomiopidae)

352

S. K. Ozman

Movement of the two-spotted spider mite Tetranychus urticae Koch and the Kanzawa spider mite T. kanzawai Kishida (Acari: Tetranychidae) in a watermelon-pea cropping system

355

Masahiko Morishita

Life cycle and behaviour of the coconut mite Neocypholaelaps stridulans (Evans) (Acari: Ameroseiidae) in India 361 M. A. Haq

Biology and Control of Mites in Horticulture

367

Brevipalpus mites (Acari: Tenuipalpidae) as vectors of plant viruses

369

C. M. Chagas, V. Rossetti, A. Colariccio, O. Lovisolo, E. W. Kitajima and C. C. Childers

Relative abundance and seasonal occurrence of mites in the family Tydeidae on citrus in Florida

376

H. Aguilar, C. C. Childers and W. C. Welbourn

Managing spider mites in field-grown strawberries using Phytoseiulus persimilis and the ‘pest-in-first’ technique

381

G. K. Waite

Control of two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) on edible crops in glasshouses using two interacting species of predatory mite

387

A. S. Rott and D. J. Ponsonby

Platyphytoptus pineae Castagnoli, an eriophyid mite described from Pinus pinae L. in Italy, present in Central Brazil

392

D. Návia and C. H. W. Flechtmann

A quantitative study of phoresy in Microdispus lambi (Acari: Microdispidae) in eastern Australia Alan Clift and Mary Ann Terras

VIII

394

CONTENTS

Development and use of a method to measure aldicarb resistance in Tetranychus urticae Koch (Acari: Tetranychidae) from cotton in Australia

399

Grant A. Herron, Victor E. Edge, Jeanette Rophail and Lewis Wilson

Seasonal abundance of the Banks grass mite Oligonychus pratensis (Banks) (Prostigmata: Tetranychidae) and a predatory mite, and their response to sulfur treatment on commercial date palms Phoenyx dactilifera L. in southern California

403

Carmen Gispert, Charles Farrar and Thomas M. Perring

Life cycle, food consumption, and seasonal occurrence of Scolothrips indicus (Thysanoptera: Aeolothripidae) on eggplant

409

Chyi-Chen Ho and Wen-Hwa Chen

Does the Lorryia formosa Cooreman (Acari: Prostigmata: Tydeidae) population visit or reside on citrus foliage?

413

M. H. Badii, A. E. Flores, G. Ponce, J. Landeros and H. Quiroz

Species and population densities of mites on Jujube

419

V. Charanasri and M. Kongchuensin

Predator prey interactions between Chrysoperla carnea Stephens (Neuroptera: Chrysopidae) and Tetranychus neocaledonicus (André) (Acari: Tetranychidae) on okra

423

H. Sharanabasava and M. Manjunatha

Acarine Biological Control Agents

427

Biological control of tetranychid mites in South African apple orchards

429

K. L. Pringle

History and perspectives of biological mite control in Australian horticulture using exotic and native phytoseiids

436

David G. James

An overview of investigations into the use of predatory mites to control the lucerne flea Sminthurus viridis (L.) (Collembola: Sminthuridae) in Tasmanian pastures

444

J. E. Ireson, R. J. Holloway and W. S. Chatterton

The use and usefulness of mites in biological control of weeds

453

D. T. Briese and J. M. Cullen

Advances in understanding the ecology of Euseius (Mesostigmata: Phytoseiidae) species on citrus in southern Africa

464

Tim G. Grout

Effect of temperature on the rate of development, fecundity, longevity, sex ratio and mortality of Amblyseius coccosocius Ghai and Menon (Acari: Phytoseiidae), an important biocontrol agent against tea red spider mite in India 470 K. Saha, A. K. Somchoudhury, P. K. Sarkar and S. K. Gupta

Trends in research on acarine biocontrol agents

473

Uri Gerson

IX

CONTENTS

Phytoseiids with potential for commercial exploitation in Australia

476

Marilyn Y. Steiner and Stephen Goodwin

A conspectus of natural enemies of phytophagous mites and mites as potential biocontrol agents of agricultural pests in India

484

S. K. Gupta

Functional responses of Amblyseius ovalis (Evans) (Acari: Phytoseiidae) on Tetranychus urticae Koch (Prostigmata: Tetranychidae): effects of prey stages

498

Chain-ing T. Shih and Chain-Ji Wang

Functional responses of Amblyseius ovalis (Evans) (Acari: Phytoseiidae) on Tetranychus urticae Koch (Acari: Tetranychidae): effects of substrate component and size of rearing arena 506 Chain-ji Wang and Chain-ing T. Shih

Biological control of two-spotted spider mite in strawberries by the predatory mite Amblyseius longispinosus (Evans) (Acari: Phytoseiidae)

513

M. Kongchuensin, V. Charanasri, T. Kulpiyawat and P. Khantonthong

Can Phytoseiulus persimilis (Acari: Phytoseiidae) invade rainforest fragments when its preferred prey Tetranychus urticae is present?

518

Saskia Kriesch, Golam Nabi Azam and David Evans Walter

Phytoseiid faunas of natural and agricultural ecosystems in Sicily

522

S. Ragusa-di Chiara and H. Tsolakis

The phytoseiid mites of major crops in China

530

Wei-nan Wu and Wen-ming Lan

Medical and Veterinary Acarology

533

The medical significance of Acari in Australia

535

Richard C. Russell

Ticks as vectors of zoonotic pathogens in Europe

547

J. S. Gray and O. Kahl

A progress report on scabies in humans

552

John R. H. Andrews

Allergenicity of the predator dust mite Cheyletus tenuipilis (Acari: Cheyletidae): a preliminary study

558

M. J. A. Morris and J. Rimmer

Survey of the mite fauna associated with Apis spp. in Kerala, southern India

565

K. Sumangala and M. A. Haq

Potential oribatid mite vectors of cestode parasites in Kerala, India

569

M. A. Haq

Population dynamics of acarid mites in two different types of poultry raising systems in Germany Rainer Ehrnsberger and Jacek Dabert

X

576

CONTENTS

Ectoparasitic mites on Heteromys gaumeri in the south of Yucatan, Mexico

583

M. M. T. Quintero, M. Vargas, B. S. Hernández, P. García and N. J. Otero

Mites associated with nests of Neotoma albigula Hartley, 1894 (Rodentia: Muridae) in Durango, México

586

Griselda Montiel-Parra, Gabriel A. Villegas-Guzman, Margarita Vargas, and Oscar J. Polaco

Ecology and Physiology of Ticks

595

Water balance of unfed Argas reflexus (Acari: Argasidae) maintained in an experimental attic

597

Hans Dautel

Juvenile hormone regulation of metamorphosis and reproduction in ticks: a critical re-examination of the evidence and a new perspective

604

R. Michael Roe, Vasant Kallapur, Paul A. Neese, Charles S. Apperson and Daniel E. Sonenshine

Bioassay, radiobiosynthesis, and GC/MS analysis of juvenile hormone in ticks: a new perspective

612

Paul A. Neese, Vasant L. Kallapur, Charles S. Apperson, Daniel E. Sonenshine and R. Michael Roe

Characterisation of immunoglobulin G binding proteins in male Rhipicephalus appendiculatus ticks

618

H. Wang and P. A. Nuttall

Vitellogenin and its synthesis in the soft ticks

622

DeMar Taylor and Yasuo Chinzei

Regulated secretion of tick salivary gland protein

628

Alan S. Bowman, Ying Qian, Jing Yuan and John R. Sauer

Clustering effects of Lone Star Ticks (Amblyomma americanum) in nature: implications for precision-targeting of acaricides

634

Jerome Goddard

Tick immunity to microbial infections: control of representative bacteria in the hard tick Dermacentor variabilis (Acari: Ixodidae)

638

Robert Johns, Shane Ceraul, Daniel E. Sonenshine and Wayne L. Hynes

Variations in numbers of Rhipicephalus appendiculatus (Acari: Ixodidae) tick populations feeding on cattle infected with Theileria parva parva (Apicomplexa: Theileridae) parasites 645 Sammy S. Kubasu, Josephat I. Shililu and Mwase E. T. Enala

XI

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CONTENTS

PREFACE

Mites are one of the most diverse groups of living organisms. With that diversity comes a host of interactions between mites and the terrestrial, freshwater and marine organisms with which they live. Many of these interactions have economic consequences for humankind, and most offer novel perspectives on basic questions in modern biology. For the last forty years, the International Congress of Acarology has been the primary forum for reviewing progress in the study of mites at the world level, and for world acarologists to gather for an exchange of current research results. This volume presents the papers that were given at the 10th International Congress of Acarology, Canberra, Australia, July 5–10, 1998. This historic occasion was the first time the Congress had been held in the Southern Hemisphere, and gave Australasian acarologists a rare chance to host the international acarological community on their home soil. The 59 Australian delegates were joined by strong contingents from USA (30), Japan (19), Netherlands (14) and the UK (14), and 80 people from another 24 countries. We were particularly pleased to see so many delegates from Asia, and we hope this visit will help to strengthen the relationship between Australia and our neighbouring countries. Delegates presented 187 spoken papers and 69 posters over the 5 days. The diversity of mites is paralleled by the diversity of the types of research of which they form a part. Mites have been the subject for research effort in fields that span virtually the whole of biological science, and this breadth of research is reflected in the range of subjects presented here. The area that is covered in greatest depth is the relationship between crop pests and their host plants, and methods for their control. Other subjects covered include human and livestock diseases transmitted by ticks and other parasitic mites, the interactions between mites and plants, the latest developments in the control of mite pests, the use of genetic markers in population studies, mites as indicators of habitat quality and environmental change, the evolutionary ecology of dispersal and reproduction, advances in understanding acarine diversity and systematics, and the use of modern techniques in identifying mites and teaching acarology. The total of 90 papers includes contributions by leading acarologists from 30 countries, as well as a younger generation of researchers, teachers of acarology, and students, who deal with all aspects of acarology at a truly international level. As well as presenting the results of current research projects, the papers include major reviews of the current state of the science of acarology, and establish priorities for future research. Many important events took place during the week of the Congress apart from the formal sessions. On Monday evening

CSIRO announced the publication of three books and a CD-ROM documenting the Australian mite fauna, which represents a significant advance in the science of acarology in this country. Wednesday evening was devoted to a workshop on the application of modern computer technology to acarology, with the demonstration of a range of software packages for the storage and analysis of acarological data, and for interactive identification, which will surely become much more popular very quickly. At the closing ceremony on Friday Reinhart Schuster and Gwilym Evans were made Honorary Life Members of the Congress, and Roy Norton presided over a discussion to adopt some changes to the rules under which the Congress operates. The meeting also passed a resolution asking the Government of the United States to restore a position or positions for acarine systematics associated with the collections of the National Museum of Natural History, through either the USDA Systematic Entomology Laboratory or the Smithsonian Institution. Delegates from China and Mexico announced their intention to prepare bids to host the 11th Congress in 2002, and and it was eventually decided that Acarology XI will be held in the city of Merida, Mexico. The Secretary, Juan B. Morales-Malacara, should be contacted for details, at [email protected]. Prizes were awarded to Freerk Molleman (Netherlands) for the best poster presented by a student, entitled ‘Niche segregation and can openers: Scydmaenid beetles as predators of armoured mites in Australia’, and equal first prizes for the best paper presented by a student were awarded to Bas Pels (Netherlands) for his paper ‘Predator dispersal before and after overexploitation of patches with prey’ and Andrew Weeks (Australia) for ‘Intense selection in clones of an obligate parthenogenic mite without sexual relatives’. A special encouragement award was made to Mr Michael Morris of Australia (aged 16) for his presentation ‘Biology and behaviour of Cheyletus tenuipilis in house dust’. The papers published here were put through a full scale process of peer review. Every paper was reviewed by at least two anonymous referees, and after revision, every paper was re-examined and edited by at least two of the scientific editors. The study of mites requires a degree of attention to detail that could threaten to fragment the science of acarology into blocs of researchers separated by barriers of language, location, or history. The International Congresses, and the publication of their Proceedings, are a vital means of breaking these barriers, in establishing international collaboration and communication, and in promoting understanding throughout the whole research community.

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Contents

ACKNOWLEDGEMENTS

The organisation of an International Congress is a major undertaking, and cannot be done without the support of an enthusiastic team. The Program Committee consisted of Dave Walter (Chair, Brisbane), Steve Barker (Brisbane), Matt Colloff (Canberra), Heather Proctor (Brisbane), Marjorie Hoy (Gainesville), Marilyn Houck (Lubbock), Danuta Kropczynska Linkiewicz (Warsaw), and Zhi-Qiang Zhang (London). The members of the Local Organising Committee were Steve Barker, Matt Colloff, Heather Proctor, James Ridsdill-Smith (Perth), David James (Yanco), Graham Osler (Sydney), Glenn Hunt (Sydney), and Richard Russell (Sydney). We were also privileged to have Roy Norton in Canberra on a long-term visit during the planning stages, and he generously gave us the benefit of his experience. I am also very grateful to all the people who agreed to organise and chair sessions, who contributed their time generously in the refereeing of manuscripts, to the staff of the Australian Convention and Travel Service, who cheerfully solved myriad non-scientific problems, and to all of our employers for allowing us to devote our time to this project.

A grant from the Australian Agency for International Development allowed some people to attend who would otherwise not have been able to do so. Financial support was also provided by the Australian National University, the Cooperative Research Centre for Legumes in Australian Agriculture, and the Australian Quarantine and Inspection Service. Refreshments at the poster session on Tuesday evening were generously hosted by Indira Publishing House. On behalf of the Local Organising Committee, I thank all of these organisations for their support. I finally offer my very sincere thanks to Ebbe Nielsen, the Director of the Australian National Insect Collection, for his constant encouragement and support during the preparation of these Proceedings, and especially to the Schlinger Foundation, for a very generous grant to help with the cost of publication. Without their support we would not have been able to produce these Proceedings in this attractive and accessible form. Bruce Halliday President, 10th International Congress of Acarology Canberra, July 2000

The compact disk accompanying this volume contains the full text and illustrations of every paper in the volume, in pdf format. The disk may be used to make printouts of any paper, as an alternative to the publisher’s supplying reprints. XIV

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ACAROLOGY: PROCEEDINGS OF THE 10TH INTERNATIONAL CONGRESS

INTRODUCTION: PAST, PRESENT AND FUTURE ACAROLOGY

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

250 YEARS OF AUSTRALIAN ACAROLOGY R. B. Halliday

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CSIRO Entomology, GPO Box 1700, Canberra ACT 2601, Australia, [email protected]

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Abstract This paper reviews some of the historical trends in the development of acarology in Australia, from Linnaeus to the present. It includes brief biographies of some of the important acarologists of the past (Tryon, Womersley, Southcott, Lee, Roberts), and a few examples of long term research projects, on ectoparasites of grasshoppers, redlegged earth mite Halotydeus destructor, and cattle tick Boophilus microplus. The Australian mite fauna is shown to include 2,620 described and named species, and is estimated to include a total of 20,000 species.

INTRODUCTION

BEGINNINGS

The purpose of this paper is to review the historical development of the science of acarology in Australia over a 250 year period beginning with Linnaeus in 1758. It represents an edited transcript of the Presidential Address to the 10th International Congress of Acarology. The premise is that this historical information is a valuable aid to understanding the position that the science had reached in 1998. It does not pretend to present a complete list of the people who have worked on Australian mites, with a biography of each, and details of their achievements. Instead it uses a few selected examples to demonstrate some of the things that happened in the past, some of the species that have had a long and complex research history, and some of the characters and institutions that were involved. In the attempt, it draws freely on the information compiled by Southcott (1982), which should be consulted for greater detail and a more comprehensive bibliography. Further biographical and bibliographical information about some of the people mentioned can also be found in Musgrave (1932). A complete list of the Australian mite fauna and a bibliography of the associated literature can be found in Halliday (1998).

The first mite to be described from Australia was a tick collected from a lizard during Captain Cook’s voyage of exploration in the ship Endeavour in 1770 (type locality ‘Nova Hollandia’). That is not surprising, since Australia has a particularly rich fauna of lizards, which would have made a strong impression on the early European explorers. The tick in question was returned to the British Musuem and described by Fabricius (1775) as Acarus undatus, now known as Aponomma undatum. It took over 30 years for the second species to be recognised, and that was a species of scabies mite (Sarcoptes sp.) collected from a wombat from Tasmania. It was collected in 1804 but not described until almost 80 years later, as Sarcoptes scabiei var wombati Railliet (1893). The only new species of mites that were described between 1800 and 1850 were 5 species of ticks described by 5 different authors, 4 of them from lizards – Ixodes australasiae Fabricius 1805, Aponomma hydrosauri (Denny 1843), Ixodes coxalis Gervais 1842, 3

R. B. Halliday

and Amblyomma triguttatum Koch 1844, and one from the platypus, Ixodes ornithorhynchi Lucas 1846. In the 25 years following 1850, most of the new species that were being described were still ticks, and those were being described at the rate of only one or two a year, still mostly from lizards, most of them from around Brisbane. The most important paper from this period is that of L. Koch (1867). The first paper of any substance on the Australian fauna was published by Giovanni Canestrini (1884). He recorded 15 species belonging to 12 genera. Thirteen of those species were new, and the other two Canestrini recognised as species that had been described from Malaysia by Thorell. This was the first paper that dealt with Australian mites that were not ectoparasites of vertebrates – Canestrini described a range of Mesostigmata, Acaridae, and Uropodina, as well as ticks and parasitic Trombidiidae. Canestrini found these mites in a collection of insects from Queensland in the estate of the entomologist Francesco Pullè, at the University of Padua in 1883. All the mites he described were either parasitic or phoretic on insects, or were found in the vials that had had insects in them. The Mesostigmata in this collection are Trigynaspida, Uropodina, and Laelapidae, the Astigmata are hypopodes, and the specimen of Trombidiidae is a parasitic larva from a cerambycid beetle. Also in the mid 1880s, a group of French acarologists led by Trouessart and Mégnin was working on a vigorous program of describing feather mites from birds that been brought back to the Paris Museum from all over the world. Their collections included a wide range of birds from New Guinea, so Trouessart and others described a large number of species of feather mites from there. Many of those species were also found to occur in Australia, either at the time or subsequently (Mégnin and Trouessart, 1884a, 1884b, 1884c, and other papers by Mégnin and Trouessart cited by Halliday, 1998). The next group that received attention was the Halacaridae. The German plankton collecting expedition of 1890 collected halacarids from many sites, including some species from the coasts of Australia, and these were described by Lohmann (1893, 1909).

1898), and he was also responsible for describing Aculops lycopersici Tryon (1917), one of the important eriophyid pests of the tomato. Further details of Tryon’s life and work can be found in Mather (1986).

EARLY 20TH CENTURY All the work that had been done on the Australian mites up to 1906 was reviewed and catalogued by Rainbow (1906). Rainbow was an Englishman who arrived in Australia in 1883, and served for over 20 years as Entomologist at the Australian Museum in Sydney (Musgrave 1932). He published on a range of insects and arachnids, but his main contribution to acarology was the 1906 catalogue, in which he listed 102 species of mites known from Australia at that time. More than half of those were parasites of vertebrates, either ticks or feather mites, which had been found on their Australian hosts in European museums. For the most part Rainbow’s catalogue simply repeated published information in a fairly uncritical way, but he did describe some new species, mainly of Erythraeidae, and as a result he was honoured by the erythraeid genus that bears his name, Rainbowia Southcott (1961a). Apart from the descriptions, bibliographic references, and other catalogue data, Rainbow added selected passages of text about mite biology and classification. His information was mainly derived from North American work by Banks (1904), but, this was the first time this sort of information covering a wide range of mite groups had been published in Australia. Taxonomic work on Australian ticks continued in Europe during the early part of the 20th Century, and a large number of Australian species date from the period 1899 to 1920 (e.g. Neumann 1901, 1910; Nuttall and Warburton 1908, 1911, 1915; Cooper and Robinson 1908). The next significant contribution, in terms of the number of new species described, was a paper by the American entomologist Nathan Banks (1916), describing a collection of mites associated with ants that had been sent to him by Arthur Lea when he was Government Entomologist in Tasmania. In this paper Banks recorded no fewer than 38 species of myrmecophilous mites, all but two of them new species. They are mostly Mesostigmata, including some trigynaspids and uropodines, with some Prostigmata and Astigmata. His descriptions are brief and the illustrations are not detailed, and all of these species require redescription.

All the research described so far was done in Europe by Europeans, working on material that had come from Australia to the European Museums. The first exception came in the 1880s when Australian farmers noticed damage to their crops being caused by what we now know were spider mites and eriophyids.

HERBERT WOMERSLEY

The results of this phase of agricultural acarology were summarised by Tryon (1889), in a book that included a survey of insect and fungus pests of Australian crops. Tryon was Assistant Curator in the Queensland Museum in Brisbane, and later became Entomologist in the Queensland Department of Agriculture. As State Entomologist he worked on a wide range of insects, and his publications include work on tobacco beetles, hessian fly, scale insects, fruit piercing moths, and termites, as well as mites (Southcott 1982; Musgrave 1932). His contributions to acarology include descriptions of a tarsonemid and an unidentifiable species of Astigmata associated with a disease of pineapples (Tryon

Probably the name that comes up more often than any other in conversations about Australian acarology is Herbert Womersley. Detailed biographical and bibliographical information can be found in the obituaries written by Southcott (especially Southcott 1963, 1964) and in the history by Upton (1997), and the following summary is derived from those sources. Womersley was an Englishman, born in Lancashire in 1889. His father was an amateur lepidopterist, who encouraged his son’s interest in entomology. As a child he also met Abraham Flatters, who was one of the founders of the firm Flatters and Garnett, manufacturers of entomological equipment, including microscopes. Under Flatters’

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supervision, Womersley took night school courses at the Manchester School of Technology, including courses in how to prepare and examine biological specimens. In 1907, at the age of 18, Womersley took a job as an apprentice chemist. In his spare time he was already collecting flies in a systematic way, and observing new records for the British fauna. At around this time he also used his training in microscopy to make a collection of Collembola and other insects and mount them on slides. During the First World War Womersley served in the St John’s Ambulance Brigade and joined the Royal Army Medical Corps. In that position he served as a bacteriologist and pharmacist, and eventually found his training as a chemist being used in factories making explosives and solvents for the Chemical Corps of the Royal Engineers. In 1920 he returned to industrial chemistry, this time in the soap industry in Bristol in southern England. There he resumed his work in entomology, especially concentrating on Collembola and other wingless insects such as silverfish, and he published a series of papers on wingless insects of southern England through the 1920s (e.g. Womersley 1927a, 1927b). He joined the Royal Entomological Society and the Linnean Society of London, and resolved to take up entomology as a full time profession as soon as an opportunity arose. That opportunity came in 1929. In that year Womersley met R. J. Tillyard, who was Chief of the CSIR Division of Economic Entomology (the predecessor of CSIRO Entomology). Tillyard had gone to England looking for young entomologists, and came to the conclusion that Womersley was a suitable candidate. He offered Womersley a job as entomologist in Australia, and asked him to look at two pests that were causing extensive damage to pastures here, namely the Collembolan Sminthurus viridis (Sminthuridae), and the redlegged earth mite Halotydeus destructor (Penthaleidae). Tillyard first asked Womersley to spend a period at the British Museum for most of 1930, specifically to make a study of mites and Collembola, to make a reference collection, and to make himself familiar with their identification. After his period in London Womersley and his family moved to Australia, and on the way they stopped for a few weeks in South Africa. While there, he was very impressed by the degree of diversity of the South African mite fauna. He eventually arrived in Western Australia in late 1930. During the late 1920s and early 1930s Womersley was continuing with his taxonomic work on silverfish and Collembola, and producing a steady stream of publications on the results. One of those papers, Womersley (1932), was a preliminary account of some Collembola from Australia, which is noteworthy because it was the first taxonomic publication published by CSIR. By this time, 1932, he was coming to the end of his 3 year appointment with CSIR, and the organisations’s funding situation was such that term appointments were not being renewed. In fact Womersley’s appointment was the last one the Division made for several years, and there was talk at the time that the Division of Ecomomic Entomology would be disbanded.

Womersley therefore accepted a position he had been offered as entomologist in the South Australian Museum in Adelaide. He was appointed at the beginning of 1933, and spent the rest of his career there until he retired in 1954. When he retired he was given the special title of Acarologist, and later Honorary Acarologist, a position that he held until he died in 1962. During his period of 30 years at the South Australian Museum he published 150 papers on mite taxonomy, covering an amazingly diverse range of groups. They include important work on the trombidiids, listrophorids, sarcoptids, phytoseiids, macrochelids, and trigynaspids (see bibliography in Southcott 1963). He also worked on descriptions of the mites from one of the early Australian trips to the Antarctic, that of Sir Douglas Mawson in 1911 (Womersley 1937). His biggest and most important work was his 1952 monograph on the trombiculids of the Asia-Pacific region, nearly 700 pages of taxonomy that was motivated by the importance of these groups as the vector of scrub typhus (Womersley 1952). He provided specialist taxonomic advice to both the Australian and United States Armies, and continued to play an important role in providing taxonomic support and identification of chiggers during research on the epidemiology of scrub typhus throughout the 1940s and 1950s all over southeast Asia. His work in these areas was eventually brought together in a series of papers on Malaysian Parasites, published in 1957 by the Institute of Medical Research in Kuala Lumpur, with the support of the United States Medical Research Unit and a grant from the United States Public Health Service (Womersley and Audy 1957). At the same time as publishing all this work on mites, he continued up until 1953 in working on other groups of animals, including spiders, harvestmen, centipedes, flies, and wingless insects. He served actively in the Royal Society of South Australia, where he occupied various positions including Secretary, Treasurer, VicePresident, and President, and he represented the Royal Society of South Australia as an advisor to Government on National Parks and nature conservation. When his major work on trombiculids was finally finished, he began to publish an increasing amount of work on Mesostigmata, and through the mid to late 1950s he produced a series of papers on Phytoseiidae, Macrochelidae, Laelapidae, and Ologamasidae, which provide the essential starting point for more recent work on these groups. He managed to produce work on all these groups despite suffering from glaucoma, which was treated surgically, but which caused him increasing loss of sight, until his death in 1962.

THE GRASSHOPPER MITE PROJECT In 1934 the farmers and graziers of New South Wales asked CSIR Division of Economic Entomology to study the grasshoppers that were causing extensive damage to their crops and pastures (Upton 1997). The Division appointed Dr Ken Key in 1936, and asked him to investigate the habits and ecology of pest grasshoppers, with the objective of eventually finding methods to control them. That project led to Key’s lifetime of work in grasshopper taxonomy, which continued until he retired in 1994. By the late 1940s Key had assembled a vast collection of grasshoppers from all over Australia. He and his team collected thousands of specimens from

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many remote places, and the specimens are now in the Australian National Insect Collection. Key observed that a high proportion of the grasshoppers he collected were carrying ectoparasitic mites, and decided that something should be done to find out what part these mites played in the biology of their hosts. There was no acarologist in Canberra at the time, so Key approached Womersley at the South Australian Museum, to investigate the possibility of collaborating in research on the taxonomy of these mites. Womersley was not able to accept that invitation, but by that time Key and his staff had built up a collection of over 4000 slides of grasshopper mites, and CSIRO was anxious to have work done on them. At that time there was a medical practitioner in Adelaide, Ron Southcott, who had already shown an interest in Trombidiform mites, and in 1959 CSIRO approached him to take on the taxonomic work on the mites from grasshoppers. The original plan was that it would take about 18 months for Southcott to sort out and describe the mites. In fact the number of specimens kept on growing, and the taxonomic problems kept on multiplying, to the stage where the project eventually took more than 30 years, and is still not finished. During the 40 years he was working on this project Southcott published an impressive string of taxonomic papers on the Australian Erythraeidae, Trombidiidae, and Trombellidae, drawing heavily on the specimens Key had sent him (including Southcott 1961a, 1961b, 1966, 1972, 1986a, 1986b, 1986c, 1991). During the latter part of that 40 years of collaboration, Key began to publish a parallel series of biological papers on the geographic distribution and host range of the mites, based on the taxonomic data that Southcott was providing (e.g. Key 1990, 1991, 1994, Key and Southcott 1986). The mites are now back in the ANIC, and the work that was published on them probably represents the biggest body of data anywhere on the ectoparasitic mites associated with a group of invertebrate hosts. Even though an enormous amount of work has already been done on this project, there is still much that remains unfinished, and many specimens that have not yet been identified. The most important groups that still need work are the erythraeid genus Leptus and the family Podapolipidae, which are represented in the collection by hundreds of specimens that have been sorted but not described, or not sorted at all.

RON SOUTHCOTT Ron Southcott was born in Adelaide in May 1918. That is significant because it makes him the first native-born Australian to have a major impact on acarology in this country. He spent his childhood in the eastern suburbs of Adelaide, and even as a young child he was making observations on the insects and plants he found around him. It was very natural that he should come into contact with Womersley, and soon started collecting insects for him. Among the things that caught the eye of the young Southcott were the red velvet mites of the family Trombidiidae (Halliday and Pearn 1998). Womersley rewarded the young man by naming a mite after him – Microtrombidium southcotti, which Southcott had collected in the hills behind Adelaide in 1934 (Womersley 1934). This

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honour was enough to excite the young Southcott, who was then 16 years old, and to stimulate his interest in mites that would last the rest of his life. One of the observations that Southcott made very early in his career was of some mites that he found skating around on the surface of the water in some cattle troughs near his home. These he gave to Womersley, who described them as Speleognathus australis. In the description Womersley incorrectly stated that they had been collected in moss, and it took many years before he eventually admitted his mistake. This incident is described by Southcott (1986d). Southcott also learned from Womersley the arts of microscopy and illustration, and he quickly developed the distinctive style of drawing that anyone who has looked at his work will recognise. In 1937 Southcott decided that his career opportunities in zoology were limited, and enrolled in a medical degree at the University of Adelaide. Throughout his degree he continued collecting and rearing mites to study their life cycles and behaviour. He quickly realised that if his biological observations were to mean anything at all, he would have to become a taxonomist as well, and with Womersley’s help, he did exactly that. Their one and only joint paper was a revision of the Smarididae, published in 1941, which was Southcott’s first publication in acarology (Womersley and Southcott 1941). Southcott then joined the Army and practised as a Medical Officer, but throughout his service he used his spare time to collect mites and insects, especially ectoparasitic mites from kangaroos and other wildlife. Among the wildlife he collected were some grasshoppers that were parasitised by larval erythraeids, which he eventually described, and which eventually led to the grasshopper mite project described above. Southcott took the opportunity to extend his medical training by taking a course in tropical medicine and hygiene at the University of Sydney, which included courses in medical entomology and acarology. One of the instructors in that course was Frank Taylor, who introduced Southcott to the Linnean Society of New South Wales. In the Proceedings of the Linnean Society Southcott published a steady stream of papers for over 30 years. They included a series of papers published in 1946 that collected together most of his observations on the families Erythraeidae and Trombidiidae (Southcott 1946a, 1946b, 1946c). In the early 1950s Southcott published some small papers on Trombidioid mites while he practised medicine at the Adelaide Children’s Hospital. In 1961 he published his massive revision of the Erythraeidae (Southcott 1961a), which eventually formed the basis of his Doctor of Science degree from the University of Adelaide. Through the 1960s and 1970s Southcott continued his work on the taxonomy of Trombidiform mites, and kept producing a steady stream of major revisions. He also found time to pursue an amazing range of other interests, particularly using his medical training to produce a string of papers on the medical effects of plants and animals. He published substantial works on poisonous plants, toxic and venomous fishes, the medical effects of jellyfish,

250 YEARS OF AUSTRALIAN ACAROLOGY

sea anemones, sponges, caterpillars, moths and butterflies, and on hallucinogenic and toxic mushrooms (Covacevich et al., 1987). During the 1970s he published a series of major papers on the medical effects of mites and spiders in the Australian region, which remain the definitive work on this subject (Southcott 1976). On the basis of his knowledge of these subjects, he was made a special consultant to the South Australian Poisons Information Centre, and an advisor to the Adelaide Children’s Hospital. For a more extensive account of Southcott’s life and work, see Halliday and Pearn (1999), and for a description of his work with the box jellyfish, see Underhill (1987).

SOUTH AUSTRALIAN MUSEUM Herbert Womersley made his major contributions to Australian acarology while he was working at the South Australian Musuem. Although Ron Southcott was never actually employed by the Museum, he was an Honorary Research Associate there for most of his career, Chairman of the Museum’s Board of Trustees for nearly 10 years, and his collection of specimens is kept there. One of the other early figures at the South Australian Museum that is of interest to acarology is Stanley Hirst. Hirst started his career at the British Musuem in London, and while he was there he published on taxonomy of parasitic mites that were being sent to the Museum from all over the world (Musgrave 1932). In 1927 he moved to Australia to a position at the University of Adelaide, and spent the last few years of his career working next door at the South Australian Musuem. Like Southcott, he published on medical and veterinary acarology, especially on trombiculids and erythraeids, and to a lesser extent on parasitic mesostigmata (e.g. Hirst 1929, 1930, 1931). The dynasty of acarologists at the South Australian Musuem continued with the appointment of David Lee (Southcott 1982). Lee was born in Trinidad but spent most of his childhood in Britain. He started working on Mesostigmata at the British Museum under the supervision of G. O. Evans, and it was there that he developed his enthusiasm for leg chaetotaxy. David moved to Adelaide in 1964 and started work on the taxonomy and biology of soil mites. At first he worked on Mesostigmata, especially the Rhodacaridae, but the family as he knew it has since been broken up, so most of the species he worked on are now in the Ologamasidae, which seem to be unusually diverse and abundant here (Lee 1970). In the middle of the 1970s he switched his attention to the oribatid fauna of South Australia, partly because the oribatid fauna of Australia at that time was almost completely unstudied. Throughout the 1980s and early 1990s he produced a series of major publications on the Australian oribatids that form the basis of current work on oribatids in Canberra and in Sydney (e.g. Lee 1981, 1982, 1985). Further detail on Lee’s contributions can be found in Colloff and Halliday (1998). With the combined contributions of Womersley, Hirst, Southcott, and Lee, the South Australian Museum was the most important centre of taxonomic acarology in Australia for over 50 years. There is no acarologist there now, but the collection that all these people put together is probably the most comprehensive mite collection in Australia.

REDLEGGED EARTH MITE Herbert Womersley’s first research project on the Australian mite fauna was on the taxonomy and biology of the redlegged earth mite Halotydeus destructor (Tucker) (Penthaleidae). Since then many people have spent a great deal of time working on this species and the community to which it belongs. Taxonomic and ecological research on this species has had a very long and complex history, which demonstrates many of the successes and pitfalls of research in acarology. H. destructor is a major pest that causes many millions of dollars worth of damage to leguminous pastures in southern Australia every year. These pastures are the basis of the sheep and cattle industries over most of southern Australia, and also form a critical component of crop and pasture rotation systems. This mite also feeds directly on crop plants, such as canola and seed legumes, but it will feed on almost any crop and cause serious losses of productivity (reviewed by Ridsdill-Smith 1997). The taxonomic history of this species has been analysed in detail by Halliday (1991) and Qin and Halliday (1996a), and only the salient points will be repeated here. The redlegged earth mite first appeared in the scientific literature in a paper by Jack (1908), who referred to it as the Earth Flea, and pointed out that some farmers also knew it as the Sand flea or the redlegged spider. He described its life history and biology, and he also described the damage it was causing to vegetables in the Cape Province of South Africa, but did not give it a scientific name. This and subsequent events in the synonymy of this species are summarised below : Halotydeus destructor (Tucker) Earth Flea (Aardvloi), Sand flea, Redlegged spider: Jack 1908 Penthaleus sp. : Banks 1915 Earth Flea : Newman 1920 Notophallus bicolor Froggatt sensu Newman 1923 Penthaleus destructor Tucker 1925 (Black sand mite) Penthaleus destructor Jack : Newman 1925 Penthaleus destructor Jack : Anonymous 1929 Halotydaeus destructor (Tucker) : Anonymous 1930 (sic) Halotydeus destructor (Tucker) : Womersley 1933; Swan 1934 Halotydeus destructor (Tucker) : Qin and Halliday, 1996a The next time it was mentioned in the literature appears to be by Banks (1915), who referred to the South African Earth Flea as an unidentified species of Penthaleus. It was first recognised in Australia by Newman (1920), referring to it as the Earth Flea, and it appears likely that it was accidentally introduced into Australia from a ship in about 1917. Later Newman (1923) referred to it as Notophallus bicolor Froggatt, which had been described from New South Wales in 1921. At the same time Newman coined the name Red Legged Velvet Earth Mite for the species that occurred in Western Australia.

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Tucker (1925) described the Earth Flea taxonomically, gave it the new name Penthaleus destructor, and also coined the new common name, Black Sand Mite. In the process of doing that Tucker said that Jack in his 1908 paper had referred to the species as Penthaleus destructor, but had not given a description of it. Unfortunately Tucker was mistaken on both counts – Jack did describe the general appearance of the species, but did not use the name Penthaleus destructor, or any other scientific name. Newman (1925) realised that the redlegged earth mite of Western Australia was not the same as Froggatt’s species from New South Wales, and began referring to the Western Australian species as Penthaleus destructor (Jack). We now know that Froggatt’s species from New South Wales was actually a quite different species, which is known in Australia as the blue oat mite and in the United States as the winter grain mite Penthaleus major (Dugés) (Qin and Halliday 1996b). Newman (1925) added to the confusion by referring to a publication by ‘W. E. Jacker’, which keyed and described the Black Sand Mite Penthaleus destructor. There is no such person as W. E. Jacker, and Newman may have been confusing Jack and Tucker. Anonymous (1929) published brief notes on its biology and life cycle, and pointed out that it had the potential to develop into a dangerous pest, referring to it as Penthaleus destructor Jack. Anonymous (1930) then corrected the authorship of the name, and placed the species in the Berlese genus Halotydeus, after he had received advice from Womersley. Womersley (1933) then published on it in as Halotydeus destructor, but it was left to Swan (1934) to produce a reasonably complete analysis of its nomenclatural history and a thorough summary of its life cycle. The existence of males

Halliday (1991) discussed the confusion that arose over the mode of reproduction of this species. In summary, Jack (1908) described the male as being smaller than the female, and having an abdomen that was tapering rather than rounded. Newman (1925) published photographs labelled ‘adult male’ and ‘adult female’, which agreed with Jack’s analysis. However Womersley (1933) stated that males of redlegged earth mite had not been seen, and quoted Tucker (1925) as stating that the species was parthenogenetic. Statements that there were no males in the species can be found in the literature as recently as Meyer (1981), apparently derived from Tucker’s (1925) statement. Tucker (1925) did say that he had seen ‘several cases of apparent parthenogenesis’, and he also said that copulation had never been observed, but this is easy to explain by non-copulatory sperm transfer, using spermatophores. Solomon (1937) had already observed specimens of H. destructor spinning webs, noted that there were ‘small globules of water-like fluid spaced at intervals along the threads’, and thought that the specimens producing these webs were probably males. He suggested at the time that the webbing contained, or was composed of, spermatophores, perhaps with spermatozoa in the fluid droplets (Halliday 1991). It was not until much later that the male of this species was properly described (Baker 1995). Attempts to control the pest

There was an early attempt to use biological control to reduce the damage caused by redlegged earth mite, but the project was ham8

pered by mistakes and misunderstandings. Womersley (1933) thought that redlegged earth mite had been introduced into South Africa, and suggested a search for potential natural enemies in Mediterranean coast of France. A search for predatory mites was made in clover pastures in southern France, and a species was found that looked promising. It was identified as a species of Anystis (Wallace 1981). Although no redlegged earth mites were found there, this predator was feeding on another pest Penthaleid, Penthaleus major, so it was thought to be potentially useful. In 1938 CSIR staff in France collected large numbers of this Anystis and prepared them for shipment to Australia. The predator was then identified as Anystis baccarum, which Womersley pointed out was already widespread in southern Australia, so there was no point in introducing it. The shipment of predators was cancelled, and the biological control project was abandoned (Otto and Halliday 1991). Research on redlegged earth mite in Western Australia in the late 1930s was being led by K. R. Norris. The research effort there was devoted to the biology and life cycle of the mite (Norris 1950), its population fluctuations (Norris 1938), and measurements of how much damage it was causing (Norris 1944). This stage of the work included trials with a wide range of the insecticides that were in use at the time, including carbolic acid, tobacco dust, lime sulphur, naphthalene, derris dust, and pyrethrum (Norris 1943). However, in the late 1940s the strategies used for controlling H. destructor, like many other pests, were dramatically changed by the appearance of DDT and the other new chemical pesticides. In the early 1950s, CSIRO, as it was now called, was testing these pesticides against H. destructor and other pests of pasture, and it was very quickly realised that these chemicals also killed beneficial predatory mites and could actually lead to an increase in the pest population (Wallace 1954). M. M. H. Wallace continued the work on chemical pesticides that Norris had started a few years earlier. He did extensive experiments on the effects of DDT, and also tried the other new insecticides that were coming on to the market in the 1950s, like parathion, and then malathion (Wallace 1960). Apart from redlegged earth mite, Wallace was also looking at another important pasture pest, the Collembolan known as the lucerne flea, Sminthurus viridis. He showed that there were two species of bdellids that could have a significant effect on populations of lucerne flea, and found that there were large areas of Australia where there were no bdellids. By contrast, lucerne flea was not an important pest in Europe, but there were large numbers of bdellids in Europe that did not occur in Australia (Wallace 1981). Wallace’s work on the biology and control of pasture pests included a major taxonomic study of the Bdellidae (Wallace and Mahon 1973, 1976). Wallace’s next attempt to control lucerne flea was a trip to Europe to look for its natural enemies. What he found was a bdellid, Neomolgus capillatus, that fed on lucerne flea, and that occurred in the right habitats and the right climatic areas, so he introduced this species into Australia in 1965. During those same field trips in southern Europe, he was making observations on other predators as well, including the species of Anystis that other people had looked at almost 30 years earlier. The thing that caught his eye

250 YEARS OF AUSTRALIAN ACAROLOGY

about this species was that it was abundant in clover pastures, and that in those habitats it was preying on the pest mite Penthaleus major. He knew that this mite had previously been identified as Anystis baccarum, and also that Anystis baccarum was never very abundant in Australia, but occurred in cultivated gardens and orchards, not in clover pastures. That aroused his suspicions, and he soon proved that the French species was not Anystis baccarum, did not exist in Australia, and was in fact an undescribed species which he called Anystis species A. On the basis of that observation, he decided to reverse the decision that had been made in 1938 to abandon this biological control program, and introduced Anystis species A into Australia in 1965 (Wallace 1981). Anystis species A was originally unidentified, then misidentified as Anystis baccarum, then referred to as Anystis species A for nearly 30 years, then identified as Anystis salicinus by some authors, and was eventually described as a new species Anystis wallacei Otto (1992). This is a case of a biological control project that was held up for 30 years because the natural enemy had been misidentified.

STENEOTARSONEMUS BANCROFTI Another early example of research on an agricultural pest mite occurred in the sugar industry. Sugar was first planted in Australia in 1825 in an area that is now the city of Brisbane, but which at the time was a convict colony. By the 1870s there were increasing reports of a disease called rust, because its symptoms included the appearance of red or brown spots on the leaves of the plants (Griggs 1995). These would spread and eventually cause the whole plant to die and fall over. There were a variety of explanations for the cause of the disease, including sudden changes of weather, poor soil, and inadequate drainage. In 1875 a group of sugar growers asked for help from the Professor of Chemistry at Sydney University, Archibald Liversidge. Liversidge examined some diseased plant material and found it to be infested with a fungus disease, but more interestingly, he also observed that there was a mite feeding on the fungus (Liversidge 1876). The problem was then taken up by a schoolteacher and keen amateur naturalist, by the name of Joseph Bancroft. Bancroft examined samples of infested sugar, and observed both the fungus and the mites, and presented his observations in a report to the Queensland Parliament (Bancroft 1877). It can be seen from Bancroft’s illustration that the mite involved is a tarsonemid. Bancroft did not name the species, but he did send some material to Kew Gardens in London for identification. In 1890, the English acarologist A. D. Michael examined this material and described the mite as Tarsonemus bancrofti Michael 1890. Shortly after that Hirst (1912) recognised a mite doing similar things to sugar cane in the West Indies, which he described as Tarsonemus spinipes. It was only as recently as 1954 when Robert Beer was revising the Tarsonemids on a world-wide scale that he realised the Australian mite and the West Indian mite were one and the same, now known as Steneotarsonemus bancrofti (Michael) (Beer 1954).

CATTLE TICK One of the other species of mites that has occupied the attention of a large number of Australian acarologists for many years is the

cattle tick Boophilus microplus. The species was described by Canestrini (1887) from South America, but it is virtually cosmopolitan, and by the time it was described it had already reached Australia. It was introduced into northern Australia through a shipment of cattle that arrived in Darwin in 1872. At first the tick infesting cattle in the Northern Territory was identified as Rhipicephalus annulatus, and was listed under that name in Rainbow’s 1906 catalogue. It was also described as a new species Rhipicephalus australis by Fuller (1899). In 1917 the Commonwealth Advisory Council of Science and Industry published its first Bulletin, Cattle Tick in Australia (Upton 1997). Roberts (1934) recognised that the Australian cattle tick was the same as the Canestrini species, and that this was also the same as the species known in the United States as Ixodes bovis. Meanwhile the tick was spreading in northern Australia. By 1900 it had spread into Western Australia and Queensland, and soon after that it reached northern New South Wales, which gave it a total range in Australia of about 4 million square kilometres (Angus 1997). The research on this tick passed through a series of phases once again reflecting the technology that was available at the time. In the 1920s cattle were dipped in solutions of arsenic in a variety of formulations, but by the early 1940s resistance to arsenic started to appear, and by the middle of the 1940s arsenic was being replaced by DDT. Then at the end of the 1940s chlordane, dieldrin and parathion were added to the list, with the inevitable result that resistance to these eventually appeared as well (Angus 1997). A second economically important species of tick in Australia is the paralysis tick Ixodes holocyclus, which occurs in a narrow strip down the east coast of Australia, from north Queensland to Victoria. It causes major health problems for humans and dogs, due to a paralysis reaction to its saliva, and it may be a vector of some other diseases as well (Russell, Hudson, this volume).

F. H. S. ROBERTS The dominant name in tick systematics in Australia is F. H. S. Roberts. He was born in Queensland, and started his career there with some work on biological control of weeds with the Comonwealth Prickly Pear Board in the 1920s, and then moved to the Queensland Department of Agriculture and Stock as entomologist and parasitologist. He took an interest in the taxonomy of bombyliid flies, and his revision of the family is still in use today (Roberts 1928–1929). During the 1930s he surveyed the biology and systematics of a variety of veterinary parasites, including lice, mange mites, intestinal worms, fleas, and ticks, on all livestock species, and he brought together his work in all of these areas in his book Insects Affecting Livestock (Roberts 1952). His interests in ticks gradually grew until by the middle of the 1950s he was publishing on nothing else, and through the 1960s he produced a series of revisions of one tick genus after another, and summarised all of that work in his book Australian Ticks (Roberts 1970), written after he retired, and which is still the definitive monograph on the subject. There has been very little change in tick taxonomy in this country over the last 25 years, with only a handful of new species descriptions, giving Australia a total of about 80 known species (Halliday 1998). 9

R. B. Halliday

NEW SOUTH WALES AGRICULTURE One of the other institutions that has made an important contribution to the study of mites in this country is a government department now known as Agriculture New South Wales. The first important name in the organisation is that of Walter Froggatt. Froggatt was Government Entomologist at the Department of Agriculture from 1896 until he retired in 1923, and after that he continued working as Forest Entomologist to the New South Wales Forestry Commission. He was an amazingly productive publisher of research in entomology, with over 400 publications to his name between 1890 and 1937, covering everything from sawflies and coccids to caterpillars, termites and sheep blowfly (Musgrave 1932). He also managed to produce some papers on mites, and during the process he corresponded with Berlese in Florence, and sent specimens to him for identification. After Froggatt, mite research continued at the Department of Agriculture’s Biological and Chemical Research Institute at Rydalmere, a suburb of Sydney. It was not until 1975 that the first full-time acarologist, Eberhard Schicha, was appointed (Schicha 1984). Schicha had the title of Curator of the insect and mite collection of the New South Wales Department of Agriculture, which is now one of the more important entomological collections in Australia. As Curator, he was responsible for supervising the enormous numbers of requests for identification and information that the Department received. He felt strongly that identification services could not be provided in a satisfactory way unless they were supported by taxonomic research, and he especially drew attention to the fact that there were large numbers of economically important insects and mites that had never been worked on in a systematic way. Soon after he was appointed, Schicha began research on spider mites in the important apple growing areas around the city of Bathurst. Their natural enemies in the family Phytoseiidae dominated his research for the next 20 years. He set about identifying and describing the native phytoseiids and comparing them with foreign and introduced species. That process produced a long string of papers that culminated in his publication of a major revision of the phytoseiid fauna of Australia and surrounding regions (Schicha 1987). In the same western Sydney institution, Alan Clift and his colleagues were working on mites associated with mushrooms (e.g. Clift and Toffolon 1981), and others people were working on chemical control of a variety of mites (e.g. Levot 1993). The institute was also intimately involved with the major quarantine station in Sydney, and they can number among their achievements the successful interception of both Varroa jacobsoni and Acarapis woodi on honeybees (Schicha and Loudon 1980), both of which are still absent from Australia.

THE AUSTRALIAN MUSEUM Another important research institution in Sydney is the Australian Museum. From here Rainbow published his important catalogue of the Australian mites (Rainbow 1906). He was succeeded at the Australian Museum by Anthony Musgrave.

10

Musgrave started at the Museum in 1910 as a library assistant, but he also found time to work on a variety of insect groups, and became Assistant Entomologist, under Rainbow’s supervision. He eventually combined his background as a librarian with his training in entomology to produce the piece of work that he is most remembered for, his 1932 Bibliography of Australian Entomology (Musgrave 1932). Apart from being a bibliography, this extraordinary book is a compendium of biographical and historical information on over 1000 people who had contributed to Australian entomology to that time. He planned to produce a companion volume on acarologists and arachnologists, but it was never published, and parts of it exist only as unpublished notes and a card index. Current acarological research at the Australian Museum centres on the Oribatida (e.g. Hunt 1996, Hunt et al., 1998).

QUEENSLAND INSTITUTE OF MEDICAL RESEARCH The Queensland Institute of Medical Research was established by Dr Edward Derrick, who led the Queensland State Department of Health Microbiology Laboratory from 1935. Derrick was responsible for research into a variety of tropical diseases, especially rickettsial and viral diseases such as scrub typhus. The Institute was formally established in 1945 and quickly became one of the most important medical research institutions in Australia. These days it occupies a site in the grounds of the Royal Brisbane Hospital, next door to the medical school of The University of Queensland (Queensland Insitute of Medical Research 1998). As part of their program on mite-borne disease, the Institute appointed Bob Domrow in 1955, to work on the taxonomy and biology of ectoparasitic mites of vertebrates. Bob Domrow had a profound effect on the science of acarology in this country. His career lasted nearly 40 years, from 1955 until his retirement in 1988 and beyond. In that time he published over 150 papers dealing with every group of parasitic mites, and a wide range of non-parasitic groups as well. Like Womersley and Southcott before him, Bob Domrow worked for a time in Malaysia, and published extensively on the parasite fauna of southeast Asia as well as Australia. When he was no longer publishing original research results, Domrow produced a series of catalogues of the Australian parasitic mite fauna, that bring together all the results of his own lifetime’s work, as well as all the information published by other people all the way back to Linnaeus. These are comprehensive catalogues on the family Trombiculidae (Domrow and Lester 1985), on parasitic Mesostigmata (Domrow 1988), on other groups of the Prostigmata (Domrow 1991), and Astigmata (Domrow 1992). Together these catalogues total nearly 500 pages, and include quite a few species that had a complicated history, with many synonyms and misidentifications.

CSIRO ENTOMOLOGY CSIRO Entomology has had a long history of acarological research, since it was established in 1928. Some of its long-term projects have been on the redlegged earth mite and cattle tick, as described above. Recent spinoffs from the redlegged earth mite project have included studies of the taxonomy and biology of the Anystidae (Otto 1992; Otto and Halliday 1991) and a comprehensive revision of the Australian Eupodoidea (Qin and Halliday

250 YEARS OF AUSTRALIAN ACAROLOGY

Table 1

Number of described species in Australia before and after modern revisions. (Reprinted slightly modified with permission from ‘Nature and Human Society’, copyright 2000 by the National Academy of Sciences. Courtesy of the National Academy Press, Washington DC).

Group

Revision

Before

After

Factor

Water mites

Cook, 1986

133

334

2.51

Macrochelidae

Halliday, 1986–1998

25

64

2.56

Phytoseiidae

Schicha, 1987

31

97

3.13

Scutacaridae

Mahunka, 1967

4

19

4.75

Steganacaridae

Niedbala, 1987,1989

6

63

10.5

17

45

2.65

216

622

2.90

Niedbala and Colloff 1997 Ascidae

Walter et al., 1993 Walter and Lindquist, 1997 Halliday et al., 1998

Total

1996a, 1996b). Other projects have included the biology and control of spider mites in orchards (e.g. Readshaw 1975a, 1975b), and the use of eriophyids as biological control agents of weeds (e.g. Caresche and Wapshere 1974). In 1960 CSIRO began a project on the biological control of dung and dung-breeding pest flies, by the use of introduced dung beetles (Waterhouse 1974). In 1975 the scope of the dung beetle project was expanded to include mites, with ecological and taxonomic research by M. M. H. Wallace, who had been transferred from the redlegged earth mite project. The result was a study of the Australian Macrochelidae (Wallace 1985, 1986), which is currently the subject of my own research (Halliday 1986, 1988, 1990, 1993). In 1981 the South African species Macrocheles peregrinus Krantz (1981) was introduced into Australia in an attempt to contribute to the control of flies, and quickly became established (Wallace and Holm 1983). In 1993 CSIRO Entomology appointed M. J. Colloff to undertake a project on the systematics and biology of Australian soil mites. The results of this study have begun to appear as a series of taxonomic papers (Colloff and Niedbala 1996; Niedbala and Colloff 1997), a catalogue of the Australian Oribatida (Colloff and Halliday 1998), and an interactive key and glossay for their identification (Hunt et al. 1998).

sented in Table 1. The known Australian fauna of water mites in 1985 was 133 described species (data derived from Halliday 1998). Cook (1986) then published a major revision of the group in which he described over 200 new species. The result was that the number of described species went from 133 to 334, which represents a multiplication by a factor of 2.51. My own work on the Australian Macrochelidae over the last 10 years has had a similar effect – from 25 species in the early 1980s to 64 now, a multiplication factor of 2.56 (Halliday 1986, 1988, 1990, 1993, and unpublished data). In the Phytoseiidae, Schicha took the fauna from 31 species to 97 in 10 years (Schicha 1987), and the results for the Scutacaridae, Steganacaridae, and Ascidae are summarised in Table 1. Combining these groups gives a total of 216 described species in about 1985, to 622 species now. When these groups were revised, the number of described species was multiplied by an average factor of 2.90. If the same pattern were to be repeated with all the other groups of Australian mites that are waiting to be revised, the number of species would be 2,620 × 2.9 = 7,600, so we could conclude that this is the number of species of mites in Australia. However I believe that this would be a gross underestimate, because the multiplication factor of 2.9 is very conservative.

An important feature of the mite fauna of any area is the number of species it contains. Halliday et al. (2000) presented a brief discussion of the number of mite species in Australia, and I now take the opportunity to do so in more detail. The question of how many species of mites there are in Australia can conveniently be broken into two parts – how many described species are there, and how many are still to be described?

In the groups shown in Table 1, many species are known to exist that were not included in the revisions listed. In most cases undescribed species already exist in collections, but were not included in the studies for a variety of reasons, and in others there are habitats or geographic areas that have not yet been adequately sampled. Even in the groups that have been subjected to reasonably serious taxonomic effort, there is still room for increase in the known number of species. Furthermore, and more importantly, some of the groups that have not been studied are likely to contain many more species than the factor of 2.9 would suggest.

The number of described species of mites in Australia is now known accurately, as 2,620, at 31/12/97 (Halliday 1998). Estimating the number of undescribed species is more difficult and more interesting. Halliday et al. (2000) approached this question by choosing selected groups of mites and comparing the number of described species in those groups before and after they had been the subject of modern taxonomic revisions. The results are pre-

A comprehensive list of the birds that can be found in Australia would include something over 700 species (Slater 1970). Experience from other parts of the world suggests that these 700 species of birds probably carry about 2–3 species of feather mites each (Gaud and Atyeo 1996), so we might expect a total of maybe as many as 2000 species of feather mites in Australia. At the moment we know of only 64 named species of feather mites (Halliday

HOW MANY SPECIES?

11

R. B. Halliday

600

500

Species per decade

400

300

200

100

0 1765

1785

1805

1825

1845

1865

1885

1905

1925

1945

1965

1985

Midpoint of decade

Figure 1

Number of species of Australian mites described in each decade, from Linnaeus to the present (closing date 31/12/1997).

1998), and the descriptions of most of those date back over 100 years. The Australian flora includes at least 20,000 species of flowering plants (George 1981). At a conservative estimate, about a quarter of these may have a specific eriophyid feeding on them. We may therefore estimate that Australia could have as many as 5,000 species of eriophyoids, while we have names for only about 50 at the moment (Halliday 1998). The fauna of the United States includes more than 600 described species (Baker et al. 1996), more than 10 times as many as Australia, in an area of similar size with a roughly similar range of plant types. More than 80 undescribed species of Halacaridae have been found on one small island off Western Australia (Bartsch 1996), but the total number of described species from the whole of Australia is only 80 (Halliday 1998), and most of these were described in the last 5 years. There are certainly several hundred more Australian halacarids waiting to be found and described. The world fauna of Uropodina includes over 2000 described species (Hirschmann and Wisniewski 1993). If Australia had only about one tenth of the world’s fauna, we should have about 200 described species, but at the moment we only know of about 60 (Halliday 1998). There are many areas of wet forest in eastern Australia where uropodines are extremely abundant and diverse, but taxonomic study of these has not even started. Certainly several hundred more species are waiting to be described. As a result of this analysis, I conservatively estimate the total number of mite species in Australia is of the order of 20,000.

12

CONCLUSIONS Figure 1 shows the number of species of Australian mites described in each 10 year period, starting with 1758. It should be noted that the date shown is the date of description of each species, even if it was not recognised in Australia until some time later. From 1758 to 1865 progress was very slow, with just a few species being described each year. The first conspicuous increase in the rate of descripton of the fauna is in the 1880s, due in large part to the efforts of Trouessart and Mégnin, working on feather mites. There was another increase in the early 1900s, with an increasing number of species described by Berlese. Progress began to accelerate through the 1930s, 40s and 50s, with big contributions by Womersley and then Southcott. It continues to accelerate through the 60s and 70s, with increasing numbers of taxonomists working on a more and more diverse range of groups. The enormous increase in the 1980s was mainly due to Cook (1986), who described over 200 species of Australian water mites in a single publication. The 1990s are unlikely to exceed the 1980s, but will certainly surpass the 1970s when papers published after 31/12/97 are included. If taxonomists can sustain the rate of productivity they have shown over the last 20 years or so, of about 400 new species every 10 years, it will take about 400 years to fully document the estimated 20,000 species estimated to occur in the Australian fauna. In the title of this paper I referred to a period of 250 years of Australian acarology. If that period starts with Linnaeus in 1758, it concludes 10 years from now in 2008. Where are the most dramatic changes likely to occur over the next 10 years? On the basis

250 YEARS OF AUSTRALIAN ACAROLOGY

of some projects that are currently in progress, a big growth can be expected in our taxonomic knowledge of the Halacaridae, Eriophyidae, Oribatids and other soil mites, and in a range of groups that are needed to support biological control and IPM programs. In 10 years from now we are likely see big advances in applications of molecular techniques to taxonomy and pest control, as those programs continue to make demands for more and more sophisticated taxonomic information. Medical and veterinary acarology, which at the moment is almost non-existent in Australia, apart from work on house dust mites and ticks, needs a greater investment of effort, as does our work on feather mites. All of this taxonomic effort will be made easier by the application of sophisticated data-processing technology, such as that demonstrated by Hunt et al. (1998). The next 10 years will place increasing demands on acarologists in Australia and elsewhere, as financial pressures continue to intensify, as international trade poses increasing challenges for quarantine and pest control, and as the role of mites in biodiversity measurement and environmental quality monitoring is understood more fully. To meet these challenges, acarologists must continually adapt their science to incorporate new technologies as they become available, without losing sight of the enormous contributions made by previous generations. The International Congresses of Acarology will continue to play a vital role in these processes.

ACKNOWLEDGEMENTS I like to thank Vik Prasad for agreeing to let me use some of the photographs I used in the spoken version of this paper, and John Macdonald and Murray Fletcher, who helped me locate other illustrations and unpublished information.

REFERENCES Angus, B. M. 1997. ‘Tick Fever and the Cattle Tick in Australia.’ (Queensland Department of Primary Industries: Brisbane.). Anonymous, 1929. The Red Legged Earth Mite in Western Australia (Penthaleus destructor, Jack). Journal of the Council for Scientific and Industrial Research 2, 244. Anonymous, 1930. Entomological investigations in Western Australia and Tasmania : The Red-legged Earth Mite and the Clover Springtail (Lucerne Flea). Journal of the Council for Scientific and Industrial Research 3, 189–190. Baker, A. S. 1995. A redescription of Halotydeus destructor (Tucker) (Prostigmata: Penthaleidae), with a survey of ontogenetic setal development in the superfamily Eupodoidea. International Journal of Acarology 21, 261–282. Baker, E. W., T. Kono, J. W. Amrine, M. Delfinado-Baker, and T. Stasny. 1996. ‘The Eriophyoid Mites of the United States.’ (Indira Publishing House: Michigan.) Bancroft, J. 1877. Development of sugar-cane disease. Second Annual Report of the Board Appointed to Enquire Into the Causes of Diseases Affecting Live Stock and Plants. Votes and Proceedings of the Legislative Assembly, Queensland, Appendix K. 12–13 + 1 Plate. Banks, N. 1904. A treatise on the Acarina, or mites. Proceedings of the United States National Museum 28, 1–114. Banks, N. 1915. The Acarina or mites. A review of the group for the use of economic entomologists. United States Department of Agriculture Report 108, 1–153.

Banks, N. 1916. Acarians from Australian and Tasmanian ants and antnests. Transactions of the Royal Society of South Australia 40, 224–240 + Plates XXIII-XXX. Bartsch, I. 1996. Halacarines (Acari: Halacaridae) from Rottnest Island, Western Australia: the genera Agauopsis Viets and Halacaropsis gen. nov. Records of the Western Australian Museum 18, 1–18. Beer, R. E. 1954. A revision of the Tarsonemidae of the Western Hemisphere (Order Acarina). University of Kansas Science Bulletin 36 : 1091–1387. Canestrini, G. 1884. Acari nuovi o poco noti. Atti del Reale Istituto Veneto di Scienze, Lettere ed Arti (Series 6) 2, 693–724 + Plates VI-IX. Canestrini, G. 1887. Intorno ad alcuni Acari ed Opilionidi dell’ America. Atti della Società Veneto-Trentina di Scienze Naturali 11, 100–111 + Plates IX, X. Caresche, L. A. and Wapshere, A. J. 1974. Biology and host specificity of the Chondrilla gall mite Aceria chondrillae (G. Can.) (Acarina, Eriophyidae). Bulletin of Entomological Research 64, 183–192. Clift, A. D. and Toffolon, R. B. 1981. Biology, fungal host preferences and economic significance of two pygmephorid mites (Acarina : Pygmephoridae) in cultivated mushrooms, N.S.W., Australia. Mushroom Science 11, 245–253. Colloff, M. J. and Halliday, R. B. 1998. ‘Oribatid Mites : A Catalogue of the Australian Genera and Species.’ (CSIRO Publishing: Melbourne.) Cook, D. R. 1986. Water mites from Australia. Memoirs of the American Entomological Institute 40, 1–568. Cooper, W. F. and Robinson, L. E. 1908. On six new species of Ixodidae, including a second species of the new genus Rhipicentor N. & W. Proceedings of the Cambridge Philosophical Society 14, 457–470. Covacevich, J., Davie, P., and Pearn, J. 1987. ‘Toxic Plants and Animals. A Guide for Australia.’ (Queensland Museum: Brisbane.). Contributions by R. V. Southcott: 33–36, 73–78, 79–85, 93–98, 107–112, 243–258, 273–284. Denny, H. 1843. Description of six supposed new species of parasites. Annals and Magazine of Natural History (First series) 12, 312–316. Domrow, R. 1988. Acari Mesostigmata parasitic on Australian vertebrates: an annotated checklist, keys and bibliography. Invertebrate Taxonomy 1, 817–948. Domrow, R. 1991. Acari Prostigmata (excluding Trombiculidae) parasitic on Australian vertebrates : an annotated checklist, keys and bibliography. Invertebrate Taxonomy 4, 1238–1376. Domrow, R. 1992. Acari Astigmata (excluding feather mites) parasitic on Australian vertebrates: an annotated checklist, keys and bibliography. Invertebrate Taxonomy 6, 1459–1606. Domrow, R. and Lester, L. N. 1985. Chiggers of Australia (Acari : Trombiculidae): an annotated checklist, keys and bibliography. Australian Journal of Zoology Supplementary Series 114, 1–111. Fabricius, J. C. 1775. ‘Systema Entomologiae.’ (Lipsiae: Flensberg.) Fabricius, J. C. 1805. ‘Systema Antliatorum. Secundum Ordines, Genera, Species, Adiectis Synonymis, Locis, Observationibus, Descriptionibus.’ (Reichard: Brunsvigae.) Fuller, C. 1899. Notes on the Queensland cattle tick, and its relationship to the Texas fever tick and the blue tick of Cape Colony (South Africa). Queensland Agricultural Journal 4, 389–394. Gaud, J. and Atyeo, W. T. 1996. Feather mites of the world (Acarina, Astigmata): The supraspecific taxa. Annales Musee Royal de l’Afrique Centrale Tervuren, Belgique, Sciences Zoologiques 277, Part I, 1–193, Part II, 1–436. George, A. S. 1981. The background to the Flora of Australia. In ‘Flora of Australia, volume 1’. pp 3–24. (Canberra: Australian Government Publishing Service.) Gervais, F. L. P. 1842. Quinzaine d’espèces d’insectes aptères qui doivent presque toutes former des genres particuliers. Annales de la Société Entomologique de France 11, xlv-xlviii.

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R. B. Halliday Griggs, P. 1995. ‘Rust’ disease outbreaks and their impact on the Queensland sugar industry, 1870–1880. Agricultural History 69, 413–437. Halliday, R. B. 1986. Mites of the Macrocheles glaber group in Australia (Acarina : Macrochelidae). Australian Journal of Zoology 34, 733–752. Halliday, R. B. 1988. The genus Holostaspella Berlese (Acarina : Macrochelidae) in Australia. Journal of the Australian Entomological Society 27, 149–155. Halliday, R. B. 1990. Mites of the Macrocheles muscaedomesticae group in Australia (Acarina : Macrochelidae). Invertebrate Taxonomy 3, 407–430. Halliday, R. B. 1991. Taxonomic background of the redlegged earth mite Halotydeus destructor (Tucker) (Acarina : Penthalaeidae). Plant Protection Quarterly 6, 162–165. Halliday, R. B. 1993. Two new species of Macrocheles from Australia (Acarina : Mesostigmata : Macrochelidae). Australian Entomologist 20, 99–106. Halliday, R. B. 1998. ‘Mites of Australia: A Checklist and Bibliography.’ (CSIRO Publishing: Melbourne.) Halliday, R. B. and Pearn, J. H. 1999. Ronald Vernon Southcott. Acarologist, physician, naturalist. International Journal of Acarology 25, 151–153. Halliday, R. B., Walter, D. E. and Lindquist, E. E. 1998. Revision of the Australian Ascidae (Acarina : Mesostigmata). Invertebrate Taxonomy 12, 1–54. Halliday, R. B., OConnor, B. M. and Baker, A. S. 2000. Global diversity of mites. In ‘Nature and Human Society: The Quest for a Sustainable World’. (Eds P. Raven and T. Williams.) pp. 184–195. (National Academy Press: Washington DC.) Hirschmann, W. and Wisniewski, J. 1993. Acari Parasitiformes. Supercohors Atrichopygidiina Hirschmann 1975. Die Uropodiden der Erde. Acarologie. Schriftenheihe für Vergleichende Milbenkunde 40, 1–466. Hirst, S. 1912. On a new species of mite (Tarsonemus) injurious to sugarcanes in Barbados. Bulletin of Entomological Research 3, 325–328. Hirst, S. 1929. On the larval trombidiid mite (Trombicula hirsti L. Sambon) that causes the ‘scrub itch’ of northern Queensland and The Coorong, South Australia. Transactions of the Royal Society of South Australia 53, 24–26. Hirst, S. 1930. On a new species of tick (Ixodes victoriensis sp. n.) from Victoria, Australia. Annals and Magazine of Natural History (Tenth series) 5, 575–576. Hirst, S. 1931. On some new Australian Acari (Trombidiidae, Anystidae, and Gamasidae). Proceedings of the Zoological Society of London 1931, 561–564. Hunt, G. S. 1996. A review of the family Pheroliodidae Paschoal in Australia (Acarina: Cryptostigmata: Plateremaeoidea). Records of the Australian Musuem 48, 325–358. Hunt, G. S., Colloff, M. J., Dallwitz, M. J. and Walter, D. E. 1998. ‘An Interactive Key to Oribatid Mites of Australia.’ (CSIRO Publishing: Melbourne.), incorporating : Hunt, G. S., Norton, R. A., Kelly, J. P. H., Colloff, M. J. and Lindsay, S. M. 1998. ‘An Interactive Glossary to Oribatid Mites’ (CSIRO Publishing: Melbourne.) (CD-ROM). Jack, R. W. 1908. The earth flea. A common pest of winter vegetables. Agricultural Journal of the Cape of Good Hope 32, 615–620. Key, K. H. L. 1990. Host relations and distribution of species of Caeculisoma (Acarina : Erythraeidae) parasitising grasshoppers in Australia, with supplementary information for the genus Trombella (Trombellidae). Australian Journal of Zoology 38, 11–18. Key, K. H. L. 1991. Host relations and distribution of Australian species of Charletonia (Acarina : Erythraeidae) parasitising grasshoppers. Australian Journal of Zoology 39, 31–43.

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Key, K. H. L. 1994. Host relations and distribution of the Australian species of Eutrombidium (Acarina : Microtrombidiidae), a parasite of grasshoppers. Australian Journal of Zoology 42, 363–370. Key, K. H. L. and Southcott, R. V. 1986. Host relations and distribution of Australian species of Trombella (Acarina : Trombellidae) parasitising grasshoppers. Australian Journal of Zoology 34, 647–658. Koch, C. L. 1835–1844. ‘Deutschlands Crustaceen, Myriapoden und Arachniden. Ein Beitrag zur Deutschen Fauna.’ (Herrich-Schäffer: Regensberg.) Koch, L. 1867. Beschreibungen neuer Arachniden und Myriapoden. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 17, 173–250. Krantz, G. W. 1981. Two new glaber group species of Macrocheles (Acari : Macrochelidae) from southern Africa. International Journal of Acarology 7, 3–16. Lee, D. C., 1970. The Rhodacaridae (Acari : Mesostigmata); classification, external morphology and distribution of genera. Records of the South Australian Museum 16 (3), 1–219. Lee, D. C. 1981. Sarcoptiformes (Acari) of South Australian soils. 1. Notation. 2. Bifemorata and Ptyctima (Cryptostigmata). Records of the South Australian Museum 18, 199–222. Lee, D. C. 1982. Sarcoptiformes (Acari) of South Australian soils. 3. Arthronotina (Cryptostigmata). Records of the South Australian Museum 18, 327–359. Lee, D. C. 1985. Sarcoptiformes (Acari) of South Australian soils. 4. Primitive oribate mites (Cryptostigmata) with an extensive, unfissured hysteronotal shield and aptychoid. Records of the South Australian Museum 19, 39–67. Levot, G. W. 1993. Control of northern fowl mite, Ornithonyssus syliarum infestations on commercial poultry. General and Applied Entomology 24, 3–10. Liversidge, A. 1876. Report of the sugar-cane disease in the Mary River District, Queensland. Journal of the Agriculural Society of New South Wales. 2, 126–130, 142–146. Lohmann, H. T. 1893. Die Halacarinen der Plankton-Expedition. Ergebnisse der Plankton-Expedition der Humboldt-Stiftung 2, 1–95 + Plates I-XIII. Lohmann, H. T. 1909. Marine Hydrachnidae und Halacaridae. In ‘Die Fauna Südwest-Australiens 2 (11).’ (Eds W. Michaelsen and R. Hartmeyer.) pp. 149–154. (Gustav Fischer: Jena.) Lucas, H. 1846. Sur quelques espèces nouvelles d’Ixodes qui vivent parasites sur les serpens (Boa constrictor and Python sebae) et sur l’Ornithorhynque (Ornithorhynchus paradoxus Blum.). Annales de la Société Entomologique de France (Second series) 4, 53–64 + Plate I. Mahunka, S. 1967. A survey of the scutacarid (Acari : Tarsonemini) fauna of Australia. Australian Journal of Zoology 15, 1299–1323. Mather, P. 1986. ‘A Time for a Museum. The History of the Queensland Museum 1862–1986.’ (Queensland Museum: Brisbane.) Mégnin, P. and Trouessart, E. L. 1884a. Les Sarcoptides plumicoles. Révision du groupe des Analgesinae, et description des espèces et genres nouveaux de la collection du Musée d’Angers. Journal de Micrographie 8, 257–266. Mégnin, P. and Trouessart, E. L. 1884b. Les Sarcoptides plumicoles. Révision du groupe des Analgesinae, et description des espèces et genres nouveaux de la collection du Musée d’Angers. Journal de Micrographie 8, 331–338. Mégnin, P. and Trouessart, E. L. 1884c. Les Sarcoptides plumicoles. Révision du groupe des Analgesinae, et description des espèces et genres nouveaux de la collection du Musée d’Angers. Journal de Micrographie 8, 92–101. Meyer, M. K. P. (Smith) 1981. Mite pests of crops in southern Africa. Department of Agriculture and Fisheries, Republic of South Africa, Science Bulletin 397, 1–92.

250 YEARS OF AUSTRALIAN ACAROLOGY

Michael, A. D. 1890. Report on diseased sugar-cane from Barbados, forwarded by Mr John R. Bovell. Bulletin of Miscellaneous Information, Royal Botanic Gardens, Kew 40, 85–86. Musgrave, A. 1932. ‘Bibliography of Australian Entomology, 1775–1930, with Biographical Notes on Authors and Collectors.’ (Royal Zoological Society of New South Wales: Sydney.) Neumann, G. 1901. Revision de la famille des Ixodidés. Mémoires de la Société Zoologique de France 14, 249–372. Neumann, L. G. 1910. Description de deux nouvelles espèces d’Ixodinae. Tijdschrift voor Entomologie 53, 11–17 + Plate 1. Newman, L. J. 1920. Report of the Entomologist. Annual Report, Western Australia Department of Agriculture 9, 39–41. Newman, L. J. 1923. The red-legged velvet earth mite. Bulletin, Western Australia Department of Agriculture 106, 1–4. Newman, L. J. 1925. The red legged earth mite Penthaleus destructor (Jack). Journal of the Department of Agriculture, Western Australia 2, 469–475. Niedbala, W. 1987. Phthiracaroidea (Acari, Oribatida) noveaux d’Australie. Redia 70, 301–375. Niedbala, W. 1989. Phthiracaroidea (Acari, Oribatida) nouveaux du royaume australien. Annales Zoologici 43, 19–50. Niedbala, W. and Colloff, M. J. 1997. Euptyctime oribatid mites from Tasmanian rainforest (Acari: Oribatida). Journal of Natural History 31, 489–538. Norris, K. R. 1938. A population study of the Red-Legged Earth Mite (Halotydeus destructor) in Western Australia, with notes on associated mites and Collembola. Pamphlet, Commonwealth of Australia, Council for Scientific and Industrial Research 84, 1–23. Norris, K. R. 1943. Experiments with insecticides against the Red-Legged Earth Mite (Halotydeus destructor (Tucker)). Bulletin, Commonwealth of Australia, Council for Scientific and Industrial Research 171, 1–28. Norris, K. R. 1944. Experimental determination of the influence of the Red-Legged Earth Mite (Halotydeus destructor) on a Subterranean Clover pasture in Western Australia. Bulletin, Commonwealth of Australia, Council for Scientific and Industrial Research 183, 1–36. Norris, K. R. 1950. The aestivating eggs of the Red-Legged Earth Mite, Halotydeus destructor (Tucker). Bulletin, Commonwealth Scientific and Industrial Research Organisation 253, 1–26. Nuttall, G. H. F. and Warburton, C. 1908. ‘Ticks. A Monograph of the Ixodoidea. Part I. The Argasidae.’ (Cambridge University Press: Cambridge.) Nuttall, G. H. F. and Warburton, C. 1911. ‘Ticks. A Monograph of the Ixodoidea. Part II. Ixodidae.’ (Cambridge University Press: Cambridge.) Nuttall, G. H. F. and Warburton, C. 1915. Ticks. A Monograph of the Ixodoidea. Part III. The Genus Haemaphysalis.’ (Cambridge University Press: Cambridge.) Otto, J. C. 1992. A new species of Anystis von Heyden compared with Anystis salicinus (Linnaeus) (Acarina : Anystidae). International Journal of Acarology 18, 25–35. Otto, J. C. and Halliday, R. B. 1991. Systematics and biology of a predatory mite (Anystis sp.) introduced into Australia for biological control of redlegged earth mite. Plant Protection Quarterly 6, 181–185. Qin, T. K. and Halliday, R. B. 1996a. Revision of the Australian and South African species of Halotydeus (Acarina: Penthaleidae). Bulletin of Entomological Research 86, 441–450. Qin, T. K. and Halliday, R. B. 1996b. The Australian species of Chromotydaeus Berlese and Penthaleus C. L. Koch (Acarina: Penthaleidae). Journal of Natural History 30, 1833–1848. Queensland Institute of Medical Research 1998. ‘QIMR – A Historical Summary.’ WWW document, http://www.qimr.edu.au/qimrhist.html. 4pp, version dated 31/10/98.

Railliet, A. 1893. ‘Traité de Zoologie Médicale et Agricole. Part I.’ (Asselin et Houzeau: Paris.) Rainbow, W. J. 1906. A synopsis of Australian Acarina. Records of the Australian Museum 6, 145–193. Readshaw, J. L. 1975a. Biological control of orchard mies in Australia with an insecticide-resistant predator. Journal of the Australian Institute of Agricultural Science 41, 213–214. Readshaw, J. L. 1975b. The ecology of tetranychid mites in Australian orchards. Journal of Applied Ecology 12, 473–495. Ridsdill-Smith, T. J. 1997. Biology and control of Halotydeus destructor (Tucker) (Acarina: Penthaleidae): a review. Experimental and Applied Acarology 21, 195–224. Roberts, F. H. S. 1928–1929. A revision of the Australian Bombyliidae (Diptera). Parts I-III. Proceedings of the Linnean Society of New South Wales 53, 90–144, 413–455, 54, 553–583. Roberts, F. H. S. 1934. Ticks infesting domesticated animals in Queensland. Queensland Agricultural Journal 41, 114–123. Roberts, F. H. S. 1952. ‘Insects Affecting Livestock.’ (Angus and Robertson: Sydney and London.) Roberts, F. H. S. 1970. ‘Australian Ticks.’ (CSIRO: Melbourne.) Schicha, E. 1984. Identification of pest and beneficial arthropods with special reference to predatory mites of the family Phytoseiidae – Current advances and future trends. Proceedings of the 4th Applied Australian Entomological Research Conference, Adelaide, September 1984. pp 442–451. Schicha, E. 1987. ‘Phytoseiidae of Australia and Neighboring Areas.’ (Indira Publishing: Michigan.) Schicha, E. and Loudon, B. 1980. The first quarantine interception of Isle of Wight Disease in New South Wales. Australasian Beekeeper 82, 31–33. Slater, P. 1970. ‘A Field Guide to Australian Birds. Volume 1, Non-Passerines.’ (Rigby: Adelaide.) Solomon, M. E. 1937. Behaviour of the red-legged earth mite, Halotydeus destructor, in relation to environmental conditions. Journal of Animal Ecology 6, 340–361. Southcott, R. V. 1946a. On the family Smarididae (Acarina). Proceedings of the Linnean Society of New South Wales 70, 173–178. Southcott, R. V. 1946b. Studies on Trombidiidae (Acarina). Some observations on the biology of the Microtrombidiinae. Proceedings of the Linnean Society of New South Wales 70, 312–316. Southcott, R. V. 1946c. Studies on Australian Erythraeidae (Acarina). Proceedings of the Linnean Society of New South Wales 71, 6–48 Southcott, R. V. 1961a. Studies on the systematics and biology of the Erythraeoidea (Acarina), with a critical revision of the genera and subfamilies. Australian Journal of Zoology 9, 367–610 + Plate 1. Southcott, R. V. 1961b. Notes on the genus Caeculisoma (Acarina : Erythraeidae) with comments on the biology of the Erythraeoidea. Transactions of the Royal Society of South Australia 84, 163–178. Southcott, R. V. 1963. Herbert Womersley (1889–1962). Acarologia 5, 323–334. Southcott, R.V. 1964. Obituary and bibliography of Herbert Womersley. Records South Australian Museum 14, 603–632. Southcott, R. V. 1966. Revision of the genus Charletonia Oudemans (Acarina : Erythraeidae). Australian Journal of Zoology 14, 687–819. Southcott, R. V. 1972. Revision of the larvae of the tribe Callidosomatini (Acarina : Erythraeidae) with observations on post-larval instars. Australian Journal of Zoology Supplementary Series 13, 1–84. Southcott, R.V. 1976. Arachnidism and allied syndromes in the Australian region. Records of the Adelaide Children’s Hospital 1, 97–186. Southcott, R.V. 1982. Australia. In ‘History of Acarology.’ (ed. V. Prasad.) pp. 1–51. (Indira Publishing: Michigan.)

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R. B. Halliday Southcott, R. V. 1986a. Description of Odontacarus veitchi sp. nov. (Acarina : Trombiculidae). Records of the South Australian Museum 19, 213–217. Southcott, R. V. 1986b. Australian larvae of the genus Trombella (Acarina : Trombidioidea). Australian Journal of Zoology 34, 611–646. Southcott, R. V. 1986c. Studies on the taxonomy and biology of the subfamily Trombidiinae (Acarina : Trombidiidae) with a critical revision of the genera. Australian Journal of Zoology Supplementary Series 123, 1–116. Southcott, R. V. 1986d. History of the discovery of Speleognathus australis Womersley (Acarina : Trombidiformes), with notes on its natural history and behaviour. Records of the South Australian Museum 19, 201–212. Southcott, R. V. 1991. A further revision of Charletonia (Acarina : Erythraeidae) based on larvae, protonymphs and deutonymphs. Invertebrate Taxonomy 5, 61–131. Swan, D. C. 1934. The red-legged earth mite Halotydeus destructor (Tucker) in South Australia : with remarks upon Penthaleus major (Dugès). Journal of Agriculture of South Australia 38, 353–367. Tryon, H. 1889. ‘Report on Insect and Fungus Pests No. 1.’ (Queensland Department of Agriculture: Brisbane.). Tryon H. 1898. Vegetable pathology. Fruitlet core-rot of pineapple. Queensland Agricultural Journal 3, 458–467 + Plates LXVIII-LXXI. Tryon, H. 1917. Report of the entomologist and vegetable pathologist. Reports of the Queensland Department of Agriculture and Stock, 1916/1917, 49–63. Tucker, R. W. E. 1925. The Black Sand Mite : Penthaleus destructor n. sp. Entomology Memoirs, Department of Agriculture, Union of South Africa 3, 21–36. Underhill, D. 1987. ‘Australia’s Dangerous Creatures.’ (Reader’s Digest: Sydney.) Upton, M. S. 1997. ‘A Rich and Diverse Fauna : The History of the Australian National Insect Collection, 1926–1991.’ (CSIRO Publishing: Melbourne.) Wallace, M. M. H. 1954. The effect of DDT and BHC on the population of the Lucerne Flea, Sminthurus viridis (L.) (Collembola), and its control by predatory mites, Biscirus spp. (Bdellidae). Australian Journal of Agricultural Research 5, 148–155. Wallace, M. M. H. 1960. Control of red-legged earth mite and lucerne flea. Treatment of seed with systemic insecticides. Journal of Agriculture of Western Australia 1, 3–6. Wallace, M. M. H. 1981. Tackling the lucerne flea and the red-legged earth mite. Journal of Agriculture – Western Australia 22, 72–74. Wallace, M. M. H. 1985. The seasonal abundance of phoretic predatory mites associated with dung beetles in south eastern Australia (Acari: Macrochelidae, Parasitidae). International Journal of Acarology 11, 183–189.

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Wallace, M. M. H. 1986. Some macrochelid mites (Acari : Macrochelidae) associated with Australian dung beetles (Coleoptera : Scarabaeidae). Acarologia 27, 3–15. Wallace, M. M. H. and Holm, E. 1983. Establishment and dispersal of the introduced predatory mite Macrocheles peregrinus Krantz, in Australia. Journal of the Australian Entomological Society 22, 345–348. Wallace, M. M. H. and Mahon, J. A. 1973. The taxonomy and biology of Australian Bdellidae (Acari). I. Subfamilies Bdellinae, Spinibdellinae and Cytinae. Acarologia 14, 544–580. Wallace, M. M. H. and Mahon, J. A. 1976. The taxonomy and biology of Australian Bdellidae (Acari). II. Subfamily Odontoscrinae. Acarologia 18, 65–123. Walter, D. E. and Lindquist, E. E. 1997. Australian species of Lasioseius (Acari: Mesostigmata: Ascidae): the porulosus group and other species from rainforest canopies. Invertebrate Taxonomy 11, 525–547. Walter, D. E., Halliday, R. B. and Lindquist, E. E. 1993. A review of the genus Asca (Acarina: Ascidae) in Australia, with descriptions of three new leaf-inhabiting species. Invertebrate Taxonomy 7, 1327–1347. Waterhouse, D. E. 1974. The biological control of dung. Scientific American 230 (4), 100–109. Womersley, H. 1927a. Notes on the British species of Protura with descriptions of new genera and species. Entomologists Monthly Magazine 63, 140–148. Womersley, H. 1927b. A study of the larval forms of certain species of Protura. Entomologists Monthly Magazine 63, 149–153. Womersley, H. 1932. The Collembola-Symphyleona of Australia: A preliminary account. Pamphlet of the Council for Scientific and Industrial Research of Australia 34, 9–47. Womersley, H. 1933. On some Acarina from Australia and South Africa. Transactions of the Royal Society of South Australia 57, 108–112. Womersley, H. 1934. A revision of the trombid and erythraeid mites of Australia with descriptions of new genera and species. Records of the South Australian Museum 5, 179–254. Womersley, H. 1937. Acarina. Australian Antarctic Expedition 1911–1914. Scientific Reports. Series C.-Zoology and Botany 10 (6), 1–24 + Plates II-XII. Womersley, H. 1952. The scrub-typhus and scrub-itch mites (Trombiculidae, Acarina) of the Asiatic-Pacific region. Part 1 (Text) Records of the South Australian Museum 10, 1–435. Part 2 (Plates) ibid 437–673. Womersley, H. and Audy, J. R. 1957. Malaysian parasites – XXVII. The Trombiculidae (Acarina) of the Asiatic-Pacific region. A revised and annotated list of the species in Womersley (1952), with descriptions of larvae and nymphs. Studies of the Institute of Medical Research, Malaya 28, 231–296. Womersley, H. and Southcott, R. V. 1941. Notes on the Smarididae (Acarina) of Australia and New Zealand. Transactions of the Royal Society of South Australia 65, 61–78.

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

POISING FOR A NEW CENTURY: DIVERSIFICATION IN ACAROLOGY

Biological Resources Program, Eastern Cereal and Oilseed Research Centre, Agriculture and Agri-Food Canada, Ottawa, Ontario K1A 0C6, Canada. e-mail: [email protected]

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Evert E. Lindquist

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Abstract The plenary addresses given at previous International Congresses of Acarology are reviewed to gain an initial perspective on the status of the field during the last four decades. Salient progress in acarology, as indicated by organisational developments and high profile research successes, is reviewed. Some chronic problems and recent concerns for the discipline are discussed. An array of enquiries for future investigations are offered, and some future challenges for acarology are considered.

INTRODUCTION I am both honoured and moved to have been invited to address this opening session of the Tenth International Congress of Acarology – the last such congress of this century and, some would say, this millenium. When Bruce Halliday asked me to deliver the keynote address for this session, he suggested that I share with you my views about the state of acarology, its strengths and weaknesses, and some thoughts on future directions. In agreeing to do this, I have also woven some more specific and personal acarological vignettes into the fabric of this presentation, which I hope will fascinate you as much as they do me. In developing this address, I gained some useful initial perspectives in reviewing the plenary addresses of past international congresses of acarology and the nature of the submitted papers given at them, as indicated by their titles. I will consider this aspect first, followed by a brief review of salient progress in acarology. Then I will turn to some chronic acarological problems, followed by some recent concerns. These will lead to a more colourful and

exciting consideration of future enquiries, and future challenges, with a brief conclusion.

I. SOME SALIENT PERSPECTIVES FROM PREDECESSORS Our beginning acarological session was perhaps the meeting held at Cornell University, Ithaca, in 1962 – a symposium entitled ‘Recent Advances in Acarology’. The welcoming address by Thomas Watkins (1963), then Director of Resident Instruction at Cornell, was both instructive and predictive. He focussed on the knowledge of a discipline and its application needing to have a ‘recognized role in economic concerns of man’. He noted that full-time generalists in acarology were already being augmented by a diversity of researchers, resulting in a growing integration of specialists in such fields as physiology, biochemistry, genetics, ecology, and parasitology, and having Acari used as experimental animals by non-specialists – a healthy situation. He suggested that the time was ripe to form a lasting scientific society that would implicitly hold regular meetings, to establish a nucleus of a few publications to handle the bulk of literature in this field, and to

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develop more effective training of students in the field of acarology in university curricula. At the First International Congress of Acarology held at Fort Collins, Colorado, in l963, George Wharton (1964) noted that, in order to gain support from society, acarology as a science must benefit society by way of human values that he categorised as aesthetic, intellectual, and material. Acarology had become recognised as a separate and important subdivision of biology, primarily through its contribution to man’s material welfare in combatting the ravages of pest species. Little in the way of aesthetic and intellectual value had as yet been determined from studies of Acari. Three years later, at a plenary symposium entitled ‘Entomology looks at its mission’ held at the annual meeting of the Entomological Society of America in 1966, Wharton (1967) urged a curricular emphasis on courses and studies dealing with processes and mechanisms, in contrast to kinds of organisms; whole organisms are products of processes. For example, the field of microbiology was well supported by exploiting studies of processes that were best manifested in microbes. In the broad field of applied biology, entomology had become highly visible in demanding knowledge of insects as organisms based on the mechanisms that produce those organisms. Entomologists were to remain aware that their ability to control targeted insect populations was the major reason that entomology was so well supported by society. Entomology must continue to develop its applied aspects, but at the same time exploit subjects that are best understood or tested by the study of activities of insects. Wharton’s views echoed those of other prominent entomologists at the time. Edward Steinhouse (1964), a leader in insect pathology, noted that entomology, to grow as a virile discipline, ‘…must lose itself in the mainstream of science’. And Vincent Wigglesworth (1965), a leader in insect physiology, noted that, given a sufficient acquaintance with insects, it was generally possible to find material ideally suited to the study of any biological problem. Can we now say the same for the Acari and their study? One of our greatest challenges is to realise for the study of Acari what has already been done for the insects. I will return to this challenge later. In his presidential address at the Second International Congress of Acarology, Sutton Bonington, in 1967, T. E. Hughes (1969) emphasized how some of the elegant new techniques becoming available could facilitate studies of fine structure of various types of cuticular organs, which would shed light on how Acari detect and respond to various types of stimuli. With the aid of micromanipulation and the advent of intracellular electrodes, detection of the sensory mechanism of individual structures should be possible on ticks and larger mites. He noted how much enriched the field of ecology could become with a greater knowledge of the intimate activities of the Acari. His caveat, that ‘…the acarologist brings to the technique as much or more than the technique gives to the acarologist’, is as relevant now as it was those 30 years ago. He noted the accuracy of Robin’s early illustrated work on Sarcoptes scabiei with the limitations of the microscopes 130 years ago; and to this I may add the illustrated observations of Albert Michael on sarcoptiform mites and those of Alfred Nalepa on the tiniest of mites, the Eriophyoidea, a century ago.

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The practical importance of acarology was the main theme of Bohumír Rosicky’s presidential address (1973) at the Third International Congress of Acarology at Prague in 1971. Acarology is subsidised to an extent that its results have practical value that is reflected in the national economy. His presentation ended with a note on the problem of passive dispersal over great distances commercially by ship, surface and air, as well as naturally. The globalisation of economies has exacerbated this problem, such that the need to be able to identify and know about the economic importance of species of Acari is greater now than ever before. The real distributions of both destructive and beneficial mites of agricultural importance are poorly known, to say nothing of what may be the limiting factors to their dispersal and distribution. Reinhart Schuster’s presidential address (1979) at the 4th International Congress of Acarology at Saalfelden in 1974 noted both the poorly known regions with regard to the acarofauna of but one small country, Austria, in Europe and the poorly known major groups of Acari in that country, particularly the Uropodina in the Parasitiformes and many families in the Trombidiformes. Ironically, the same can probably still be said for that country, and a similar but more aggravated situation is true for North America and elsewhere. Surely this is now the time to consider these inadequacies for as many of the countries and regions of the world as possible, even though they can not be addressed for some regions soon. In the plenary session at the same congress, Tyler Woolley (1979) noted a few examples of unique biological phenomena among the Acari – the moth ear mites studied by Asher Treat, the follicle mites by Bill Nutting, and the turtle cloacal mites by Joe Camin. These findings are of the aesthetic and intellectual categories noted earlier by Wharton (1964), and they are examples of the kind that need to be more popularised if mites are to gain a better appreciation by the public. In the other plenary address at the 4th Congress, Yuri Balashov’s thoughtful review (1979) of the state of genetics of Acari noted how limited this field was, other than for a few species of ticks and spider mites. His noting of the high variability of physiological features and photoperiodic responses in spider mites, and of their species consisting of many chromosomal races that are not always genetically compatible with each other, continue to pose serious problems today in quarantine regulation of species at a global level. He also noted that our poor knowledge of genetic data has limited our understanding of phylogenetic relationships between groups of Acari. Great strides have been made since then in acquiring data on sex determining mechanisms among major lineages of Acari (e.g. the work of Wim Helle and colleagues 1984), though a synthesis of these data as patterns relevant to the phylogeny and classification of Acari is not yet completed. Data for many families of Parasitiformes and Trombidiformes are still wanting. In his presidential address at the 6th International Congress of Acarology at Edinburgh in 1982, Gwilym Evans (1984) reemphasised the earlier commentary by Hughes in urging more sophisticated techniques of electrophysiology to clarify the functions of minute sensilli of Acari, noting that our exploration of acarine structure and function was still in its infancy. I would add to this the need for comparative studies of such structures and

A NEW CENTURY: DIVERSIFICATION

their functions. Can we determine whether structures that are presumed to be homologous from their form and location can be modified and adapted to a different function? If so, perhaps some forms and functions can be determined as derived from previous states, and therefore useful phylogenetically. Evans noted ‘the replacement’ of the setiform pilus dentilis by a placoid sensillus among some unrelated mesostigmatic taxa (Dinychus and Eviphis). The innervation and function of these structures are unknown, yet their external form may provide useful taxonomic characters. To this I add another modification of the same structure: For over 30 years, the modified form of the pilus dentilis to a hyaline flaplike structure has been used as an apomorphic attribute to define the tribe Melicharini of the family Ascidae (Lindquist and Evans 1965), though again without any idea of the function of this structure. In this same address, Evans noted that the evolutionary significance of the diversity of methods of insemination displayed in the Acari had received little attention, and that this area of investigation may provide valuable information for elucidating relationships between major groupings of Acari. Subsequent investigations, such as those by Harald Witte (1991) primarily on parasitengone Trombidiformes, and by Dave Walter (unpublished) primarily on gamasine Parasitiformes, evince substantial progress in this area. More observations are still needed before general patterns of acarine insemination are clear. Evans also noted that progress in the embryology of various groups of Acari, as well as that of Ricinulei and Palpigradi, was slow, and that such studies could provide another source of information relevant to phylogenetic relationships among the Acari and other arachnids. Progress in this area continues to be slow, and this may be related to the intellectual nature of such investigations, which are less competitive in engendering funding support. However, current work by Max Telford and Richard Thomas (1998) using molecular techniques pioneered on Drosophila to identify the head segments in early mite embryos and to homologise them with those of insects and crustaceans is a ray of light. This work may give new insight to the unresolved question of relationships among the major groups of arthropods. Evans’ address also noted the understandable concentration on phytoseiid-tetranychid predator/prey systems for economic and academic reasons. However, he urged that such studies also feature more euedaphic predator/prey systems including mite-nematode and mite-Collembola interactions. The investigations of Murray Wallace (e.g. 1974) and colleagues on the use of bdellid mites to control lucerne flea Collembola in Australia in the 1970s is one salient example of this, but other than several investigators such as Wolfgang Karg (e.g. 1983) and Dave Walter and colleagues (e.g. Epsky et al. 1988; Walter and Ikonen 1989; Walter et al. 1993), confirming that nematodes are preferred prey for various species of gamasine mites, little applied acarological progress has been made in this subject area. However, ongoing experimental work first reported by Izabela Lesna and Maurice Sabelis during the Third Symposium of the European Association of Acarologists, Amsterdam, 1996 (Lesna and Sabelis 1999), on predator-prey interactions between a polyphagous predatory soil

IN ACAROLOGY

mite, Hypoaspis aculeifer, and the bulb mite, Rhizoglyphus robini, and on cross-breeding to cause a shift in food preferences of this predator, is notable. A presentation by G. P. ChannaBasavanna, who was president of the 7th International Congress of Acarology at Bangalore in 1986, and Neelu Nangia (1988) emphasised how timely it was to hold a congress for the first time in a developing country in Asia. Many Indian workers have concentrated on the taxonomy of mites, especially of plant feeding mites. Basic studies on behaviour, feeding habits and reproductive attributes of mites and ticks, and the role of predators and other suppressive natural factors in the control of mite pests, had been given little attention in this and other developing countries. Suggested investigations for development of acarology in developing countries included: (1) faunistic investigations of the general mite fauna, which would require vast resources, preferably with international collaboration; (2) organised systematic studies of Acari of agricultural and medico-veterinary importance, preferably with funding from international organisations concerned with such problems that transcend geographical boundaries and may have global implications; (3) intensive studies of predators and pathogens of mite pests, and utilization of effective ones in integrated management of pests; (4) intensive investigations of the biology and behaviour of ticks, and of biochemical and immunological aspects of tickborne diseases, leading to development of vaccines to manage ticks and tick-borne diseases more effectively. From the perspective of developing countries and the tropics in general, in which most of these countries are located, relatively little progress has been made during the 12 years since that presentation, other than some substantial investigations on ticks and tick-borne diseases and on a few species of plant-feeding mites. In particular, organised and intensive faunistic investigations of the Acari of the world’s tropical regions have yet to be implemented. A plenary address by Bohumír Rosicky (1991), who was president of the 8th International Congress of Acarology held at ¯eské Budejovice in 1990, focussed on environmental acarology. His consideration of mites as bioindicators of environmental alterations, including pollution, creation of ecotones through various land usages, devastation and restoration of landscapes, synanthropic associations, urbanisation, and formation of new biotopes (dams, canals, parks, outdoor zoos, etc.), pointed to the need for comprehensive species-level knowledge of local, regional and global acarofaunas. This knowledge is all the more needed if we are to recognise and deal with the movements of non-native species. Other than for a few countries in Europe, the challenge of organising and developing an adequate faunistic knowledge of the Acari has not been addressed. In an accompanying plenary address by Conroy (1991) at the same meeting, water mites were noted as potential indicators of water quality, but the difficulty in identifying them was the reason most often given as to why they are not yet used extensively. Whereas Evans, during the 6th Congress, had welcomed the considerable recruitment to acarology of non-taxonomists who would change the course of this science previously dominated by taxonomy, Jerry Krantz (1998), during his plenary address at the 9th International Congress of Acarology at Columbus, Ohio in

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1994, noted the alarming decline in interest and support for systematics, including a dramatic student decline in graduate studies in this area, substantial retirements among professionals available to train and encourage students in this area, and academic positions refilled by non-systematists or left unfilled for economic reasons. The resultant serious shortage in systematic expertise has remained with us during this decade, though relevant funding is beginning to become available to address biodiversity issues. If acarology is to gain more recognition in the public domain, it is imperative that the acarofauna be included in major projects on biodiversity and on arthropods as bioindicators to monitor environmental changes. However, Krantz voiced optimism about what Edward O. Wilson saw in 1989 as a coming ‘pluralization of biology’, with systematics playing a leading role in the study of taxonomic groups at all levels of organisation, whether molecular or whole organism or guilds. More recently, Wilson (1998) has enlarged on this concept in his vision of ‘consilience’ – the integration of causally linked phenomena across disciplines, including causal connections between the natural sciences, the social sciences, and the humanities. The commonality of themes in previous plenary congress addresses is clear. To be supported, acarology must benefit society in material, practical ways. Acarology has been strengthened by the diversity of specialists in other fields who deal with mites and ticks as experimental entities. However, gains in acarological knowledge have been slow in the areas of embryology, functional morphology, behaviour, faunistic data, systematics of certain major groups, and in achieving general public awareness.

II. SALIENT PROGRESS IN ACAROLOGY Organizational growth and fostering of the science

Societies. Apart from the International Congress of Acarology, which was planned for four-year intervals beginning in 1963 at Fort Collins, Colorado, the Société des Acarologues de Langue Française (SALF), was initiated as the first organised society of acarology 30 years ago, in 1968. It has since changed its name to Société Internationale des Acarologues de Langue Française (SIALF). It has a newsletter and holds a meeting each year to discuss business matters. The meeting may sometimes be accompanied by a colloquium, and SIALF also organises acarology courses. The Acarological Society of America was founded three years later, in 1971. It, too, has a newsletter and holds a meeting annually, concurrent with that of the Entomological Society of America. The meetings include invited and submitted oral and poster presentations. The Acarological Society of India (ASI) was founded in 1974, and it was the first to issue its own periodical, the Indian Journal of Acarology, in 1976. Publication of this journal, however, was discontinued after its ninth volume, in 1984. The European Association of Acarologists (EURAAC) was established in 1987. It publishes a newsletter and holds highly successful symposia, with invited and submitted oral and poster presentations, every fourth year at intervals between the international congresses of acarology. This association is particularly successful in its international bridging of acarological interests, which

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is difficult to achieve in other regions of the world where countries are so much larger and farther apart. The present decade has seen the establishment of three more acarological societies. The Acarological Society of Japan began in 1992, with a newsletter and its own publication, the Journal of the Acarological Society of Japan, now in its seventh volume. The Systematic and Applied Acarology Society was founded in 1995 and dedicated to promoting development of acarology in China and elsewhere. It has a newsletter and website, and has published its own journal, Systematic and Applied Acarology, since 1996. The Sociedad Latinoamericana de Acarología (SLA) was initiated in 1994 during the 9th International Congress of Acarology. Its fundamental aim is to promote the development of investigations, as well as facilitate the dissemination of knowledge, in acarology among Latin American countries and elsewhere. All of these societies and their meetings are centered on a taxonbased science, focussed on the Acari. Increasingly, however, process-oriented research on physiology, ecology, genetics, and molecular analysis of Acari is pursued by many who may not consider themselves to be acarologists. As 1998 president of the Entomological Society of America, George Kennedy (1998) noted that our societies must regularly assess whether the format and programming options for our meetings accomodate the ongoing changes in disciplinary structure of our sciences. In acarology meetings, these changes include the increasing demands for interdisciplinary solutions to mite- and tick-related problems and phenomena. Journals. Apart from the 3 journals issued from acarological societies noted above, there are 3 widely circulated journals in which much of our acarological findings are now published. The doyen of these is Acarologia, a quarterly initiated in 1959 and now in its 39th volume. The International Journal of Acarology was founded in 1975. It is issued bimonthly and now is in its 24th volume. It gives one pause to realise that next year will see the 40th anniversary of Acarologia and the 25th of International Journal of Acarology! Experimental and Applied Acarology was initiated as a quarterly in 1985. It later became bimonthly and began issuing more than one volume per year, and more recently it became monthly and issues one volume annually. As a result, though just into its 14th year, it is in its 22nd volume. Three other periodicals merit note. In 1962 Acarologie was initiated and produced privately by Werner Hirschmann as Hirschmann-Verlag. With Hirschmann as the primary contributor to this publication, strictly devoted to the taxonomy of mesostigmatic mites, it progressed through 40 Folgen in 37 years, until the time of his death in 1993. In 1993 a new Russian periodical was begun, Acarina: Russian Journal of Acarology, now in its 5th volume. As of last year, the Journal of Arachnology has opened its door to the submission of papers dealing with behaviour, ecology, physiology, evolution, and higher-level systematics of the Acari. Just how widely open that door is, and how many people will want to submit papers to a journal whose readership long has focussed on arachnids other than Acari, remains to be seen. Electronic communication. Perhaps the most exciting recent advance in acarological communications is the appearence of

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websites for acarology and acarologists on the world wide web. An acarology home page developed by Zhi-Qiang Zhang, then at the Natural History Museum, London, is intended to promote the advancement of acarology worldwide. It presents a list of acarological journals with contact addresses, current projects in acarology at the NHM, regularly updated acarological news and announcements, other web sources of acarological information, and the beginning of a list of names of acarologists. We are also beginning to see user-directed acarological products on CDROM. Along with a burgeoning of web sites relevant to acarology is our marvellous capability to interact with colleagues and collaborators via e-mail almost instantaneously throughout the world, and the number of our colleagues having e-mail access has increased tremendously during the past five years. Some high profile research successes

Some examples of research successes that have had impact far beyond acarology in the biological sciences include the discovery by Wim Helle and colleagues (1978) and Marjorie Hoy (1979) of pseudoarrhenotoky, or parahaploidy, as a sex-determining mechanism among some of the lineages of parasitiform mites; the genetic engineering by Hoy and colleagues (1979) of resistance to acaricides in species of predatory mites used in integrated control of spider mite pests; the description by Marylin Houck and colleagues (1991) of a possible case of horizontal gene transfer between two species of Drosophila, involving a species of ascid mite as vector; advanced perspectives by Dana Wrensch (1993) on the adaptive advantages of sex ratio control in haplodiploid colonising species, with hypotheses for evolution of fixed and variable strategies for sex ratios that may explain a fundamental cause underlying the evolutionary success of arthropods, and by Wrensch and colleagues (1994) on the apparent pervasiveness of holokinetic chromosomes and inverted meiosis among the Acari and the possibility that these systems are ancestral in eukaryotic organisms; investigations of Marcel Dicke, Maurice Sabelis and colleagues (1988, 1990, 1998) on ‘infochemicals’ in tritrophic interactions between host plants, phytophagous mites and predatory mites, including odour-mediated responses of predatory mites to volatiles produced by plants under herbivore attack, and responses of phytophagous mites to the presence of conspecific and heterospecific competitors; the use of ribosomal DNA and mitochondrial DNA markers and sequences by Maria Navajas, Jean Gutierrez and colleagues (1997) to identify spider mites to species, to confirm conspecificity among biologically variable races of these species, and to assess genetic differentiation and host plant associations in polyphagous and biologically variable spider mite species (Navajas 1998); and investigations reported by Patrick Guerin during the Third Symposium of the European Association of Acarologists, Amsterdam, 1996, on individual chemoreceptors, specialised for reception of different aliphatic and aromatic constituents of host odours and substrates, on the first pair of legs of ticks and large mesostigmatic mites such as Varroa (Steullet and Guerin 1994a, 1994b). Elegant studies of Acari that are of perhaps more immediate interest to comparative arachnology include: the superb fine structure and ultrastructure studies of Gerd Alberti and collaborators on spermatozoa (Alberti 1980) and coxal glands (Alberti and Storch

IN ACAROLOGY

1977) of diverse taxa of Acari, and on particular acarine organs such as oribatid porose areas and related structures (Alberti et al. 1997) and oribatid trichobothria (Alberti et al. 1994); the functional anatomical studies of Harald Witte (e.g. 1978) and Giorgio Nuzzaci, Enrico de Lillo and colleagues on gnathosomal structures of representative mite taxa (e.g. Nuzzaci 1979; Nuzzaci and de Lillo 1991; Di Palma 1995); the detailed functional morphological studies of Igor Akimov and collaborators (e.g. Akimov et al. 1988, 1990, 1993) on external structures and internal systems of varroid, phytoseiid, cheyletid and tetranychid mites; and the studies of Witte (1984, 1991, 1999) on spermatophore morphology and miniaturisation, and modes of sperm transfer among Acari and other groups of Arachnida. In elucidating the homologies and functions of structures, these studies also offer important new characteristics for consideration in phylogenetic analyses of the relationships between major lineages of Acari. Our knowledge of Acari has progressed to the level where we are increasingly concerned about the conspecificity and distribution of closely similar organisms of major agricultural or medico-veterinary importance. The elegant studies by Jim Oliver and collaborators (1993) to determine the conspecificity or distinctiveness of ticks named Ixodes scapularis and I. dammini involved: (1) hybridisation and assortative mating experiments through F3 generations; (2) size-free discriminant analyses of morphometric measurements (see also Hutcheson et al. 1995); (3) analysis of chromosomes; (4) analysis of isozymes, including enzyme allele frequencies for 7 polymorphic loci to determine genetic relatedness; and (5) analysis of divergences in host preferences, vector competence, and life cycles. An analysis by Norris et al. (1996) of sequence variation in two mitochondrial ribosomal DNA genes, to test for maternal lineages, further confirmed Oliver’s results. This is an example of the powerful array of criteria that can now be brought to bear on problems of conspecificity that merit this level of resolution. Similar problems of the systematic status of closely related forms are evident among some of the species of the spider mite genus Tetranychus, particularly in the urticae species complex. Recent and ongoing molecular sequencing studies by Maria Navajas and collaborators (e.g. Navajas 1998; Gotoh et al. 1998) have shed considerable light on species and their intraspecific variability and distribution in this group. In so doing, the quarantine concerns of certain countries involved in the import and export of fruit have come to focus on the prevention of entry not only of exotic species but of physiological races of species that may already be present in a country in the form of other races. Clearly, the pressures of our global economy will continue to foster these problems.

III. SOME CHRONIC PROBLEMS IN ACAROLOGY Language and cultural barriers

Language and cultural barriers persist as obstacles to the dissemination of acarological information and literature, both in advanced and developing countries. Various of the fundamental papers by François Grandjean (e.g. 1934, 1939, 1941, 1947a, 1952) on acarine structure, terminology and notation, remain relatively obscure to acarologists who have not specialised in systematics of the Oribatei. Their obscurity has been also due in part to

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their being in French, with some published in journals having limited circulation. However, their availability has been enhanced by a reprinting of the complete works of Grandjean together with an index by van der Hammen (1972–1976). Timing has also played a role. For example, the magnificent magnum opus on Acari by Vitzthum (1940–43) published during the years of the Second World War was never really appreciated, even though it formed the core of a subsequent smaller book of more limited scope by Ed Baker and George Wharton (1952), which was widely consulted for many years. Vitzthum’s tome was published in German, in a very limited edition. Dissemination of information by way of computers and via the Internet and World Wide Web, along with the potential of nearly immediate computer-translation of information, should lessen these barriers. Acarological terminology

Thirty-five years ago, during the 1st International Congress of Acarology, Evans (1964a) reported on the formation of a committee on acarological terminology and plans for an illustrated glossary of external morphological terms. Then-current problems of conflicting systems of terminology and the confusion they caused were noted. Some 14 specialists of different orders of Acari were to prepare a preliminary draft of the glossary, but no end dates were proposed. Nearly 20 years later, in his presidential address at the 6th International Congress of Acarology in 1982, Evans (1984) reported that little progress had been made in compiling the glossary, notwithstanding the unilateral efforts of van der Hammen (1976, 1980) in publishing his Glossary of Acarological Terminology during the interim. The need for a comprehensive acarological glossary persists to this day. Systems of notation for setae and other external structures

Substantial advances have been made during the last 10 to 15 years in adapting a standardized system – that of François Grandjean (1934, 1937, 1941, 1947a, 1952) for the setae of the idiosoma and appendages of acariform mites – and applying it to mites of a wide array of families, both in Trombidiformes and Sarcoptiformes (the latter including the Oribatei and Astigmata). Don Griffiths and collaborators (1990) resolved the application of Grandjean’s system to astigmatic mites, while others did the same for a variety of trombidiform mites including many families of Heterostigmata (Lindquist 1977), Tetranychoidea (Lindquist 1985), and Eupodina (Baker 1990). However, taxonomists working in some groups have not yet adapted this system or realised its comparative importance and usefulness. Specialists of water mites, like those of chiggers, have seemed reluctant to adopt Grandjean’s system, and they continue their descriptive work in their own separate spheres. Recent endeavours by a few specialists of Parasitengona to rectify this must confront the difficulties of the holometabolous nature of postembryonic development of members of this huge lineage, and of the plethotrichy of setation that is characteristic of the deutonymph and adult of most of its taxa. Standardisation of terms and notation in the Parasitiformes, especially the Mesostigmata and Ixodida, has been hampered by the

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use of several modifications of one system for the idiosoma that originated with Max Sellnick (1944), which was limited to the idiosomal dorsum, though it was later extended to the idiosomal venter by Werner Hirschmann (1957). Fortunately, the one system developed for the appendages by Gwilym Evans (1963, 1964b, 1969) seems to be accepted by many taxonomists worldwide, without serious modification. Its use has also been extended to the larval instar of ticks and it may have potential for the larva of Holothyrida as well. The complex of lyrifissures, gland openings, and muscle sigilla manifest in parasitiform mites has not yet been well resolved by systems of notation that may indicate homologies between different supraspecific taxa, and which in turn may open up entire new suites of taxonomic attributes. Recent attempts by Hans Klompen and collaborators (1996) to do this for the Ixodida are a step forward, though their notation is awkward in some ways and in need of further comparative study. The earlier attempts by Claire Athias-Henriot (1969, 1970) to develop notation for the lyrifissures and gland openings in families of Gamasida have been largely ignored, and perhaps these need reconsideration. The serious application of a standardised notation implies hypothesised homologies of the structures so denoted, so that great care should be taken to study the ontogenetic expression and position of these structures. Ontogenetic studies have resulted in a variety of new attributes to define and distinguish taxa at supraspecific levels. They also have minimised the confusion caused by trying to cope with previous usages of a variety of incompatible systems of terms and notation. As yet, relatively few such studies have been made, and the new attributes resulting from them, particularly the ontogeny and patterns of leg setation, have not been accounted for in systematic revisions even in economically important groups like the spider mites. Limited knowledge of global acarofauna

Current classifications of the Acari and its families are based largely on our knowledge of acarine biodiversity in temperate regions. Paleoclimatologist Lonnie Thompson of the Byrd Polar Research Center of Ohio State University, recently noted (1998) that the key to understanding global climate is that one’s work must involve the tropical regions, which contain over 50 percent of earth’s land mass, and that their heat drives global weather. And so it may be with acarology from a global standpoint: the tropics surely contain far more than 50 percent of earth’s acarine diversity, and the ‘heat’ of acarine evolution and adaptation there may well drive global diversification, all the more so as tropical landmasses may not have been depauperated or deactivated by the polar effects of glaciation. Using the plant-parasitic superfamily Eriophyoidea alone as an example, one can estimate from the projections given by Jim Amrine and Terry Stasny in 1994 that only 10 percent of the estimated 25,000 to 30,000 species in the global eriophyoid fauna is known. Similarly, Bob Husband (personal communication, May 1998) estimates that the approximately 170 species known to him of the insect-parasitic family Podapolipidae represent about 10 percent of its world fauna. The unknown elements among tropi-

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cal acarofaunas will surely test some of our current familial and superfamilial concepts to the breaking point. Many startling discoveries have yet to be made amongst the Acari, even in areas other than the tropics. Recall that the somewhat enigmatic gamasid family Arctacaridae, which was discovered in arctic North America and described by Evans (1955) over 40 years ago, is still known only from boreal to arctic regions of the Northern Hemisphere. The classification and phylogenetic relationships of this family among other taxa of Gamasina remain problematical. As another example, the most early-derivative taxon of Eriophyoidea yet known, Pentasetacus, was described by Joachim Schliesske (1985) just 13 years ago in association with Araucaria trees in Chile. Little or no further surveying for these mites has been done elsewhere in the cool-temperate Gondwanian distribution of these ancient plant hosts. Moreover, just four years ago a new genus of relictual Araucariaceae was discovered by David Noble in Australia, in Wollemi National Park not far from Sydney (Anderson 1994). Though the isolated population of this tree is small and highly vulnerable (some 40 trees in one gorge), and access to it is highly restricted, has any concerted effort been made to sample the foliage of this tree for possibly an even more ancient taxon of Eriophyoidea – perhaps one retaining remnants of the third pair of legs? Still, warm-temperate to tropical regions are where by far the most undiscovered or undescribed species representing unknown suprageneric taxa are waiting to be found, and these may challenge or flesh out our current classificatory concepts of Acari. These may represent rare (rather than speciose) free-living taxa, or they may represent tips of evolutionary icebergs that, once noticed, may manifest a wondrous diversification within ecologically specialised circumstances. From my own experience, two examples of the former come to mind: the finding of but one specimen of Proterorhagiidae, a new family of endeostigmatic mites from a soil sample near the bottom of a natural vertical cavelike formation in Mexico (Lindquist and Palacios-Vargas 1991), and similarly, but one of a yet undescribed family of Eupodoidea at a lowland tropical rainforest site in Costa Rica. Despite knowing the exact location of these finds, repeated attempts to collect additional material at these localities have not met with success. In contrast, the description of Pyrosejidae as a new family was based on 10 species, 3 species-groups and 2 genera from samples of leaf litter through Mesoamerica, though only one of these species was described formally to validate the proposal of the new genus and family (Lindquist and Moraza 1993). Knowledge of this family challenges current cladistic definitions of the major groupings Cercomegistina and Antennophorina in the Trigynaspida. The tips of evolutionary icebergs are considered further below. Inadequately described taxa

In the description of species, there is an increasing tendency to leave previously described species inadequately accounted for, thus increasing the number of synonymies to be confirmed by subsequent authors. Relatively few authors describing species of Acari take time to study type material of previously described species, which often are inadequately described or described on material that is insufficient to provide data on variation within or between

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populations. Unresolved synonymies leave us with little idea of real distributions, habitats and host ranges of widely spread species, and they certainly confound the quarantine concerns of countries trying to guard against the introduction of pests.

IV. RECENT CONCERNS FOR ACAROLOGY Teachers and training in acarology

To be effective in providing a biological perspective on the Acari, courses offered in acarology should provide some basic information on the systematics, classification, morphology and development of Acari before leading into behavioural, ecological and applied aspects. How many institutions worldwide still offer more or less regularly a course in acarology? There are clearly fewer such courses given in North America now than ten years ago, and I wonder whether this is so across Europe and elsewhere, or will become so during the next ten years as key professors with acarological knowledge retire. If the wheel turns, such that the needs and funding for acarological expertise increase, it will be one thing to have term or indeterminate positions to offer – but will the next generation of candidates have the background to fill them? Can we continue to depend increasingly on short, seasonal programs in acarology given by very few institutions for training? How indeterminate will these programs be, as appropriate expert teachers leave the acarological scene? These are questions that our acarological associations and societies must address seriously, and soon. Our corps of retirees

We have undergone a serious thinning of professional acarological ranks during the last five years, when we consider the retirements of such productive mentors or researchers as Gwilym Evans, Jim McMurtry, Jerry Krantz, Wolfgang Karg, Ed Baker, Mercedes Delfinado-Baker, Magdalena Meyer, Gisela Rack, Don Chant, Harold Denmark, Tom Atyeo, John Kethley, Bob Husband, Bob Smiley, Anita Hoffmann, Jean Gutierrez, Shôzô Ehara, and M. Mohanasundaram, and the passing of others as George Eickwort, Marek Kaliszewski, Don Johnston, Isabel Bassols-B., Earl Cross, Werner Hirschmann, Russ Strandtmann, Ron Southcott, Carlos Perez-Iñigo, Nina Bregetova, and Paul Vercammen-Grandjean, among others. In North America alone, our biosystematic expertise for the economically most important family of plant-feeding mites, Tetranychidae, and the economically most important family of beneficial predatory mites, Phytoseiidae, is retired. In some cases, our retirees are so imbued with mites and ticks that they have continued to play highly meaningful roles in acarology. As in entomology, the contributions of retired associates in curatorial work, teaching programs, and productive research, is of increasingly critical importance, and their collaboration should be encouraged by adequate logistical support and facilities. As we face some hopefully serious collaborative acarological involvement in some of the major biodiversity investigations anticipated, we may be substantially dependent on the experience and expertise among some of our still-active retirees. Collections of Acari

As universities and other institutions have downsized their academic and research staff concerned with whole organisms, entire

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collections of Acari have been jeopardised as orphaned entities, which many institutions no longer want to, or can afford to, maintain. As a result, collections are being amalgamated into larger collections that are being maintained by fewer and fewer institutions, which is cause for major long-term concern. Arrangements must be sought for the maintenance of taxonomically and ecologically significant collections of type, voucher and reference specimens on a truly indefinite basis. This is another subject that our societies and associations should address. Another ongoing and unresolved problem with mite collections is the deterioration of slide preparations of mites mounted in impermanent media such as Hoyer’s and similar forms of Berlese media, and polyvinyl alcohol and similar media. Although fully impermeable ringing sealants are known to extend the ‘life’ of Hoyer’s medium for nearly a century, the spectre of eventual deterioration and subsequent restoration of hundreds of thousands, and perhaps millions, of slide preparations is a horrific inevitability. Committees have been struck to consider this problem, but a general resolution has not been reached or promulgated. Recently-developed computer programs have facilitated the initiation of interactive databases for collections. For example, BIOTA (Colwell 1996), a specimen-based relational database, enables a variety of data to be captured, including entry fields for date and time of collection, sampling methods, site, habitat, microhabitat and vegetation, plus a range of structural and molecular data, including text and images. Barcoded labels that allow rapid accessioning of specimens and linking them to databases can now be applied to preparations of specimens on slides, pins or in alcohol.

V. FUTURE ENQUIRIES FOR ACAROLOGY More than ever before, as we have acquired much knowledge on a diversity of Acari, there remains unanswered a vast variety of fascinating questions. Following is a variety of topics that come to mind, but each of you can think of a series of examples that reflect your own experience and interests. Dispersal mechanisms and patterns among mites representing major taxa that live in patchy habitats

In some cases, phoresy is the obvious and evident behavioural mechanism, e.g. for a great variety of mites associated with insects that cohabit subcortical habitats, beach wrack, bracket fungi, manure piles, etc. But consider the taxa of obligately phytophagous mites with considerable host specificity. Apart from the subfamily of spider mites capable of spinning silk and dispersing passively by ballooning on the wind, how do the other groups disperse? How do bryobiine spider mites and tenuipalpid false spider mites disperse? There are few observations about this, but Pieter Oomen’s studies (1982) on Brevipalpus phoenicis indicated that these mites are sedentary, showing little tendency to move about, and that they ‘…tend to remain on the same bush while migrating, thus keeping the mite populations of the bushes separate.’ Can this be the general picture? How do eriophyoid mites disperse? There is considerable evidence of dispersal by wind currents for members of this group, yet some recent arguments put forward by Mous Sabelis and Jan Bruin (1996) suggest that wind

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alone is not sufficiently effective for the dispersal of such host-specific mites. How do arboreal predatory cunaxid mites disperse? And so forth…. Further acquisition and evaluation of data on behavioural patterns of dispersal among major groups of mesostigmatic mites are also needed. The deutonymph is evidently the instar primitively adapted for phoretic behaviour among taxa of Mesostigmata, e.g. Uropodina, Sejina, Parasitoidea, Rhodacaroidea. As well, I (unpublished) have recently confirmed the deutonymph as phoretic in one species of Veigaiidae, a relatively early-derivative family of Dermanyssina. In more derived families, e.g. Ameroseiidae, Ascidae, Phytoseiidae, Hypoaspididae, it is the adult female that behaves as the dispersant, either phoretically or, in the case of Phytoseiidae, passively by wind drift. The patterns are less clear among the families of Eviphidoidea and Trigynaspida, and a correlation of the dispersal instar with some other biological attribute(s), such as sex-determining mechanisms and sex ratios, remains to be elucidated. Sex-determining mechanisms and patterns among lineages of Parasitiform and Trombidiform mites

Considerable progress has been made in this area, as synthesised in a recent major paper by Roy Norton and collaborators (1993). An overlay or correlation of these patterns with families or higher groupings of these mites remains incomplete, along with some accordant scenario of how, why and when these patterns may have evolved. Biogeographic patterns of major lineages of Acari

Some relatively early derivative taxa of Acari, e.g. Holothyrida, manifest Gondwanian distributions that, along with their absence in the Devonian fossil record as known so far, perhaps belie how ancient these lineages may be, in contrast with early derivative lineages of Acariformes that manifest a Pangaean distribution. However, similar patterns of Gondwanian distribution are evident among some much more recently derived taxa, e.g. some genera (Gamasiphoides, Evanssellus) of Ologamasidae according to David Lee’s work (1970). What do these patterns mean, and how should they be interpreted? Clearly, care should be taken in deploying such data to negate or support relationships between lineages, including Parasitiformes and Acariformes, and their relative ancientness. Studies of acarine biogeography from other standpoints, such as whether some lineages reveal major disjunct distributions like eastern Asia and eastern North America, or whether centers of endemism are evident, are still in their infancy, though considerable progress is being made for some groups of Oribatei. Tolerances of habitats with great heat or pressure

Advances have been made in understanding the physiological mechanisms of extreme cold hardiness among some Acari in polar extremes (e.g. Block 1980; Cannon and Block 1988). However, we know little or nothing about how some water mites tolerate living in aquatic habitats as hot as 50°C, and how some halacarid mites survive under deep sea pressures at 5000 metres below sea level.

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Size and secondary reduction of peritremes in the Parasitiformes

The general function of peritremes in respiration and their more specialised function as plastrons are known from the literature on parasitiform mites (Hinton 1971). Holothyrid mites have well developed peritremes, but the stigmata of Ixodida ticks lack peritrematal extensions. Both well developed and highly abbreviated peritremes are evident among relatively early derivative families of free-living Mesostigmata, though patterns have not been analysed cladistically. Clearly, peritremes have become abbreviated secondarily among some of the more recently derived genera of mites that are closely associated with insects, such as iphiopsine Laelapidae and Varroidae, and among some species groups of Digamasellidae. What is the adaptive value of the shortened state? In a paper published this year, Jay Yoder (1998) wondered whether the peritremes of Typhlodromus occidentalis, which are short relative to those of most other species of Phytoseiidae, help favour water retention by reducing water loss across respiratory surfaces. This mite thrives in arid regions of western North America, where it is an important biological control agent of spider mites. However, its most closely related species, T. longipilus, has somewhat shortened peritremes but it does not appear adapted to thriving in arid regions. Clearly, more data that relate peritrematal length to water loss prevention are needed to test Yoder’s notion. A severe peritrematal shortening is also found in a few derivative genera of Zerconidae, no members of which are known to have other than a free living way of life. Also, in most zerconids and some digamasellids at least, the peritremes become abbreviated ontogenetically in the adult instar from a greater length in the deutonymph, which may indicate a secondary shortening. There is much room here for biological investigation. Homologies of tarsus I sensilli among Parasitiform mites

The relatively densely setose, dorsal sensory field on the apical third of tarsus I in parasitiform mites has been the subject of a number of independent studies that span many decades. However, none of these studies came to grips with the homologies of setae in this sensory field between different major groupings of these mites. Some focussed on the homologies of setae, and developed a notation that was applicable to just a few taxa within one family. Others considered a broader range of families, but could not resolve the homologies of sensilli of Gamasina with those of Antennophorina or, in turn, with those of Haller’s organ of Ixodida. Clearly, part of the problem has lain in attempting to recognise homologies among more derived taxa whose tarsal sensory fields lack a relatively full complement of sensilli and have the remaining sensilli diversely modified. According to recent work of Pekka Lehtinen (1991), the sensilli of Haller’s organ in the families of Holothyrida have evident homologies with those of Ixodida, which in turn may be comparable to the telotarsal sensory field of Opilioacarida. The sensillar homologies should be clarified for Holothyrida and Ixodida, using a variety of the sophisticated fine structure and electrophysiological techniques now available, as well as the classical ontogeny, form and position of sensilli. Thereafter, it should be possible to turn to exemplars of the more setose earlier derivative taxa of Antennophorina and Sejina to determine the homologies of their sensory field struc-

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tures on tarsus I, and then to work upwards into the less setose, higher derivative taxa of Gamasina. Function of urnulae in balaustiine mites

In deutonymphal and adult balaustiine mites, one or two pairs of structures, termed ‘urnulae’ by Southcott (1961), are present as conspicuous cylindrical protrusions with paddle-like setae on their rims, either as one pair behind the lateral eyes on the prodorsum, or as two pairs, of which the second pair is positioned posterolaterally on the opisthosoma. They are well known as external structures but nothing is known of their function and internal structure. Other terms for them, such as ‘verrues dorsales’ by François Grandjean (1947b) and ‘glandular openings’ by Irv Newell (1963), seem inappropriate, though ‘Rückenstigmen’, coined earlier by Oudemans (1916) and used by Willmann (1951), may be closer to the mark. It seems that nobody has examined them carefully. Harald Witte’s studies of the functional anatomy of erythraeid structures, especially his paper on the gnathosoma (1978), came close and even dealt with the main pair of tracheal stems that terminate in an end chamber from which arise numerous tracheoles. In freshly mounted specimens of Balaustium, I have noted that the tracheal trunks stop near and below the prodorsal urnulae, but no spiral-walled trachea is evident leading dorsally to the urnula. Is the dorsal surface of the urnula covered by a flap? May the urnulae be elaborated and modified cupules representing ia and ip? Silk production in trombidiform mites: location of the silk-producing organ and form of the emitting structure

The location of the silk glands and their spinnerets are known for but few of those trombidiform taxa that are capable of producing silk. Unpublished observations by Mark Judson, presented during the Third Symposium of the European Association of Acarologists, Amsterdam, 1996, have confirmed that members of the anystid subfamily Erythracarinae have palpal silk glands, with a pair of ducts opening through two modified hollow setal spinnerets at the tip of each palp, much as in the sister subfamily Anystinae. This arrangement, though simplified to one duct opening through a single enlarged palptarsal eupathidium, is also found in the spider mite subfamily Tetranychinae, in contrast to silk production by glands of the podocephalic canal among members of the Eupodoidea. The palpal silk gland system is postulated to be phylogenetically older, and perhaps present in the common ancestor of all acariform mites, while the system in Eupodoidea is thought to be an autapomorphy of that group. The door is wide open to test these concepts with investigations of the silk-producing systems of other groups known to spin silk, e.g. Cheyletidae, Tydeidae, Bdellidae, Cunaxidae, and perhaps taxa of Eriophyoidea thought to produce silk-like substances. Vertical movement among oribatids: correlated with parasitism by cestodes?

There is a large body of data showing that acanthocephalan worms can modify the behaviour of their intermediate arthropodan hosts to make them more accessible to consumption by vertebrates that become the final, or definitive, hosts of the worms (Moore 1984). For example, uninfested amphipods shun light, and when disturbed, burrow into bottom mud. When parasitised

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with Polymorphus paradoxus, however, they move toward light, and when threatened, tend to cling to floating vegetation or skim along water surfaces where they are readily consumed by dabbling ducks such as mallards, which are the final hosts of this worm (Holmes and Bethel 1972). As reviewed by John Wallwork (1976), it is well established that some taxa of soil-dwelling oribatid mites show vertical movements which generally take them upwards from the soil onto the aerial parts of vegetation during the daytime, and downwards at night. Factors other than temperature may stimulate this behaviour. Several species of grassland oribatids are known to act as intermediate hosts in the life cycles of various anoplocephalan tapeworms of sheep and cattle (Rajski 1959), and this diurnal behaviour pattern would facilitate transmission of the parasites from the intermediate host to the grazing mammal as the final host. Investigations are in order to determine whether the diurnal behaviour pattern of oribatids is a result of their being parasitised by these worms. Feeding behaviours and patterns in selected taxa of Acari

How prevalent is predatory behaviour among genera of the Stigmaeidae? The determination of members of the genus Eustigmaeus (=Ledermuelleria) as moss feeders by Uri Gerson (1972) long ago put an end to the concept of stigmaeids generally being predators, though members of some genera like Agistemus and Zetzellia certainly are. Investigations on the behaviour of members of other genera would not only clarify their feeding preferences but they might shed light on the phylogenetic relationships among genera. Similarly, the question, ‘How prevalent is fungivory among Tydeidae?’, may clarify whether phytophagy or predation are preferred ways of life among some members of this group, and help shed light on position of the subfamily Pronematinae in the superfamily Tydeoidea. Elucidation of life histories and developmental instars of selected taxa of Acari

Many of you will have your own selection of taxa in mind as I address this area of investigation. However, I have in mind some fascinating examples of mites with probable tri- or quadri-trophic relationships that involve at least a phoretic association with insects that inhabit temporary habitats. As an example among Parasitiformes, adult females of the ascid genus Mucroseius are phoretic in the metathoracic spiracular atria of adult sawyer beetles of the genus Monochamus, some of which are vectors of the nematode that causes the highly destructive pine wilt disease in conifers (Lindquist and Wu 1991). The adult female mite has a peculiar pointed process apically on its fixed chela; the adult male and developmental instars remain unknown. Undoubtedly, these mites undergo their life history in the galleries of the wood-boring larvae of their hosts. What are the feeding habits of these mites in association with the immatures of the beetle, the burgeoning population of nematodes, the growth of subcortical fungi, and the succumbing of the tree host? Could a DNA sequencing method be used to discern the nature of the gut content of these mites when active in the galleries?

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As an example among Trombidiformes, adult females of the heterostigmatic family Athyreacaridae (Lindquist et al. 1990) are phoretic on adult athyeriine scarab beetles, which excavate vertical burrows in soil and provision the bottom of them with compacted accumulations of plant fragments as food for their young. Such provisioning would appear to form an ideal substrate for fungal growth, in the absence of beetle brood. The adult female has strongly-formed cheliceral stylets and extensive areas of plicate soft cuticle on the body that indicate a capacity for expansive physogastry. The adult male and developmental instars remain unknown, but these mites almost certainly undergo their life cycle in the subterranean galleries dug by their beetle hosts. Whether the female mites are parasitoids of the immatures of the beetles or fungivores in their nest is unknown. Classifications based on molecular analyses

Recent phylogenetic analyses based on DNA sequence data or other molecular techniques to improve phylogeny-based classifications have met with some success and some problems, as well as resistance to their acceptance when they challenge previous classifications based largely on morphology. One problem is the conflict posed by unrooted molecular analyses resulting from alternative choices and sequences of outgroup taxa. In a study on phylogenetics of whales published this year by Sharon Messenger and Jimmy McGuire (1998), the combined analyses of molecular and morphological data provided well-supported estimates consistent with that based on morphological data alone. Rather than re-interpret morphological attributes in the context of a controversial molecular tree, a larger data set composed of molecular and morphological attributes was recommended for phylogenetic analyses. Ultimately, if the results of such analyses are going to be applied meaningfully to nested sets of taxa recognised, each taxon should be defined by apomorphic attributes, or admitted to be an unresolved and possibly paraphyletic or polyphyletic group. An abbreviated molecular phylogenetic study of 19 species of Tetranychoidea, representing 8 genera, 2 subfamilies and 2 families, was given by Maria Navajas and Jean Gutierrez (1996) at the 9th International Congress of Acarology. Its results largely supported previous classifications based on morphological and biological attributes, though it questioned the monophyly of the genus Oligonychus. This agrees with discordances in some unpublished observations that I have, based on the leg setation of members of this genus. A newly published analysis of DNA sequence variation among species of Dermacentor by Paul Crosbie and collaborators (1998) indicates that D. occidentalis and D. variabilis are distinct species. However, D. albipictus shows substantial intraspecific variation and warrants further investigation to determine whether it may be a species complex. This parallels the considerable variation in colour, size and morphology noted long ago by Cooley (1938), who was first to establish a synonymy between two forms that were treated by previous authors as separate species, D. albipictus and D. nigrolineatus. The paucity of morphological attributes and the difficulty in determining their homologies, and a lack of an informative fossil record, hinder us from developing a plausible phylogeny and

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accordant evolutionary framework for some major groups of Acari, such as the Eriophyoidea. A phylogenetic hypothesis along with an evolutionary framework that considers trophic ecologies has been newly proposed for the phylum Nematoda, based on analysis of 41 small subunit ribosomal DNA sequences from a wide range of nematodes by Mark Blaxter and collaborators (1998). The results indicated that convergent morphological evolution may be extensive, that animal parasitism arose independently at least four times and plant parasitism three times, and that the present higher-level classification of the Nematoda needs revision. Studies of this sort for the Acari are awaited with interest. Eriophyoid mites are so morphologically reductive that there are relatively few attributes left by which to analyse and classify them, and to base the genera, tribes and higher categories consistently. In the highly speciose family Eriophyidae, unrelated taxa may have evolved to resemble one another. For example, the genus Aceria may consist of two unrelated lineages that are morphologically similar. Recent observations by George Oldfield and Katarzyna Michalska (1996) indicate that it contains species on monocot hosts, in which sperm is stored in both spermathecae of females, as otherwise is found among members of the primitive family Phytoptidae, while its other species, found on a variety of more derived taxa of hosts, are typical of Eriophyidae in storing sperm asymmetrically in just one of the pair of spermathecae. Perhaps analyses of DNA sequences or other molecular approaches can resolve such problems of reductive convergence. Acarine pathology

Acarine pathology is an undeveloped field. Information on the groups of parasites and pathogens associated with mites is still fragmentary, and existing accounts are mainly descriptive. Mites offer opportunities to investigate new pathogens and new types of associations, some of which may have a potential role in control of pests. Mite-specific parasites, pathogens and associations may, when elucidated, enhance our basic understanding of pathogenhost systems in general. A newly published review article by George and Roberta Poinar (1998) provides a good perspective of investigations needed in this area.

VI. FUTURE CHALLENGES FOR ACAROLOGY Identification and descriptive taxonomy of Acari

There is an ongoing, in fact an increasing, need for whole organism expertise in identification and alpha-level taxonomic description of Acari, and this in the face of a steady, serious decline in such expertise and positions for such expertise. On one hand, much of the descriptive work being done is parochial and inadequate for subsequent users without access to the type material of the described species. On the other hand, less and less descriptive work is being done, often in countries or regions most in need of it. Some reviewers demand that any presentation or review of new and described species of a genus or family should be accompanied by a cladistic analysis. In my view, this is simply premature in many cases, particularly with such an inadequate representation of taxa yet known on which to base such analyses. In view of the few people hired and overburdened with responsibilities for whole organism description and identification, there is simply not

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time for this next level of beta or gamma systematics. For purposes of imminent major projects on biodiversity and use of organisms as bioindicators of environmental change, as well as for quarantine decisions concerned with our global economy, the immediate needs are for adequate description, information on distribution and hosts, and reliable identification of regional and global acarofaunas. If acarology is to have a role in these enterprises, we need to have an accelerated production of excellent alpha-level taxonomic revisions, regionally and globally. An example is Keith Hyatt’s fine 1980 revision of the subfamily Parasitinae in the British Isles, with keys to deutonymphs, females and males, good illustrations and descriptions for these instars and even for protonymphs and larvae when available, notes on their habitats, and their regional and more general distribution; no phylogenetic considerations are presented. Keith has retired and very few whole organism acarologists continue with this kind of work. Solid alpha-level revisions are also a prerequisite to the development of computerised interactive keys. With the decline in tenured or indefinite positions for taxonomists to do this work, should we seriously consider a less costly option of training parataxonomists, or parabiologists, for some of this alpha-level work? There are probably some in our midst (or a more general midst) that may question the continued need for this kind of work at all, in view of our technological capability to identify species by DNA fingerprinting. Why not just describe and identify species in this way, rather than via the labor of whole organism observation and description? While molecular techniques are powerful and increasingly critical adjuncts to circumscribing species, they do not provide us with the generalisations that can be gleaned from morphology, e.g. feeding behaviour, ontogeny, phoretic behaviour, host range, overwintering behaviour. Acquisition and study of missing links

For the ticks, of course, the finding of all instars of the type and only known species of Nuttalliellidae is critical to an enhanced understanding of the relationships between the major lineages of Ixodida. Only the nymph and adult female are known as yet, and attributes of the larva and adult male may be quite informative phylogenetically. Harry Hoogstraal (1985) suspected that lizards or the rock hyrax (Procavia capensis) may be preferred hosts of this tick. For the Tetranychoidea, the finding of all instars of the enigmatic genus Allochaetophora is important to a fuller understanding of the relationships between families of this superfamily. Described originally (McGregor 1950) and long known subsequently only from a single deutonymph collected from Bermuda grass in California, the larva, deutonymph and adult female and male of a second species were collected from grass in South Africa and described recently by Magdalena Smith Meyer and Eddie Ueckermann (1997). Setal counts for the leg segments were given, but a study of the ontogeny and homology of the leg setal patterns, which would give insight to the relationships between this and other families of Tetranychoidea and test the hypotheses already given for its position among these families, was not attempted. I have already noted the possibility of an early derivative taxon of

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Eriophyoidea existing in the recently discovered genus of Araucariaceae in Australia. Acarine biodiversity

Regional studies on biodiversity have recently become one of the hottest research areas, with promise of increased funding for large-scale investigations to cover a selection of many (though perhaps not all) taxa of eukaryote organisms. Studies of biodiversity are fundamental to understanding not only comparative species richness in different areas, but also to establishing baseline information upon which to evaluate losses or changes in the biota of areas due to impacts of climate, cataclysmic events, and landscape changes by humans. The use of selected groups of organisms as biological indicators of environmental change in a given area depends on baseline data on the biodiversity of those groups in that area. In the wake of little having been added to the sum of scientific knowledge on biodiversity five years since the signing of the UN biological diversity convention, there is increasing demand to move on with investigations to identify and classify the unknown 80 percent of Earth’s biota, to begin to unravel the complex mechanisms through which different species depend on each other for growth and survival, and to find consensus on the rate of biodiversity loss. We should make every effort to have the Acari, or subsets of the Acari, included in such studies wherever they are undertaken. However, there will be much, much to do if the Acari are included, and who is going to do it? Although biodiversity is not officially recognised as one of the core research topics of the Long Term Ecological Research network areas, it is widely seen as fundamental to understanding ecological processes. LTER has recently focussed on developing a broader-scale understanding of processes that lead to and maintain biodiversity and the influence that these processes have on ecosystem structure and function (Waide 1998). Cross-site studies on the relationship between productivity and species richness based on data from LTER sites would be useful in examining this question. The Australian LTER effort is back on line, and five national networks in Latin America have appeared and are moving toward a regional network (French 1998). The establishment of LTER networks in other countries is expanding the opportunities for meaningful cross-site studies. Notable also, urban LTER sites, such as the Central Arizona – Phoenix LTER, are being initiated to monitor human-induced ecological changes resulting from rapid land-use transformations (Anonymous 1998). Along with the indicator aspect of biodiversity studies, an exciting new opportunity for interactivity of long-term research on a global scale has become available through the Global Terrestrial Observation System (GTOS), established in 1996 by several co-sponsoring organisations including the United Nations Environment Program (UNEP), Food and Agricultural Organisation (FAO), and Educational, Scientific and Cultural Organisation (UNESCO). The central mission of GTOS is to provide data for detecting, quantifying, locating and providing early warning of changes in the capacity of terrestrial ecosystems to sustain development and improvements in human welfare (Gosz 1998). Protocols for standardised methods of collecting targeted groups of arthropods should be planned to facilitate comparisons

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between the biodiversity of different ecozones or other delimited regions. Computerised, compatible relational databases will form essential components of these studies, and funding for data gathering and entry by suitable support staff must be a component of these projects. Tips of investigatory icebergs

While collaborating in the Arthropods of La Selva (ALAS) project in a lowland tropical rainforest area of Costa Rica during the last few years, my eyes have been opened as to how amazingly diverse and fascinating are the Acari in just this one small area (ca 1600 hectares, with an altitudinal gradient of only 115 meters). Some of Rob Colwell’s more recent investigations (e.g. Colwell 1995; Naskrecki and Colwell 1998) on hummingbird flower mites and their interaction, competition and specialisation for flower resources were realised there. And there are other interactions of equal fascination to investigate at La Selva. The tarsonemid tribe Tarsonemellini is represented there, and the intricacies of these mites in association with the agaonid fig wasps which pollinate the figs and whose larvae inhabit the fleshy syconial receptacle of figs that the mites cohabit (Compton 1993), is just begging to be revealed. Using the family Ascidae as a focal taxon for assessment of the biodiversity in that one small area serves as an example of what has yet to be described and investigated. We have collected and recognised about 100 species of Ascidae, nearly all of which are undescribed and include at least seven new genera, including two in the tribe Melicharini, two in the tribe Blattisociini, one in the subfamily Arctoseiinae, one in the subfamily Platyseiinae, and one of uncertain placement. Several of the new genera are represented by bizarre mites whose unusual structures beg for investigations of their function and the mite’s way of life. One is an amazingly stilt-legged form associated with a genus of bracket fungus; the length of its legs put to shame those of podocinid mites. Another is a thick-legged form associated with another genus of bracket fungus. It reminds one a bit of the genus Hoploseius, which is also found there in association with other bracket fungi, but it is not a member of the same tribe. Another has females with a pair of large circular areas of soft cuticle that appear to be suctorial and reminiscent of those of heterozerconid mites. The new genus of Platyseiinae is found in nests of Azteca ants in the hollowed internodes of stems of Cecropia trees, and is the first example of this subfamily known to have other than a free-living way of life. Although some of the field work by the eminent authorities Bert Hölldobler and Edward Wilson (1990) for their monumental book on ants was done at La Selva, these mites apparently did not come to their attention. Two species in one of the new genera of Melicharini undergo their life cycles apparently quickly on the inflorescences of a genus, Spathiphyllum, of Araceae (aroids) and a genus, Calyptrogyne, of Palmaceae, respectively. The mites apparently develop rapidly during the limited time of development of the inflorescence, called a ‘spadix’, between the onset of flowering and fragrance of one sex and the subsequent flowering and fragrance of the other sex on the same spadix a week to ten days later, by which time a new generation of adult female mites must be ready pho-

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retically for visitations by pollinators. One spadix may bear hundreds of the developing mites in all instars. Adult males have bizarrely-modified setae peripherally on the body dorsum and on the dorsal surfaces of legs, which may perhaps be used aggressively, in much the same way as in male hummingbird flower mites. Carriers of the female mites are primarily Trigona bee pollinators for the aroid host, and Dermanura bat pollinators and Lagochile scarab beetle visitors for the palm host (Saul Cunningham, personal communication, June 1998). Even within one of the known genera, Lasioseius, the diversity of about 50 species is fascinating and the disparate forms of cheliceral structure alone are indicative of diverse feeding behaviours. Some of the forms of dorsal shield ornamentation are spectacular, though their adaptive value is unknown. Perhaps our most fascinating find is the microcosm of Acari found within the young unfolded leaves of large, sheath-leaved, monocotyledonous plants, such as Heliconia. These are invaded by hispine beetles of several genera, where we have found: First, members of an undescribed family of Gamasina. All instars live on the adult beetles and have strangely modified mouthparts for an unknown way of life with their hosts. We have two genera and several species of this group, which evince considerable host specificity with the beetles. Second, members of a new genus apparently of Ascidae. Its adult females maintain contact with the adult beetles, running off and on them. There appear to be several species, again indicating host specificity with the beetles. All instars have wonderfully elongated cheliceral shafts apparently adapted for reaching for nematodes in the water film of the folded leaf surfaces. These shafts are fully retractable, and whether this involves some unusual mechanism of telescoping is problematical. After examining them, my esteemed colleague Gwilym Evans’ summary comment about the chelicerae of these mites read, ‘The whole structure is intriguing and begs so many questions’ (G. O. Evans, personal communication, October 1997). Third, members of a new species-group of Lasioseius, which are probably also phoretic on the hispine beetles, in the apparent absence of other potential carriers. Again there are several species, and some degree of host specificity may be involved. Fourth, members of at least one new species of Macrocheles, which appears to represent a distinctive species-group according to Jerry Krantz (personal communication, June 1998). Fifth, members of one or two taxa of Histiostomatidae, about which I hope to obtain comment from Barry OConnor, and sixth, members of at least one taxon of Canestriniidae. The behavioural and trophic interactions of this assemblage of mites, nematodes and their hispine beetle associates in a temporarily almost closed system of the host plant leaf, provides a fascinating arena for investigations on a food web which may yield results to rival or exceed the story about hummingbird mites. How many such examples exist elsewhere, particularly in tropical regions? As just one example, what is the way of life of species of the poorly known and somewhat bizarre-looking tarsonemids of the genera Nasutitarsonemus and Tarsanonychus associated with hispine beetles on leaves of palms and other trees in southeast Asia (Lindquist 1986)? The key to detecting such associations is the

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often serendipitous finding of the phoretic association of one instar of a mite on insect carriers that occupy special niches of a transient nature. Many poorly known species and genera are known only from such phoretic instars. Our challenge is to engage others to initiate biological investigations on the ways of life of these mites and their carriers in their niches. Public awareness and support

One of the most serious shortcomings in support of the study of Acari is the public’s general lack of awareness of our science. Attracting the public to the Acari and acarology is not easy, other than its general awareness of pests like ticks, chiggers, house dust mites, spider mites, and varroa mites of bees. As John Conroy noted during the plenary session of the 8th International Congress of Acarology at ¯eské Budejovice, ‘Let’s face it , we are losing the Public Relations game.’ Indeed, we have not conveyed the inherent beauty and elegance and pervasiveness of Acari to the world at large. Not since the wondrous hand-painted likenesses of mites and ticks among other arthropods by C. L. Koch (1836–1841) over 150 years ago and by Antonio Berlese (1882–1903, and unpublished) about a century ago have there been serious efforts to capture the beauty and diversity of colour and form of Acari, coupled with information about where these vibrant dots of life may be found. We now have modern techniques to promote this and to bring the world of Acari to arenas of public enjoyment or curiosity. Scanning electron microscope images of Acari have conveyed some of the beauty of form to a wider readership, but they are colourless (unless enhanced by computer imagery) and lifeless, and they do not come close to capturing the vivid depictions of Berlese. So-called microvideo cameras can now capture with adequate resolution the colour and action of mites, to some extent under natural conditions – and surely these will continue to improve. The videos of Rob Colwell and collaborators on hummingbird flower mites are an example of this, and earlier, the fascinating observations of Asher Treat on moth ear mites approached this in an audiovisual presentation confined to a meeting. Popularly written articles with colour images in periodicals with large subscription and wide circulation, such as National Geographic, New Scientist and yes, even Popular Science, as well as television documentaries for programs such as the Nature of Things and National Geographic Explorer would narrow the gap of unawareness of the world of Acari. Dave Barr’s 1970 article, ‘Tiny wolves of the water’, published in Natural History magazine is an example, as is, of course, Rob Colwell’s 1985 article, ‘Stowaways on the hummingbird express’, in the same magazine. There are so many aspects of Acari that could be focussed upon in spectacular ways – the unbelievable speed of erythracarine mites in open areas, the amazing tolerance of some water mites to scalding hot water, the presence of mites in the muck of deep sea floors, the incredible fecundity of acarid mites whose populations may burgeon into countless millions in stored food products, the level of toxicity of venoms produced by some pyemotid mites, the numbers and diversity of mites in a square meter of forest litter, the emphysema in honey bees caused by tracheal mites, and on and on. Such accounts need an imaginative, though accurate, style of presentation, like Asher Treat (1975) began some of his narrative

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on moth ear mites: ‘The magic of the microscope is not that it makes little creatures larger, but that it makes a large one smaller. The microscope… makes us, for a time, fellow citizens with the great majority of living things. It lets us share with them the strange and beautiful world where a meter amounts to a mile and yesterday was years ago. Let us shrink to the height of a moth ear mite, creep under the wing of a sleeping noctuid, and roam for a little while through the sculptured caverns of the insects’s ear.’

themselves. Perhaps they see an order in our messy bedlives … that we have not discovered yet. Perhaps they regard us as glorious, even… As a rule, we do not sing in our beds. We have no need. The mites sing for us. Sing of us. They are our Greek chorus, … choirs of microscopic angels ever ready to dance on the head of a pin. …’

VII. BRIEF CONCLUSIONS

We need books for children and their parents to nurture their awareness of Acari in the world around them – the brightly coloured, swimming specks in ponds, the red whirligig mites on all sorts of surfaces including tables, the erinea of eriophyoids on leaves, the spider mites on ornamentals and false spider mites shaken from cedar hedges, the mites in ears of bats and those in nares of hummingbirds, etc. Recently, we showed our 3-year-old grandson the abundance of small red Balaustium mites, their bodies about 1 mm long, that run over curbs and cement retaining walls alongside the lawns and gardens in our suburban yard. He now delights in spotting them and watching them scurry about. They are just as familiar to him as are ants, bees, flies, and butterflies.

Tenured or indefinite positions devoted primarily to acarology will continue to decrease. Our challenge is to endeavour to highlight the Acari as subjects of importance and interest for multidisciplinary investigations, as well as attractive animals in the natural world around us that the public in the broad sense is willing to support.

Perhaps we can not go so far as to capture an audience of amateurs by means of handbooks or paperback guides to the Acari like those for the butterflies, mushrooms, etc., but we could appoach this to some level, to genera in some cases like tracheal mites, to families or superfamilies in other cases like ixodid hard ticks, spider mites and eriophyoid mites, and to higher categories for others like oribatid mites. In addition, the images that can be captured and reproduced on the World Wide Web offer more captivating possibilities to promote and engender a natural history level of enjoyment of the Acari.

It has been my special pleasure to share these thoughts with you.

Speaking of popularised accounts about mites, I cannot refrain from sharing an example quoted with permission from a recent novel, Half Asleep in Frog Pajamas, by Tom Robbins (1994), which may raise the level of public awareness of mites in one synanthropic niche, at least: ‘You kick off your shoes and flop onto the bed – landing, of course, among millions of mites. Had you any inkling that your bedding was alive with arthropodic crablets, chomping away on flakes of your dead skin, you would be so disgusted you would probably choose to lie on the floor. Yet every one of us, including the rich, the pious, and the royal of blood, sleeps each night in colonies of such mites. The ultimate witnesses, the most intimate voyeurs, these mites. What books they might author, what tales they could tell! …. Who knows more of our secrets? Who? Nightly, and often by day, they sail with us in the lunar barge, their flake steaks marinated in our tearwater, their breakfast boiled in our sweat, the winds of our farting at play in their hair. They are familiar with wife and mistress, husband and lover, hot-water bottle and fetish, favorite sitcom and favorite drug; have memorized confession, recrimination, prayer, delirium, and that sweet name we cry out in our sleep. … Yes, all this: but the mites do not betray us. If they gossip, it is only among

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We have not yet conveyed the overall importance of the Acari to the tax-paying public. Edward Wilson (1990) once said, ‘If all mankind were to disappear tomorrow, the world would regenerate back to the rich state of equilibrium that existed 10,000 years ago. If insects were to vanish, the terrestrial environment would collapse into chaos.’ Can we make such a statement, and back it up with convincing data, about the Acari?

ACKNOWLEDGEMENTS I am grateful to Michelle MacKenzie and Marc Simard for their computer skills in scanning, organising and enhancing many of the illustrations that accompanied the oral version of this presentation. Permission granted by Bantam Books, to quote a passage from Half Asleep in Frog Pajamas by Tom Robbins, is appreciated. Reviews of the manuscript by Valerie Behan-Pelletier prior to its being given at the Congress, and especially by Roy Norton in readying it for publication improved its content considerably.

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

TAXONOMY OF NEW ZEALAND PROSTIGMATA: PAST, PRESENT, AND FUTURE

Landcare Research, Private Bag 92170, Auckland, NEW ZEALAND *Present address: Plant Biosecurity, Biosecurity Australia, AFFA, GPO Box 858, Canberra, ACT 2601, AUSTRALIA

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Ting-Kui Qin* and Rosa C. Henderson

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Abstract Taxonomic studies on Prostigmata in New Zealand are reviewed. There was little taxonomic work on this group in the previous century and early this century. Most species have been described since the late 1940s, with a more rapid increase since the 1960s. Comprehensive revisions of Bdellidae, Stigmaeidae, Tenuipalpidae, and Tetranychidae were undertaken in the 1960s and early 1970s. Checklists were compiled by Lamb (1952a) and Spain and Luxton (1971). Monographs were produced on water mites (Cook 1983) and Eriophyoidea (Manson 1984a, b). A catalogue of New Zealand Prostigmata is currently being compiled. A total of 539 species has been reported, placed in 61 families and 219 genera. An additional 149 generic records have been reported without specific identification. The knowledge of many groups is poor or absent and more taxonomic studies are needed for the fauna.

INTRODUCTION Prostigmata is a large and diverse group of mites in terms of number of species and range of habitats. It probably accounts for more than one-third of the mite species reported from New Zealand. General reviews of the acarology and/or its history in New Zealand were provided by Dumbleton (1962), Spain and Luxton (1971), and Manson and Ramsay (1982) who included biographies of the people contributing to New Zealand acarology. The present paper focuses on the past and present taxonomic study of Prostigmata in New Zealand and provides some suggestions and comments on their future study.

PAST Before 1922: pioneering studies

Little work was done on Prostigmata in New Zealand before 1904. Only three species of water mites had been described by then. Chilton (1883) described the first two native Prostigmata, the marine mites Halacarus parvus Chilton (now Agaue parvus)

and H. truncipes Chilton (now Halixodes truncipes) (Halacaridae) from Lyttelton Harbour. Koenike (1900), a German acarologist, described the third water mite Eylais schauinslandi Koenike in the family Eylaidae, from D’Urville Island, Cook Strait. There were apparently no reports of native species in the following 23 years. In addition, a few non-systematic reports were made on introduced pests during this pioneer period. The first published observation of a prostigmatic mite in New Zealand is probably that of Morton (1874) who reported two-spotted mite Tetranychus urticae (Koch) (as a species of Acaridae) on apple, plum and other trees. Kirk (1896a, 1896b, 1897, 1906) reported and prepared leaflets for the eriophyoid mite Phytoptus pyri Pagenstecher (now Eriophyes pyri) and reported Bryobia pratensis Garman (now a junior synonym of Bryobia praetiosa Koch) from apple. Hutton (1904) listed the above three native prostigmatic water mites in his ‘Index Faunae Novae Zealandiae’. In his list of naturalised animals and plants in New Zealand, Thomson (1922) included six species of Prostigmata: 3 Demodex (Demodicidae),

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Ting-Kui Qin et al. Table 1

Number of species, genera, and families of Prostigmata reported in New Zealand based on the published (Lamb 1952a; Spain and Luxton 1971) and unpublished lists.

Year

Species

Genera

Families

1883

2

2

1

Spp. /years

References

1922

9

6

3

7/39 = 0.18/y

Hutton 1904; Thomson 1922

1952

51

30

17

42/30 = 1.4/y

Lamb 1952a

1971

271

124

46

220/19 = 11.6/y

Spain and Luxton 1971

1996

539 +149*

219

61

268/25 = 10.7/y

Qin, unpublised

Chilton 1883

*Identified only to genus

2 Tetranychidae, and 1 Eriophyidae. By 1922, the total number of prostigmatic mites reported from New Zealand was only 9 species belonging to 6 genera and 3 families, including introduced and native species (Table 1). 1923–1952: first checklist phase

This period started with the description of the first native species of terrestrial Prostigmata, Chyzeria novaezealandiae Hirst (Erythraeidae) (Hirst 1924). One or more native species were then added by Hirst (1926) on Erythraeidae, Womersley (1936, 1941) on Cheyletidae, Cryptognathidae, Microtrombidiidae, Pterygosomatidae, Raphignathidae, and Trombiculidae, Dumbleton (1947) on Leeuwenhoekiidae and Trombiculidae, and Lamb (1952b) on Eriophyoidea. This period ended with the publication of Lamb’s (1952a) comprehensive list of New Zealand mites, including introduced and native species. The list included 51 species of Prostigmata, placed in 30 genera and 17 families (Table 1), of which less than half are native species. This represents an increase of 5.7 times for species, 5.0 for genera and 5.7 for families over 30 years (1922–1951). 1952–1971: second checklist phase

Starting from the late 1940s, there were local systematists who devoted their efforts to studying the New Zealand mite fauna. This resulted in a dramatic increase of the number of prostigmatic species reported from New Zealand. The active local acarologists working mainly or partly on Prostigmata were Lamb (1953a, b, c), Ramsay (1958), and Manson (1965) on Eriophyoidea, Stout (1953a, b, 1962), Stout and Viets (1959), Hopkins (1966a, b, 1967, 1969), and Hopkins and Schminke (1970) on water mites (Hydrachnidia), Collyer (1964, 1969a, b) on Tenuipalpidae and Tuckerellidae, Manson (1967a, b, c ,d, 1970) on Tetranychidae, Wood (1964a, 1966, 1967, 1968) on Stigmaeidae, and Spain (1969) on Tydeidae. Overseas acarologists working on the New Zealand fauna included Womersley (1953) on Thyasidae, Atyeo (1960, 1963, 1964) on Bdellidae, Atyeo and Crossley (1961) on Labidostommatidae, Strandtmann (1964) on six families of Prostigmata from Campbell Island, Baker and Pritchard (1956) on Tenuipalpidae, and Mahunka (1970) on Tarsonemoidea. By 1970, 271 species, 124 genera and 46 families of Prostigmata had been reported from New Zealand (Spain and Luxton 1971) (Table 1). This represents an increase of 5.3 times for species, 4.1 for genera, and 2.7 for families in a period of 19 years (1952–1970).

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During this period, Lamb (1960) published a checklist of New Zealand galls mostly caused by eriophyoid mites, Dumbleton (1962) reviewed acarology in New Zealand and provided a supplementary list of species to that of Lamb (1952a), Wood (1964b) added many new familial and generic records to New Zealand Prostigmata, and McMillan (1969) included many prostigmatic mites in an ecological study of the pasture fauna (the mites were identified only to generic rather than specific levels). 1971–Early 1990s: monographs

This period is characterised by the production of monographs and more comprehensive revisions for some groups as well as the addition of more native species of Prostigmata in New Zealand. People contributing to the species increase included Wood (1971a, b, c,1981) on Stigmaeidae, Collyer (1973a, b, c, d) on Tenuipalpidae, Husband (1974, 1990) on Podapolipidae, Nutting et al. (1975) and Desch (1986, 1989) on Demodex, Thewke and Enns (1976) on Cheyletidae, Hopkins (1975), Imamura (1977, 1978, 1979, 1983), Bartsch (1979, 1986a, b, 1995), Cook (1983), Schwoerbel (1984), and Crowell (1988, 1990) on water mites, Martin (1978a) on Siteroptes, Strandtmann (1981) on Penthaleidae, Luxton (1982a, 1984, 1989, 1990) on mites from peat soil and marine litter, Manson (1984a, b) and Manson and Gerson (1986) on Eriophyoidea, Loomis and Goff (1983) and Goff et al. (1988) on Trombiculidae, Lindquist (1986) on Tarsonemidae, Southcott (1988) on larvae of Erythraeidae. Among them, Cook’s (1983) and Manson’s (1984a, b) revisions were produced as monographs. There are also many generic records of Prostigmata in surveys of the fauna of peat soils and pasture (Martin 1978b, 1983; Luxton 1982b, c, d, 1983a, b). Unfortunately this period ended in the reduction to almost no active local acarologists doing taxonomic research on New Zealand Prostigmata.

PRESENT: CATALOGUE The present authors are currently compiling a catalogue of New Zealand Prostigmata and have completed a draft. The catalogue differs from the previous two lists (Lamb 1952a; Spain and Luxton 1971) in that it is more comprehensive and provides more data for each species, including the page numbers on which the species names and figures appear, type specimen deposition information if known, synonyms, type locality, known distributions overseas as well as in New Zealand, host plants, habitats, etc. The information for the catalogue is taken from published literature only and the cut-off date is the end of 1996. About 539 species

TAXONOMY OF NEW ZEALAND PROSTIGMATA: PAST, PRESENT, AND FUTURE

and subspecies of Prostigmata have been recorded from New Zealand, placed in 61 families and 219 genera (Table 1). This represents an increase of almost 2.0 times for species, 1.7 for genera and 1.3 for families in 20 years (1971–1996). An additional 149 generic records have been reported without specific identification (Table 1). In addition, the senior author has begun systematic revisions on some families of New Zealand Prostigmata, and a checklist of Eupodoidea has been published (Qin 1998b). Current systematic revisions include the families Penthaleidae and Penthalodidae (Qin 1998a). To date, there has been only one described species of Penthalodidae reported from mainland New Zealand (Qin 1998a) and all other species from the mainland appear to be new to science. Some work on Tarsonemidae has also been completed (Kim et al. 1998) and more studies are planned.

FUTURE STUDIES Considerable progress has been made in the study of New Zealand Prostigmata. The progress was slow before 1952 (only 0.18 or 1.4 species per year were described from 1883 to 1952, Table 1) but rapid after 1952 (11.6 or 10.7 species per year were described, Table 1). Past studies were mainly on economically important groups such as Tetranychoidea and Eriophyoidea. Moreover, Bdellidae, Stigmaeidae, and water mites (21 families) are relatively well known. Work on some families of Eupodoidea are currently underway. However, the overall knowledge of the native fauna is still poor and information on some groups is completely absent. The currently reported species may represent only a small portion of the actual fauna and more alpha taxonomy is essential for many groups. For example, recent quarantine problems encountered by export of New Zealand commodities suggests that Tarsonemidae and Tydeidae need to be studied urgently. Cladistic systematics and biogeography have not been applied to the study of New Zealand Prostigmata, except for Qin and Halliday (1997) including the New Zealand eupodoids in a cladistic analysis with the Australian species. These methods may be applied to the relatively well known groups.

ACKNOWLEDGEMENTS We are very grateful to our colleagues Graeme Ramsay, Nick Martin, and Trevor Crosby for their comments on the draft manuscript. Funds for this research were provided by the Foundation for Research, Science, and Technology under contract number C09617.

REFERENCES Atyeo, W. T. (1960). A unique species of Thoribdella Grandjean, 1938, from New Zealand (Acarina: Bdellidae). Records of the Dominion Museum, Wellington 3 (4), 289–291. Atyeo, W. T. (1963). The Bdellidae (Acarina) of the Australian realm Part 1. New Zealand, Campbell Island, and the Auckland Islands. Bulletin of the University of Nebraska State Museum 4 (8), 113–166. Atyeo, W. T. (1964). Insects of Campbell Island. Prostigmata. Bdellidae. Pacific Insects Monograph 7, 166–169.

Atyeo, W. T., and Crossley, D. A. (1961). The Labidostomidae of New Zealand (Acarina). Records of the Dominion Museum, Wellington 4(4), 29–48. Baker, E. W., and Pritchard, A. E. (1956). False spider mites of the genus Dolichotetranychus (Acarina: Tenuipalpidae). Hilgardia 24, 357–381. Bartsch, I. (1979). Five new species of Halacaridae (Acari) from New Zealand. New Zealand Journal of Marine and Freshwater Research 3, 175–185. Bartsch, I. (1986a). A new species of Halixodes (Halacaridae, Acari) and a review of the New Zealand species. Journal of the Royal Society of New Zealand 16, 51–56. Bartsch, I. (1986b). New species of Halacaridae (Acari) from New Zealand. New Zealand Journal of Zoology 12, 547–560. Bartsch, I. (1995) Lobohalacarus subterraneus n.sp., a freshwater halacarid (Acari: Halacaridae) from New Zealand. New Zealand Journal of Zoology 22, 209–212. Chilton, C. (1883). On two marine mites. Transactions and Proceedings of the New Zealand Institute 15, 190–192. Collyer, E. (1964). New species of Tenuipalpus (Acarina: Tenuipalpidae) from New Zealand. Acarologia 6, 432–440. Collyer, E. (1969a). Two species of Tuckerella (Acarina: Tuckerellidae) from New Zealand. New Zealand Journal of Science 12, 811–814. Collyer, E. (1969b). A new species of Aegyptobia (Acarina: Tenuipalpidae) from New Zealand. New Zealand Journal of Science 12, 815–816. Collyer, E. (1973a). Two new species of the genus Colopalpus (Acari: Tenuipalpidae). New Zealand Journal of Science 16, 529–532. Collyer, E. (1973b). A new species of the genus Dolichotetranychus (Acari: Tenuipalpidae) from New Zealand. New Zealand Journal of Science 16, 747–749. Collyer, E. (1973c). New species of the genus Tenuipalpus (Acari: Tenuipalpidae) from New Zealand, with a key to the world fauna. New Zealand Journal of Science 16, 915–955. Collyer, E. (1973d). Records of Brevipalpus species (Acari: Tenuipalpidae) from New Zealand and the Pacific area. New Zealand Entomologist 5, 303–304. Cook, D. R. (1983). Rheophilic and hyporheic water mites of New Zealand. Contributions of the American Entomological Institute (Ann Arbor) 21(2), 1-224. Crowell, R. M. (1988). Two unusual water mite symbiotic associations in New Zealand. Internationale Vereinigung für Theoretische und Angewandte Limnologie. Verhandlungen 23, 2035–2037. Crowell, R. M. (1990). Unionicola (Pentatax) billieaehonore n. sp. a sponge-associated Hydracarina (Acari: Unionicolidae) from New Zealand. New Zealand Journal of Zoology 17, 265–269 Desch, C. E. (1986). Demodex aries sp. nov., a sebaceous gland inhabitant of the sheep, Ovis aries, and a redescription of Demodex ovis Hirst, 1919. New Zealand Journal of Zoology 13, 367–375. Desch, C. E. (1989). Two new species of Demodex (Acari: Demodicidae) from the New Zealand short-tailed bat, Mystacina tuberculata Gray, 1843 (Chiroptera: Mystacinidae). New Zealand Journal of Zoology 16, 221–230. Dumbleton, L. J. (1947). Trombidiidae (Acarina) from the Solomon Islands and New Zealand. Transactions and Proceedings of the Royal Society of New Zealand 76, 409–414. Dumbleton, L. J. (1962). Acarology in New Zealand. New Zealand Entomologist 3, 3–8. Goff, M. L., Loomis, R. B., and Ainsworth, R. (1988). Redescription of Neotrombicula naultini (Dumbleton, 1947) and descriptions of two new species of chiggers from New Zealand (Acari: Trombiculidae). New Zealand Journal of Zoology 14, 385–390.

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Ting-Kui Qin et al. Hirst, S. (1924). On three new Acari belonging to the superfamily Trombidioidea (Erythraeidae and Teneriffiolidae). Proceedings of the Zoological Society of London 1924, 1075–1080. Hirst, S. (1926). On some new mites of the suborder Prostigmata (Trembidiodea). Annals and Magazine of Natural History 9(18), 609–616. Hopkins, C. L. (1966a). A new species of Limnesia (Acari, Hydrachnellae) from New Zealand. Transactions of the Royal Society of New Zealand: Zoology 8(1), 1–4. Hopkins, C. L. (1966b). Two species of water-mite (Acari, Hydrachnellae) from New Zealand. Transactions of the Royal Society of New Zealand: Zoology 8(9), 111-117. Hopkins, C. L. (1967). New genera and species of water mites (Acari, Hydrachnellae) from New Zealand. Transactions of the Royal Society of New Zealand: Zoology 10(4), 33-44. Hopkins, C. L. (1969). New species of Limnesia and Tryssaturus (Acari, Hydrachnellae) from New Zealand. Transactions of the Royal Society of New Zealand: Biological Sciences 11(7), 89-92. Hopkins, C. L. (1975). New species of Hygrobatidae and Lebertiidae (Acari: Hydrachnellae) from New Zealand. Journal of the Royal Society of New Zealand 5(1), 5–11. Hopkins, C. L., and Schminke, H. K. (1970). A species of Euwandesia (Acari: Hydrachnellae) from New Zealand. Acarologia 12, 357–359. Husband, R. W. (1974). Lectotype designation for Locustacarus trachealis Ewing and a new species of Locustacarus (Acarina: Podapolipidae) from New Zealand. Proceedings of the Entomological Society of Washington 76, 52–59. Husband, R. W. (1990). New species of Podapolipoides (Acari : Podapolipidae), ectoparasites of grasshoppers (Orthoptera : Acrididae) in Australia and New Zealand, with keys to world species. Annals of the Entomological Society of America 83, 371–393. Hutton, F. W. (1904). ‘Index Faunae Novae Zealandiae.’ (Dulau and Co., London.) Imamura, T. (1977). Two new water-mites (Acari- Hydrachnellae) from cave waters of New Zealand. Journal of the Speleological Society of Japan 2, 9–12. Imamura, T. (1978). A new subgenus and species of troglobiontic water-mite from New Zealand. Journal of the Speleological Society of Japan 3, 41–43. Imamura, T. (1979). One more new subgenus and a new species of troglobiontic water-mite from New Zealand. Journal of the Speleological Society of Japan 4, 27–30. Imamura, T. (1983). A new subfamily and two new species of water mite (Acari : Hydrachnellae) from Papua New Guinea. Proceedings of the Japanese Society of Systematic Zoology 26, 11–18. Kim, J. S., Qin, T. K., and Lindquist, E. E. (1998). Description of Tarsonemus parawaitei, a new species of Tarsonemidae (Acari: Heterostigmata) associated with orchard and ornamental plants in Europe, Australia and New Zealand. Systematic and Applied Acarology Special Publications 2, 1–28. Kirk, T. W. (1896a). Appendix 4 - Division of biology and pomology. Report. Department of Agriculture, New Zealand 1896, 116–177. Kirk, T. W. (1896b). Division of biology and pomology. Report of the biologist. Department of Agriculture, New Zealand 1896, 1–39. Kirk, T. W. (1897). Pear-mite (Phytopus pyri). New Zealand Department of Agriculture leaflets for gardeners and fruitgrowers 19, 1–2. Kirk, T. W. (1906). Spraying. Report. Department of Agriculture, New Zealand 1906, 454–456. Koenike, F. (1900). Ein Acarinen- insbesondere Hydracarinen-system nebst hydracarinologischen Berichtigungen. Abhandlungen herausgegeben vom Naturwissenschaftlichen Verein zu Bremen 20, 121–164.

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Lamb, K. P. (1952a). A preliminary list of New Zealand Acarina. Transactions and Proceedings of the Royal Society of New Zealand 79, 370–375. Lamb, K. P. (1952b). New plant galls: 1 - mite and insect galls. Transactions and Proceedings of the Royal Society of New Zealand 79, 349–362. Lamb, K. P. (1953a). A revision of the gall-mites (Acarina: Eriophyidae) occurring on tomato (Lycopersicum esculentum Mill.), with a key to the Eriophyidae recorded from solanaceous plants. Bulletin of Entomological Research 44, 343–350. Lamb, K. P. (1953b). A new species of Diptilomiopus nalepa (Acarina: Eriophyidae) together with a key to the genus. Transactions and Proceedings of the Royal Society of New Zealand 80, 367–370. Lamb, K. P. (1953c). New plant galls. 2 - Description of seven new species of gall-mites and the galls which they cause. Transactions and Proceedings of the Royal Society of New Zealand 80, 371–382. Lamb, K. P. (1960). A check-list of New Zealand plant galls (Zoocecidia). Transactions and Proceedings of the Royal Society of New Zealand 88, 121–139. Lindquist, E. E. (1986). The world genera of Tarsonemidae (Acari : Heterostigmata) : A morphological, phylogenetic, and systematic revision, with a reclassification of family-group taxa in the Heterostigmata. Memoirs of the Entomological Society of Canada 136, 1–517. Loomis, R. B. , and Goff, M. L. (1983). A new species of Guntheria (Acari: Trombiculidae) from New Zealand. Journal of Medical Entomology 20, 87–89. Luxton, M. (1982a). Some new species of mites from New Zealand peat soils. New Zealand Journal of Zoology 9, 325–332. Luxton, M. (1982b). Studies on the invertebrate fauna of New Zealand peat soils. 1. General survey of the sites. Revue d’Ecologie et de Biologie du Sol 19, 535–552. Luxton, M. (1982c). Studies on the invertebrate fauna of New Zealand peat soils. 2. Restiad peats. Revue d’Ecologie et de Biologie du Sol 19, 553–578. Luxton, M.(1982d). Studies on the invertebrate fauna of New Zealand peat soils. 4. Pasture soils on Rukuhia peat. Pedobiologia 24, 297–308. Luxton, M. (1983a). Studies on the invertebrate fauna of New Zealand peat soils. 3. - Fern peats. Revue d’Ecologie et de Biologie du Sol 20, 87–109. Luxton, M. (1983b). Studies on the invertebrate fauna of New Zealand peat soils. 5. Pasture soils on Kaipaki peat. Pedobiologia 25, 135–148. Luxton, M. (1984). More marine littoral mites (Acari) from New Zealand. New Zealand Journal of Marine and Freshwater Research 18, 291–304. Luxton, M. (1989). New taxa of intertidal mites (Acari). Journal of Natural History 23, 407–428. Luxton, M. (1990). The marine littoral mites of the New Zealand region. Journal of the Royal Society of New Zealand 20, 367–418. Mahunka, S. (1970). New species of pygmephorid and scutacarid mites (Acari: Tarsonemini) from New Zealand. Transactions of the Royal Society of New Zealand: Biological Sciences 12(8), 69–72. Manson, D. C. M. (1965). Three new species of gall-mites (Acarina: Eriophyidae). Transactions of the Royal Society of New Zealand: Zoology 6(14), 133–139. Manson, D. C. M. (1967a). The spider mite family Tetranychidae in New Zealand 1. The genus Bryobia. Acarologia 9, 76–123. Manson, D. C. M. (1967b). The spider mite family Tetranychidae in New Zealand 2. The genus Tetranychus. Acarologia 9, 581–597. Manson, D. C. M. (1967c). The spider mite family Tetranychidae in New Zealand 3. The genus Schizotetranychus. Acarologia 9, 823–840.

TAXONOMY OF NEW ZEALAND PROSTIGMATA: PAST, PRESENT, AND FUTURE

Manson, D. C. M. (1967d). The spider mite family Tetranychidae in New Zealand. 4. Two new species of Tetranychus and a revised key to the genus. New Zealand Journal of Science (Wellington) 10, 1083–1091.

Stout, V. M. (1953a) New species of Hydracarina, with a description of the life history of two. Transactions of the Royal Society of New Zealand 81, 417–466.

Manson, D. C. M. (1970). The spider mite family Tetranychidae in New Zealand. 5- Tetranychus (Tetranychus) moutensis a new species of spider mite from flax (Phormium tenax Forst.). New Zealand Journal of Science 13, 323–327.

Stout, V. M. (1953b). Eylais waikawae n. sp. (Hydracarina) and some features of its life-history and anatomy. Transactions of the Royal Society of New Zealand 81, 389–416.

Manson, D. C. M. (1984a). Eriophyinae (Arachnida: Acari: Eriophyoidea). Fauna of New Zealand 5, 1–123.

Stout, V. M. (1962). Fresh water and marine mites. New Zealand Entomologist 3, 12–14.

Manson, D. C. M. (1984b). Eriophyoidea except Eriophyinae (Arachnida: Acari). Fauna of New Zealand 4, 1–142.

Stout, V. M., and Viets, K. (1959). Ueber eine parasitisch lebende Halacaride (Acari) von Neuseeland. Veroeffentlichungen des Instituts für Meeresforschung in Bremerhaven 6, 203–212.

Manson, D. C. M., and Gerson, U. (1986). Eriophyid mites associated with New Zealand ferns. New Zealand Journal of Zoology 13, 117–129.

Strandtmann, R. W. (1964). Insects of Campbell Island. Prostigmata: Eupodidae, Penthalodidae, Rhagidiidae, Nanorchestidae, Tydeidae, Ereynetidae. Pacific Insects Monograph 7, 148–165.

Manson, D. C. M., and Ramsay, G. W. (1982). New Zealand. In ‘History of Acarology’. (Ed V. Prasad.) pp. 349–363. (Indira Publishing: Oak Park, Michigan.)

Strandtmann, R. W. (1981). A new genus and species of penthaleid mite (Acarina: Penthaleidae) from New Zealand. Pacific Insects 23, 392–395.

Martin, N. A. (1978a). Siteroptes (Siteroptoides) species with pediculaster-like phoretomorphs (Acari: Tarsonemida: Pygmephoridae) from New Zealand and Polynesia. New Zealand Journal of Zoology 5, 121–155.

Thewke, S. E., and Enns, W. R. (1976). Oudemansicheyla coprosomae sp. nov. (Acarina: Cheyletidae) from New Zealand. Journal of the Kansas Entomological Society 49, 360–363.

Martin, N. A. (1978b). Effect of four insecticides on the pasture ecosystem. 6. Arthropoda dry heat-extracted from small soil cores and conclusions. New Zealand Journal of Agricultural Research 21, 307–319.

Thomson, G. M. (1922). ‘The Naturalisation of Animals and Plants in New Zealand.’ (Cambridge University Press: Cambridge.) Womersley, H. (1936). Additions to the trombidiid and erythraeid acarine fauna of Australia and New Zealand. Journal of the Linnean Society of London, Zoology 40(269), 107–121.

Martin, N. A. (1983). Miscellaneous observations on a pasture fauna: an annotated species List. New Zealand Department of Scientific and Industrial Research, Entomology Division, Report 3, 1–98.

Womersley, H. (1941). New species of Geckobia (Acarina, Pterygosomidae) from Australia and New Zealand. Transactions of the Royal Society of South Australia 65, 323–328.

McMillan, J. H. (1969). The ecology of the acarine and collembolan fauna of two New Zealand pastures. Pedobiologia 9, 372–404.

Womersley, H. (1953). An interesting new larval species of Panisopsis (Thyasidae, Acarina) from New Zealand. Records of the Canterbury Museum 6, 233–235.

Morton, J. (1874). Notice of the occurrence of a red spider among the fruit trees in the south, and the disappearance of the blight. Transactions and Proceedings of the New Zealand Institute 6, 380–381. Nutting, W. B., Kettle, P. R., and Tenquist, J. (1975). Hair follicle mites (Demodex spp. ) in New Zealand. New Zealand Journal of Zoology 2, 219–222. Qin, T. K. (1998a). Callipenthalodes, a new genus of Penthalodidae (Acariformes: Eupodoidea) from New Zealand. International Journal of Acarology 24, 221–225. Qin, T. K. (1998b). A checklist and key to species of Eupodoidea (Acari: Prostigmata) from Australia and New Zealand, and their subantarctic islands. Journal of the Royal Society of New Zealand 28, 295–307. Qin, T. K., and Halliday, R. B. (1997). Eriorhynchidae, a new family of Prostigmata, with a cladistic analysis of eupodoid species of Australia and New Zealand. Systematic Entomology 22, 151–171. Ramsay, G. W. (1958). A new species of gall-mite (Acarina: Eriophyidae) and an account of its life cycle. Transactions of the Royal Society of New Zealand 85, 459–464. Schwoerbel, J. (1984). Subterrane Wassermilben aus Fliessgewässern Neuseelands (Acari, Actinedida). Archiv für Hydrobiologie Supplementband 66, 293–308 Southcott, R. V. (1988). Two new larval Erythraeinae (Acarina : Erythraeidae) from New Zealand, and the larval Erythraeinae revised. New Zealand Journal of Zoology 15, 223–233. Spain, A. V. (1969). A new genus and species of Tydeidae (Acari: Prostigmata) from New Zealand. Acarologia 11, 23–28. Spain, A. V., and Luxton, M. (1971). Catalogue and bibliography of New Zealand Acari. Pacific Insects Monograph 25, 179–226.

Wood, T. G. (1964a). A new genus of Stigmaeidae (Acarina, Prostigmata) from New Zealand. New Zealand Journal of Science 7, 579–584. Wood, T. G. (1964b). New records of terrestrial Prostigmata from New Zealand. New Zealand Entomologist 3(3), 39–40. Wood, T. G. (1966). Mites of the genus Ledermuelleria Oudms. (Prostigmata, Stigmaeidae) from New Zealand, with records of one species from some southern Pacific Islands. New Zealand Journal of Science 9(1), 84–102. Wood, T. G. (1967). New Zealand mites of the family Stigmaeidae (Acari: Prostigmata). Transactions of the Royal Society of New Zealand: Zoology 9(9), 93–139. Wood, T. G. (1968). A new species of Cheylostigmaeus Willman (Acari: Stigmaeidae) from New Zealand. New Zealand Journal of Science 11, 276–279. Wood, T. G. (1971a). New species and records of Stigmaeidae (Acari: Prostigmata) from New Zealand. 1. Mediolata G. Canestrini and Mecognatha Wood. New Zealand Journal of Science 14, 54–61. Wood, T. G. (1971b). New species and records of Stigmaeidae (Acari: Prostigmata) from New Zealand. 2. The genera Apostigmaeus Grandjean, Summersiella Gonzalez, Pseudostigmaeus (Wood) and Eryngiopus (Summers). New Zealand Journal of Science 14, 406–418. Wood, T. G. (1971c). Stigmaeidae from Campbell Island (Acari: Prostemata). Acarologia 12, 677–683. Wood, T. G. (1981). New species and records of Stigmaeidae (Acari: Prostigmata) from New Zealand - 3. Genus Stigmaeus Koch. New Zealand Journal of Zoology 8, 369–377.

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ACAROLOGY: PROCEEDINGS OF THE 10TH INTERNATIONAL CONGRESS

ACARINE SYSTEMATICS AND PHYLOGENY

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

THE BODY SEGMENTATION OF ORIBATID MITES FROM A PHYLOGENETIC PERSPECTIVE

Institute of Biology, Lab. Soil Zoology and Ecology, Free University Berlin, Grunewaldstr. 34, D-12165 Berlin, Germany. E-mail: [email protected]

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Gerd Weigmann

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Abstract Within the Oribatida both very compact, nearly unsegmented forms and multiply-segmented forms can be observed, making it difficult to identify the most basic body divisions and segmentation. Moreover the basic segmentation type for Acariformes or for mites in general is still unclear. This paper discusses the alternative opinions of van der Hammen (since 1963), which are based on speculative comparative morphology of the Arachnida. The idea of a basic body plan of Acariformes with up to 17 segments is rejected and the older schemes of Grandjean (since 1934) appear to be more realistic. The different segmentation patterns within the Enarthronota are discussed and compared with Palaeosomata and other oribatid taxa, against a background of recent phylogenetic analyses. The most probable plesiomorphic hysterosoma in the early Oribatida is a type without segmental notogastral plates but with segmental setation. Basic Enarthronota had some erectile macrosetae on individual sclerites, found in some derived forms as intercalary setae e and f between plates. Nearly homonomous notogastral plates, as observable in Brachychthonioidea and in Haplochthoniidae, are probably secondary constructions.

1. INTRODUCTION Opinions in the acarological literature on the divisions of the oribatid body and on the evolution of notogastal segmentation in Enarthronota have changed from Grandjean (1934) to those of recent authors. In this paper I review this subject against the background of modern phylogenetic research as used in recent papers. A discussion from a phylogenetic and ontogenetic point of view should contribute to solving the issue of Oribatida monophyly.

SECTIONS OF THE ORIBATID BODY The first fundamental body design of Grandjean (1934) regarded the idiosoma of adult Oribatida as being composed of the segments 3–12, in addition to two gnathosomal segments, each characterised by a transverse row of setae. The 3rd and 4th segments represented the prodorsum and the propodosomal segments, the

12th being the anal segment. In 1963 van der Hammen initiated a discussion on the basic segmentation in Acariformes (= Actinotrichida) in the light of comparative arachnological morphology (see also van der Hammen 1989). He postulated 17 body segments from the cheliceral to the peranal segment. Grandjean (1970) modified van der Hammen’s interpretations without presenting arguments, and postulated that the tergites of the podosoma should have disappeared and that the prodorsum represents the gnathosomal tergites (‘aspidosomà’ in Grandjean 1970). In that interpretation the anterior part of the hysterosoma represents the 7th segment (joined with 8th and 9th; see section 3.2), as figured by Coineau (1974). But this hypothesis, which was adopted by other authors (Balogh and Mahunka 1983; Evans 1992; Travé et al. 1996; Alberti and Coons 1999), is not supported by good arguments. There are no serious indications of such an overgrowth of the dorsal podosoma by gnathosomal tergites from the

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Figure 1

Body divisions of an oribatid mite

front, or by opisthosomal tergites from the terminal region, neither in acariform mites generally, nor in Oribatida in particular. Furthermore, there are no reliable observations in embryology which might support these ideas. With detailed observations and arguments alternative designs should be considered. Following Grandjean (1970), the loss of podosomal tergites would raise some questions. Assertion (1): If the segments of the propodosoma have been overgrown by the gnathosomal tergites during the ontogenetical process, we should then expect to find that the central parts of the tergites have been extended backwards more than the lateral parts, which should remain in contact with the ventral parts of the gnathosomal segments. As a result, the lateral setae (exa - exp) of the two transverse segmental rows of setae on the prodorsal shield should have remained more anterior than the central setae (le, ro - sensillus, in), near the chelicerae and pedipalps. Assertion (2): Similarly, the median setae of hysterosomal segments C and D should be positioned more anteriorly than the lateral setae, if the metapodosoma had been overgrown by opisthosomal tergites. Yet, morphological findings seem to contradict the obove mentioned suppositions. Argument 1: In reality, the transverse rows of setae on tergite B (in the early terminology of Grandjean 1934, being ‘leg-II-segment’), segment C (‘leg-III-segment’), and also often segments D and E, are parallel to each other and to the dorsosejugal suture (figs 2B, C). This lends support to the hypothesis that tergites B and C developed ontogenetically adjacent to each other rather than having ‘shifted’ together secondarily. Argument 2: In contrast, the central setae (le, ro: fig 2B, C) of the anterior prodorsal segment tend to be more anteriorly placed when nearer to the median line of the prodorsum as compared with the lateral seta exa of the same segment (in contrast to the above mentioned assertion 1, according to Grandjean 1970).

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Thus, another hypothesis seems the more plausible, i.e. that the gnathosoma has been overgrown by the tergite of the first podosomal segment, which has become a rostral tectum (arrowed in fig. 2B). This process is an allometrical overgrowth, more median than lateral, causing the frontal position of ro, while exa remained at the primary posterior position. Argument 3: It is characteristic of Palaeosomata that the centrodorsal setae of segments C and D are positioned backwards while the laterodorsal setae (c3, d3) are more frontal. This contradicts the proposals of Grandjean (1970) as discussed in Assertion 2. Argument 4: On the hysterosomal tergites H and P of many taxa, the central setae (h1, p1) can be observed in a more terminal position than the lateral setae (h2, h3 - p2, p3, p4: fig. 2B, C). I assume that the segments AN and AD have ‘tilted’ down thereby changing its position from terminal to ventral. This ontogenetic process has resulted in a more terminal position of the central area of the segments H and P, as indicated by the corresponding position of the central setae. This indirectly supports other analogous arguments concerning oblique transversal rows of segmental setae. Thus assertions 1 and 2 are less probable than arguments 1–4, which are clearly more acceptable. Therefore we should return to the first scheme of body divisions as published by Grandjean (1934). In absence of desirable embryological investigations, this seems the most likely explanation at moment: (1) The gnathosoma of oribatid mites lacks any dorsal plates, but is covered dorsally by the prodorsum; (2) The prodorsum represents the tergites of propodosomal segments; (3) Dorsally the hysterosoma is composed of metapodosomal and opisthosomal tergites; (4) the anal segment is the 12th body segment (figs 1 and 2). In this hypothesis the sejugal line marks the border between the proterosoma and hysterosoma (fig. 1). The anterior border of the dorsal opisthosoma is marked by the scissure between plates

THE BODY SEGMENTATION

Figure 2

OF ORIBATID MITES FROM A PHYLOGENETIC PERSPECTIVE

A: Hypothetical archetype of an acariform mite; B: Hypothetical archetype of an oribatid mite; C: Scheme of a holonotic oribatid mite (Holonota after Haumann)

D and E in Enarthronota, or by setal rows d and e, respectively. The abjugal suture of Grandjean (1970) is the border of the prodorsal plate, which is developed secondarily, as is the disjugal suture in regard to the development of the notogastral plate. Fig. 2A demonstrates a probable hypothetical archetype of Acariformes. The precheliceral part is not regarded as a metamere (the ‘acron’ of the Articulata scheme); it might be the preformation of the acarine naso (N in fig. 2A). A primitive ancestor of oribatid mites might lack dorsal notogastral plates on the hysterosomal segments (fig. 2B) and might have nearly homonomous segmental setation (see below). It might also lead directly to a derived non-segmented form of holonotic oribatid mite (fig. 2C).

SEGMENTATION OF THE ORIBATID NOTOGASTER Within the primitive Oribatida a range of notogastral segmentation exists, from a holonotic notogaster without any scissures (Holonota sensu Haumann 1991) to 2–5 segmental plates, the latter mostly found within the Enarthronota (Grandjean 1946). Another extreme morphological type is present in some Palaeosomata and in some juvenile stages of different taxa, which have a hysterosoma without segmental plates, but with individual sclerites each bearing a seta, or no plates at all, if the notogastral setae are inserted in the unsclerotised integument. Which type of notogaster is the most plesiomorphic? We might answer this question by discussing patterns of notogastral morphology and setation against a background of recent phylogenetic analyses of the most

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Gerd Weigmann

primitive groups of oribatid mites and their ancestors, and of Enarthronota. Notogastral segmentation of Endeostigmata and Palaeosomata

Following Norton et al. (1993) the Oribatida are derived from the ‘Endeostigmata’, probably from a branch including Terpnacaridae and Alicorhagiidae, which lack notogastral plates but which show the same dorsal chaetotaxy as do primitive Oribatida (Kethley 1990). The Palaeosomata Grandjean (1969) most probably belong to the Oribatida (Haumann 1991; Norton et al. 1993), and they represent the most basic taxon. All other Oribatida belong to the sistergroup Monofemorata Haumann (1991). In some Palaeosomata the notogastral setae are inserted on individual plates, or two setae are inserted together on one plate (e.g. in Archeonothridae Grandjean 1954). In other taxa there are larger anterior or pygidial plates with multiple pairs of setae (e.g. in Palaeacaridae Grandjean 1932 and Ctenacaridae Grandjean 1954). Some taxa have free plates without setae. A segmental pattern of plates and/or setal rows is difficult to observe. The homology of some setae is uncertain or problematic, and there is even a setal hypertrichy on the posterior notogastral region in some taxa. Consequently, we cannot reconstruct a plesiomorphic pattern of notogastal plates for all other Oribatida (Monofemorata) from the morphology of Palaeosomata. Some Palaeosomata show obvious large setae, which are erectile and inserted on sclerites. These setae are very similar to setae in some Enarthronota (see below). Notogastral segmentation of Enarthronota

The Enarthronota of Grandjean are characterised by a prodorsal shield and the presence of one or more scissures in the sclerotised notogaster in adults; they normally show 16 pairs of notogastral setae. The Enarthronota sensu Haumann (1991), as used in the following discussion, are a monophyletic group. Two taxa with a similar notogastral scissure – Parhypochthonioidea Grandjean 1932 and Elliptochthonius profundus Norton 1975 – do not belong to Enarthronota. The Enarthronota can be divided into two well defined superfamilies, Hypochthonioidea and Protoplophoroidea (= Cosmochthonioidea) (Grandjean 1969; Norton 1984; Haumann 1991), and some additional smaller taxa. One of these additional families is Brachychthoniidae, whose relationship to the other cladistic branches is uncertain (Haumann 1991). The cladogram in fig. 3 follows the phylogenetic analysis of Haumann (1991) in contrast to some typological systematics (Balogh and Mahunka 1983). The notogastral segmentation with plates and setae is presented in fig. 3 in a diagrammatic manner for important genera of Enarthronota. Heterochthonius Berlese 1910 (Heterochthoniidae) and Nipponiella Gordeeva 1980 are somewhat related to Hypochthonioidea. An important question is that of the most plesiomorphic pattern of ‘segmental’ plates separated more or less completely by ‘intersegmental’ scissures (the quotation-marks indicate the hypothetical status of these structures being truly segmental). At the base of fig. 3 are two possible hypothetical patterns as they have been discussed in literature. Pattern (b) is more or less homonomous in regard to plates and setation. It shows 6 notogastral plates with the full set of 16 pairs of notogastral setae (two pairs e- and

46

f-setae each on segments E and F; segments C, D, H and P with three pairs each). Pattern (b) could be favoured by the observation that homonomous segmental structures occur more often in basal forms of different groups of Arthropoda, in contrast to more differentiated and specialised structures on various segments in derived forms. A pattern like this has been considered to be the most primitive in Oribatida (Grandjean 1946). The alternative pattern (a) shows specialisations which can be observed in different phylogenetic branches of Oribatida together with a more or less segmented notogaster. The specialisations are (1) erectile macrosetae on individual sclerites, mostly observable in setae e and f (in Heterochthonius and Nipponiella, and others – in branch A with ‘Hypochthonioidea et al.’ in fig. 3 –; in Cosmochthonius, and others – in branch B with Protoplophoroidea in fig. 3 –; also in a similar manner in some Palaeosomata!), and (2), a more or less complete fusion of plates C and D (Brachychthoniidae, Protoplophoridae, Hypochthonioidea). The argument is based partly on the position of seta ,,cp“ (sensu Grandjean 1946) posterior from seta c3; this seta is most probably seta d3. If this is correct, in those taxa with seta cp the plate ,,C“ is not restricted to segment C. The synonymy of seta cp with seta d3 (in the sense of Grandjean 1934) is not a common opinion. This seta ,,cp“ is found in different Oribatida (exclusively in Enarthronota ?) in a medio-lateral position between setal row c and d instead of a third seta in the d-row in the most lateral position. Setae cp and d3 are never observed together in the same specimen or species. The notation cp indicates a more or less unspoken hypothesis of another segment between C and D in an ancestor. Van der Hammen (1963) states explicitly, that ‘the dorsal part of the anterior ‘metamere’ C is in fact a fusion of the segments VIIIX, of which VII is probably reduced’ (cf. scheme of Coineau 1974). But there is no evidence for the existence of such an additional hypothetical segment, and it is not found in the endeostigmatid ancestors of the Oribatida. It is postulated that both rows c and d each have three pairs of setae, and this may be the plesiomorphic pattern in most dorsal segments of early Oribatida ancestors (fig. 2). It is possible that the anterior position of seta d3 evolved before the evolution of quasi-segmental plates C and D (discussion see below) or after the fusion of plates C and D in the Enarthronota. If the second hypothesis is correct this pattern (a) should not have evolved basally in Enarthronota but only basally in branch B of the Protoplophoroidea complex, where all members show an anterior position of seta d3 . But not all members of branch B in fig. 3 have fused plates C+D. If we do not postulate a secondary plate separation of C+D in those cases we must accept plate formation in the region of segments C and D after the migration of seta d3 as an apomorphous character of branch B within the Enarthronota. Such an anterior position of seta d3 can also be observed in the Brachychthonioidea. This supports the origin of Brachychthonioidea from branch B and not from the common ancestor of branches A and B, as was indicated by Haumann (1991). The quasi-segmental lateral plates in Brachychthoniidae are not found in any other group. It is possible that these plates have no real segmental origin but instead mark the beginning of a lateral sclerotisation process, as it is found in juvenile stages of diverse Oribatida (plates without setae in positions

THE BODY SEGMENTATION

OF ORIBATID MITES FROM A PHYLOGENETIC PERSPECTIVE

Hypochthonioidea Mesoplophora C

Eniochthonius adult

larval

Nipponiella

C

C

D

D

D

E

E

E

E

F

F

F

F

H P

H P

H P

H P

D

E

Heterochthonius

C

C

D

Hypochthonius Malacoangelia

Brachychthonioidea

Protoplophoroidea Haploch-

Cosmoch-

thonius

thonius

Sphaerochthonius adult

Protoplo-

Brachych-

phora

thonius

larval

C

C

C

C

C

D

D

D

D

D

E F H P

E

E

E

F H P

F H P

F H P

E F H P

? ? C D E F H P

C D E F H P

a) Figure 3

individual sclerite with erectile seta normal seta

b)

Notogastral segmentation of main taxa of Enarthronota

47

Gerd Weigmann

where adults have united notogasters). In this respect the incomplete sclerotisation in the ontogeny of Brachychthoniidae with reduced body sizes might indicate neoteny. In Palaeosomata seta d3 is in a latero-anterior position, but in most species the three d-setae form an oblique row from centroposterior (d1) to latero-anterior (d3) position, as can be found for e-setae (Grandjean 1954). The anterior position of d3 in Heterochthonius (branch A, see fig. 3) might be convergent and is not comparable with that in Protoplophoroidea, because of the special construction of transverse ridges with setae c and d and because of the lack of real plates (perhaps another example of neoteny). In regard to the ‘erectile setae e and f on individual sclerites’ the hypothesis of basic plesiomorphy in Enarthronota (a possible apomorphy of all Oribatida: see Haumann 1991) has been established by for example, Norton (1984) and Haumann (1991). In Palaeosomata the erectile macrosetae are not restricted to e- and f-setae (cf. Palaeacarus, Acaronychus: Grandjean 1954), but in Enarthronota this seems to be a basal plesiomorphy. This evidence favours hypothesis (a) being the most plesiomorphic within the Enarthronota (see fig. 3). The argument follows the principle of parsimony, which postulates that plesiomorphic homology of special characters is more probable than independant apomorphic convergence in several unrelated taxa. Thus, the partial presence of segmented notogasters and intercalary individual sclerites with erectile setae e and f in both main lineages of Enarthronota, branches A and B in fig. 3, is too complex to be convergent. The presence of similar erectile macrosetae in Palaeosomata supports this interpretation. One important consequence of this idea is the postulation of secondarily evolved homonomous plates in different lineages of Enarthronota, derived from forms with heteromorphous segments. This concept has been elaborated by Norton (1984) and Haumann (1991) extensively, substantiated by phylogenetic analyses. In Hypochthonioidea as well as in Protoplophoroidea, higher taxa with homonomous plates and setations are phylogenetically related to families with intercalary sclerites and erectile setae. The most convincing example is Haplochthoniidae and Cosmochthoniidae, which have many synapomorphies (e.g. Haumann 1991). But there are different patterns of notogastral plates in those Enarthronota which show nearly homonomous rows of setae (see fig. 3), for example Haplochthoniidae with three scissures and four plates, and Brachychthoniidae with two scissures and three plates. Adult and larval Eniochthoniidae have notogasters with one transverse scissure separating two composite plates, but the scissures in each are at different intersegmental positions. In larvae of Eniochthonius plates C and D are fused totally, and plate E is fused with plate F+H, but with a visible border; in adults plate E is fused with plate C+D with a visible border, and setae h2 and h3 are located on a special lateral plate (plate Q in Norton 1984, cf. Grandjean 1934; see fig. 3). We can assume that the morphogenetical process of plate building is quite different in diverse taxa as it is even in different stages of the same species.

48

In other taxa some setae have an intercalary position, but they are not erectile, e.g. in Sphaerochthonius (larva and adult with quite different notogaster segmentation), in Protoplophoridae and Hypochthoniidae (see fig. 3). In the latter the intercalary setae e are inserted on a special transverse intercalary sclerite, and the setae are minute or vestigial. In some cases the setae of a segment are inserted at the anterior border of the adjoined plate (e.g. setae d in Sphaerochthonius) or at the posterior border (e.g. setae e in larval Sphaerochthonius, e and f in Protoplophora). These quite different plate constructions and setal positions lead to the hypothesis that plates can be built in different independent ways, ontogenetically and phylogenetically. Knülle (1957) considered that the notogastral plates in derived Enarthronota are apomorphic; he stated that the phylogenetically secondary process of notogastral sclerotisation seems to follow the primary segmentation. The results of Norton (1984) and Haumann (1991) support this interpretation. We come to the conclusion that the notogastral plates in Enarthronota are secondary pseudosegmental structures. In the case of taxa with a seta d3 in an anterior position on a plate C it seems to be plausible that the first notogastral plate joins all setae near the anterior border of the notogaster regardless of their segmental origin. In some cases the plates are built between the setal rows in others around the setae. It cannot be determined whether non-erectile intercalary setae are derived from erectile setae. The hypothesis of secondary plate development in Enarthronota is consistent with the observation that some Palaeosomata lack segmental plates, and larvae of many taxa of lower and higher Oribatida lack any notogastral plate or show individual plates around setae. Palaeosomata and juvenile stages of Enarthronota might possess a plesiomorphic type of notogaster. As an example we have a plate-free notogaster in Haplochthonius larvae, the adults have 4 pseudosegmental plates. It is not difficult to imagine that the plates in the nymphs and adults are developed secondarily, without phylogenetic preformation.

NOTOGASTRAL SEGMENTATION OF PARHYPOCHTHONIOIDEA AND ELLIPTOCHTHONIUS Following the cladistic analysis of Haumann (1991), the genera Parhypochthonius Berlese 1904, Gehypochthonius Jacot 1936 (Parhypochthonioidea) and Elliptochthonius Norton 1975 do not belong to Enarthronota, but are basal members of Novoribatida Haumann (a sistergroup of the Enarthronota). Elliptochthonius is not closely related to the other genera mentioned. They have in common a single transverse notogastral scissure behind setal row d. This scissure marks the anterior border of the opisthosoma, as stated in section 2. Elliptochthonius also has a scissure on the ventral side. But as suggested for Enarthronota, this notogastral segmentation might be secondary. Parhypochthonius looks somewhat neotenic; its characters might not be comparable with adults of other taxa. In Oribatida without notogastral segmentation (Holonota of Haumann) it is difficult to decide whether the notogaster as one plate is developed by conjunction of segmental plates or is composed primarily as a unit. The very different patterns of notogastral sclerites or the lack of any plates in various lower and higher Oribatida support the latter hypothesis.

THE BODY SEGMENTATION

REFERENCES Alberti, G., and Coons, L. B. (1999). Acari: Mites. In ’Microscopic Anatomy of Invertebrates, vol. 8C, Chelicerate Arthropoda, chapter 6’ (Ed. F. W. Harrison.) pp. 515–1215. (Wiley-Liss: New York.) Norton, R. A. (1984). Monophyletic groups in the Enarthronota (Sarcoptiformes). In ‘Acarology 6, vol. 1.’ (Eds D. A. Griffiths and C. E. Bowman.) pp. 233–240. (Ellis Horwood Ltd.: Chichester.) Balogh, J., and Mahunka, S. (1983). ‘Primitive Oribatids of the Palaearctic region. The soil mites of the world. vol. 1’ (Elsevier: Amsterdam.) Coineau, Y. (1974). Éléments pour une Monographie morphologique, écologique et biologique des Caeculidae. Mémoires Muséum national d’Histoire naturelle, nouvelle série, série A, Zoologie, 81, 1–299. Evans, G. O. (1992). ‘Principles of Acarology.’ (CAB International: Wallingford.) Grandjean, F. (1934). La notation des poils gastronotiques et des poils dorsaux du Propodosoma chez les oribates (Acariens). Bulletin Societé zoologique France 59, 12–44. Grandjean, F. (1946). Les Enarthronota (Acariens), première serie. Annales Science Naturelle Zoologique (11. Ser.) 8, 213–248. Grandjean, F. (1954). Étude sur les Palaeacaroides (Acariens, Oribates). Mémoires Muséum national Histoire naturelle, Zoologie 7, 179–274. Grandjean, F. (1969). Considérations sur le classement des oribates. Leur division en 6 groupes majeurs. Acarologia 11, 127–153. Grandjean, F. (1970). Stases. Actinopiline. Rappel de ma classification des acariens en 3 groupes majeurs. Terminologie en soma. Acarologia 11, 796–827.

OF ORIBATID MITES FROM A PHYLOGENETIC PERSPECTIVE

Hammen, L. van der (1963). The addition of segments during the postembryonic ontogenesis of the Actinotrichida (Acarida) and its importance for the recognition of the primary subdivision of the body and the original segmentation. Acarologia 5, 443–454. Hammen, L. van der (1989). ‘An Introduction to Comparative Arachnology.’ (SPB Acad.Publ.: The Hague.) Haumann, G. (1991). ‘Zur Phylogenie primitiver Oribatiden (Acari: Oribatida).’ (dbv-Verlag Technische Universität: Graz.) Kethley, J. (1990). Acarina: Prostigmata (Actinedida). In ‘Soil Biology Guide’ (Ed D. L. Dindal.) pp. 667–756. (John Wiley and Sons: New York.) Knülle, W. (1957). Morphologische und entwicklungsgeschichtliche Untersuchungen zum phylogenetischen System der Acari: Acariformes Zachv. 1. Oribatei: Malaconothridae. Mitteilungen Zoologisches Museum Berlin 33, 99–213. Norton, R. A. (1984). Monophyletic groups in the Enarthronota (Sarcoptiformes). In ‘Acarology 6, vol. 1.’ (Eds D. A. Griffiths and C. E. Bowman.) pp. 233–240. (Ellis Horwood Ltd.: Chichester.) Norton, R. A., Kethley, J. B., Johnston, D. E., and OConnor B. M. (1993). Phylogenetic perspectives on genetic systems and reproductive modes of mites. In ‘Evolution and Diversity of Sex Ratio in Insects and Mites.’ (Eds D. Wrensch and M. Ebbert.) pp. 8–99. (Chapman & Hall: New York.) Travé, J., André, H. M., Taberly, G. and Bernini, F. (1996). ‘Les Acariens Oribates.’ (AGAR and SIALF: Wavre.)

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ACAROLOGY

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

PHYLOGENETIC RELATIONSHIPS OF HYPOZETES (ACARI: TEGORIBATIDAE)

....................................................................................................

Valerie M. Behan-Pelletier Biodiversity Program, ECORC, Agriculture and Agri-Food Canada Research Branch, K.W. Neatby Bldg., Ottawa, Ontario, Canada K1A 0C6

.................................................................................................................................................................................................................................................................

Abstract Relationships of the oribatid mite genus Hypozetes are assessed phylogenetically, using characters of adults and newly discovered apheredermous, plicate immatures. The closest relatives of Hypozetes are hypothesised to be among the Tegoribatidae (Achipterioidea) rather than among the Austrachipteriidae (Ceratozetoidea), as suggested in recent classifications. In addition, using characters of newly discovered plicate immatures, the genus Austrachipteria, is considered a member of the Achipteriidae (Achipterioidea), and Austrachipteriidae is placed in synonymy with Achipteriidae.

INTRODUCTION Hypozetes is a small genus with 8 nominal species. The known distribution is East Africa, Tchad, Saudi Arabia, Nigeria, Bulgaria, Bali and Hawai’i. Species in this genus are primarily collected from duff, soil and sand associated with grasses and low-growing herbs. For example, those from Hawai’i have been collected by washing sand from stabilised dunes among grasses and mesquite seedlings, and from grass duff. It is possible that species of Hypozetes are among the oribatid mites (e.g. Allozetes, Lamellobates) that move onto grasses and low-growing herbaceous plants during part of their life-cycle (personal observations). Hypozetes was proposed by Balogh (1959), based on specimens from East Africa. He considered Hypozetes closely related to Ceratozetes (presumably because of the presence and overall shape of immovable pteromorphs, short lamellae, and the octotaxic system) and included it in Ceratozetidae in his identification keys to world genera (Balogh 1961, 1963, 1965, 1972). Subsequently, Balogh and Balogh (1992a) moved Hypozetes to the Austrachipteriidae, a family proposed by Luxton (1985), with Austrachipteria as type genus, within the superfamily Ceratozetoidea. When first proposed, Austrachipteria was placed in the Achipter-

50

iidae (Balogh and Mahunka 1966). Hammer (1967) was the first to suggest a similarity between Hypozetes and Austrachipteria in her description of the genus Parhypozetes (a junior synonym of Austrachipteria), which she considered a member of the Ceratozetoidea. Luxton’s (1985) diagnosis of Austrachipteriidae was based on adult specimens of Austrachipteria only, and included no character states unique to Ceratozetoidea. Subsequently, NübelReidelbach and Woas (1992) questioned the placement of Austrachipteria in the Ceratozetoidea. Behan-Pelletier (1988) hypothesised a relationship between Hypozetes and Lamellobates based on the shared presence in adults of a divided and overlapping, posterior notogastral tectum and unusual notogastral sacculi. These adult characters, and the absence of solenidion ϕ on tibia IV, are shared by Hypozetes, Lamellobates, Paralamellobates and Sacculozetes, and a close relationship between these genera was posited by Behan-Pelletier and Ryabinin (1991). The genera Lamellobates and Paralamellobates also have had chequered systematic histories. Balogh (1961, 1965), Balogh and Balogh (1990), and Fujikawa et al. (1993) considered Lamellobates a member of the Oribatellidae, and both Lamellobates and Paralamellobates were included in the Oribatellidae in Balogh (1972). Balogh and Balogh (1992a) placed Lamellobates,

PHYLOGENETIC

RELATIONSHIPS OF

HYPOZETES (ACARI: TEGORIBATIDAE)

Paralamellobates, Sacculozetes, along with Hypozetes, in the Austrachipteriidae.

members of the Licneremaeoidea, Phenopelopoidea and Achipterioidea.

There are many genera and even families of Brachypylina for which immatures are not yet known, and thus numerous examples of adult convergence and misclassification remain to be revealed: such is the case with Hypozetes. This paper reports the discovery of immature instars of Hypozetes and discusses its systematic relationships in the light of new and reevaluated information. The diagnosis of the genus is expanded to include information on immatures, which are apheredermous and plicate. Based on synapomorphic adult and immature characters it is hypothesised that Hypozetes is not a ceratozetoid mite, but rather is a member of the Achipterioidea, most closely related to the Tegoribatidae.

Also absent from Hypozetes is the humeral organ, which is almost universally present in immatures of Ceratozetoidea, Galumnoidea and Oribatellidae (Norton et al. 1997). Its absence in Hypozetes is plesiomorphic and is of no value in an analysis of relationships.

MATERIALS AND METHODS Adult and immature specimens of Hypozetes laysanensis Aoki, 1964 from Hawai’i were obtained from collections made by R. A. Norton and M. L. Goff. The association of immatures with adults is based on their presence together in samples where there are few other Oribatida. These specimens (Figs 1–9) were compared with adult specimens of other species of Hypozetes and adult and immature specimens of poronotic Brachypylina including Ceratozetidae, Mycobatidae (Ceratozetoidea), Phenopelopidae (Phenopelopoidea), Achipteriidae, Tegoribatidae (Achipterioidea), Oribatellidae, and Austrachipteria housed in the Canadian National Collection of Acari (CNC). Specimens were viewed either with a compound microscope using differential interference contrast, or with scanning electron microscopy.

CHARACTER ANALYSIS OF IMMATURES Opisthosoma

The opisthosomal integument of Hypozetes laysanensis is weakly folded, strongly tuberculate, with larger tubercles bearing setae in larva and nymphs; it lacks any indication of sclerites (Figs 4–6, 7–9). Hypozetes is a member of the poronotic Brachypylina and, among this group, members of only three superfamilies are known to have plicate nymphs: Licneremaeoidea (Adhaesozetidae, Licneremaeidae, Passalozetidae, Scutoverticidae); Achipterioidea (Achipteriidae, Tegoribatidae) and the Phenopelopoidea (Phenopelopidae, Unduloribatidae) (Table 1). Plicate integument, however, is apparently an ancestral state in the poronotic Brachypylina, being possessed by several non-poronotic brachypyline families, and even members of some non-brachypyline groups (Norton and Behan-Pelletier 1986). Thus, as the plesiomorphic state, the plicate condition is no indication of relationships, and these superfamilies can be considered early-derivative Poronota (Norton and Alberti 1997). Clearly, however, the derived states (i.e. the excentric microsclerites of the Oripodoidea, the macrosclerites of the Ceratozetoidea and Galumnoidea, and the apopheredermous, smooth condition of the Oribatellidae), are absent from Hypozetes. Nymphs of H. laysanensis have a unideficient setation; setae h3 appears in the protonymph, rather than in the larva; the larva thus has 11 pairs of gastronotal setae. This delay in appearance of h3 is widespread in poronotic Brachypylina, and has been found also in

An apparently derived state is the overall structure of the hysterosomal integument in Hypozetes, which is tuberculate, or mammillate throughout (Figs 4–6). Similar tuberculate integument has been observed in immatures of T. americanus and Lepidozetes sp., especially on the ventral surface of the opisthosoma. This expression of the integument has also been found to varying extents in immatures of Phenopelopoidea: e.g. anteriad and laterad of the genital opening in Eupelops nymphs, and throughout the ventral region, other than anal valves, in nymphs of some species of Propelops (Norton and Behan-Pelletier 1986). This character state is a possible synapomorphy of these taxa. Another apparently derived state is the presence of large tubercles bearing some of the gastronotal setae: setae d1 (da), d2 (dm), e1 (dp) in the larvae, and setae e1 in the nymphs. This derived state is shared by immatures of Tegoribates americanus Hammer (Tegoribatidae), where setae c2, f2 (lp), d2, e1 of the larvae and e1 of nymphal stages are borne on large tubercles. This derived state was first illustrated for the Tegoribatidae by Tuxen (1943; Figs. 12, 13). However, Hypozetes does not share with T. americanus the apopheredermous opisthosoma. Immatures of an undescribed species of Lepidozetes which have been examined are plicate, unideficient and apheredermous, whereas those of T. americanus, though plicate and unideficient, have scalps closely adpressed to the hysterosoma. In contrast to immatures of Oribatellidae, centrodorsal setae are small in T. americanus, and the scalps are difficult to see and to remove. The opisthosomal gland of immature Hypozetes is lightly sclerotised (Fig. 8), a character state not found elsewhere in the earlyderivative poronotic Brachypylina (Table 1). This character state is independently derived in the Ceratozetoidea. Immatures of Hypozetes also lack the porose integument surrounding the opening of the opisthosomal gland found in immatures of Licneremaeoidea, Phenopelopoidea, Achipteriidae and Austrachipteria which have been examined. A similar absence of porose integument is found in immatures of T. americanus. Legs

Immatures of Hypozetes lack solenidion ϕ on tibia IV of the deutonymph and tritonymph. This loss is an apomorphy and is rare in the Brachypylina, being expressed only in the deutonymph and tritonymph of the phenopelopoid subfamily Phenopelopinae (Eupelops and Peloptulus) and in Liodes theleproctus Hermann (Grandjean 1964). Solenidion ϕ is also absent from tibia IV of adult Lamellobates, Paralamellobates and Sacculozetes, but information is lacking on leg chaetotaxy of immatures for these genera. Immatures of Hypozetes retain seta d to the tritonymph on genua and tibiae (DDC n3, sensu Grandjean 1954). Other than on tibia IV of the deutonymph and tritonymph seta d is associated with the solenidion. Similarly, seta d is

51

Valerie M. Behan-Pelletier

Figures 1–6 Hypozetes laysanensis Aoki; 1–3, adult female; 4–6, tritonymph. 1, dorso-frontal habitus; 2, detail of posterior notogastral tectum and anal region; 3, ventral aspect (arrow indicates tibia IV); 4, frontal habitus; 5, lateral aspect; 6, detail of hysterosoma.

retained to the tritonymph of Tegoribates americanus, to the adult on tibia IV of Phenopelopinae, and to the tritonymph on tibia IV of Achipteriidae and Austrachipteria. In Phenopelopinae seta d on tibia IV has no companion solenidion, whereas d is associated with the solenidion in Achipteriidae and Austrachipteria. Presence of seta d is plesiomorphic, as is the presence of solenidia. Norton and Behan-Pelletier (1986) proposed that the unusual retention of d on tibia IV of the adult of Phenopelopinae may involve an atavistic reversal associated with the need for at least some sensory capacity in the dorsal area

52

of tibia IV, but this argument is not supported by the absence of both seta and solenidion from tibia IV of adult Hypozetes, Paralamellobates, Sacculozetes and Lamellobates.

CHARACTER ANALYSIS OF ADULTS Notogaster

In Hypozetes the notogaster is similar in general appearance to that of Ceratozetoidea, Phenopelopidae, Achipteriidae and Tegoribatidae. Hypozetes has well-developed pteromorphs, which lack the

PHYLOGENETIC

RELATIONSHIPS OF

HYPOZETES (ACARI: TEGORIBATIDAE)

Figures 7–9 Hypozetes laysanensis Aoki; 7, tritonymph, dorsal aspect; 8, tritonymph, ventral aspect; 9, larva, dorsal aspect.

basal hingelike line of desclerotisation and the concentration of strong adductor muscles at their base which permit pteromorph mobility found in Phenopelopinae and Tegoribatidae. Fully movable pteromorphs are a derived state that have apparently evolved independently many times in the Brachypylina; the type of pteromorph in Hypozetes is plesiomorphic. Hypozetes have a posterior notogastral tectum which is medially divided with overlapping lobes. A posterior notogastral tectum is present in at least some members of all poronotic, brachypyline superfamilies, other than Phenopelopoidea, and the polarity of this character state is unre-

solved (Behan-Pelletier 1988). The expression of this tectum, with unfused, medial lobes (overlapping or not) is rare, and is a character state which Hypozetes shares with Lamellobates, Paralamellobates, and Sacculozetes, and which is apparently independently derived in the Adhaesozetidae (Licneremaeoidea) and Mycobatidae (Ceratozetoidea) among poronotic Brachypylina. The adult notogastral setation of Hypozetes comprises 10 pairs, which is a common setation in the Brachypylina. The octotaxic system is composed of 4 pairs of sacculi, which can be both simple

53

54 0–4 pairs A,S

macrosclerites

apheredermous

yes/no

no

no

yes

DDC el

DDC el

Integument

Opisthosoma

Humeral organ

Some gastronotal setae carried on large tubercles

opisthosomal gland porose area

Opisthosomal gland sclerotised

Companion seta d (tibia I-III)

Companion seta d (tibia IV)

IMMATURE

DDC el DDC n3

DDC el DDC n3

no

yes

no

no

apheredermous

plicate

yes

yes

Solenidion φ on tibia IV

no yes/no

yes

Postanal porose area no

3–7 pairs A,S

Octotaxic System

yes/no

no hinge

yes/no

no

Birefringent cerotegument

Axillary saccule of infracapitulum yes

no hinge/ hinged

Pteromorph

Ng NBP Ng TLP Ng TLP overlapping

LICNEREMAEOIDEA

Genal incision

Ng NBP Ng TLP Ng TLP overlapping

Notogaster

ADULT

CERATOZETOIDEA

DDC Ad

DDC el

no

yes

no

no

apheredermous

plicate; tuberculate ventrally

yes (Propelops) no (Eupelops, Peloptulus)

yes

yes

no

1,2,4 pairs A

yes

no hinge/ hinged

Ng NBP

PHENOPELOPIDAE

DDC n3

DDC el

no

yes

no

no

apheredermous

plicate

yes

yes

no

no

1,4 pairs A,S

no

no hinge

Ng TLP

ACHIPTERIIDAE

DDC n3

DDC el

no

yes

no

no

apheredermous

plicate

yes

yes

no

no

4 pairs S

no

no hinge

Ng TLP

Austrachipteria

DDC n3

DDC n3

no

no

yes

no

apheredermous; apopheredermous

plicate; tuberculate

yes

no

yes

yes

4 pairs A,S

no

hinged

Ng TLP

TEGORIBATIDAE

DDC n3

DDC n3

yes

no

yes

no

apheredermous

plicate; tuberculate

no

no

yes

yes

4 pairs S

no

no hinge

Ng TLP overlapping

Hypozetes

Summary of analysis of character state polarities. Characters in boldface are considered apomorphic. Abbreviations: Ng NBP, notogaster without posterior tectum; Ng TLP, notogaster with posterior tectum; A, porose areas; S, sacculi; DDC, companion seta d of genua and tibiae absent throughout ontogeny (el); present to the tritonymph (n3); present to the adult (Ad).

Character/states

Table 1 Valerie M. Behan-Pelletier

PHYLOGENETIC

Table 2

RELATIONSHIPS OF

HYPOZETES (ACARI: TEGORIBATIDAE)

Development of leg setae and solenidia in Hypozetes laysanensis Aoki (Setae are noted opposite the instar in which they first appear; () parentheses indicate setal pairs; [ ] parentheses indicate setal loss). Trochanter

Femur

Genu

Tibia

Tarsus

–

d bv"

ds (l)

dϕ1 (l)ν’

e

–

σ1(ft)(tc)(p)(u)(a)s(pv)(pl) ω2

LEG I Larva Protonymph

–

–

–

Deutonymph

–

(l)

–

ϕ2

–

Tritonymph

v'

-

v’

v"

(it)

Adult

–

v'

–

[d]

–

LEG II Larva

–

d bv"

dσ (l)

dϕ l'v'

ω1(ft)(tc)(p)(u)s(a)(pv)

Protonymph

–

–

–

–

–

Deutonymph

–

(l)

–

l"

–

Tritonymph

v'

-

v’

v"

(it)

Adult

–

v'

[d]

[d]

–

Larva

–

d ev'

dσ l'

dϕ v'

(ft)(tc)(p)(u)s(a)(pv)

Protonymph

–

–

–

–

–

Deutonymph

v'

–

–

–

–

Tritonymph

l’

l'

–

l' v"

(it)

Adult

–

–

[d]

[d]

–

Protonymph

–

–

–

–

ft"(p)(u)(pv)

Deutonymph

–

d ev’

d

d v'

(tc)s(a)

Tritonymph

v'

–

l’

(l)

–

Adult

–

–

–

[d]

–

LEG III

LEG IV

and furcate in the same species, based on specimens of Hypozetes in the CNC, and H. laysanensis. Sacculus S1 is comparatively closely associated with seta f2 (lp), as is S4 with h1 but, as Norton and Alberti (1997) noted, juxtaposition of the octotaxic system with notogastral setae is common in early-derivative Poronota. Prodorsum

In addition to the shape of the notogaster, the shape of the lamella has probably influenced some workers to place Hypozetes in the Ceratozetoidea. However, this character varies extensively within genera and families of poronotic Brachypylina, and the polarity of these variations is unclear. Hypozetes also shares a well-developed tutorium with Ceratozetoidea, Phenopelopoidea and Achipterioidea. It lacks a genal incision, found in the Ceratozetoidea, Phenopelopoidea and Achipteriidae, but similarly absent in the Tegoribatidae. However, the genal incision can undergo loss within a genus, for example, Melanozetes (Ceratozetidae). Podosoma and ventral plate

As with most members of the poronotic Brachypylina, Hypozetes has porose area Ah of the humerosejugal series (Norton et al. 1997). Hypozetes also has a postanal porose area, a structure absent from the Licneremaeoidea, Phenopelopoidea, Achipteriidae and Austrachipteria, and unique to Tegoribatidae among early derivative poronotic Brachypylina. The postanal porose area is also

found in Ceratozetoidea, Galumnoidea and Oribatellidae, and its presence in Hypozetes and Tegoribatidae may indicate a relationship between these taxa. Gnathosoma

The mouthparts of Hypozetes are similar to those of most members of Ceratozetoidea: a mental tectum is lacking, chelicera are developed normally, eupathidium acm is fused to the solenidion on the palp tarsus, and the axillary sacculus of the infracapitulum is present. The latter character state is found in adults of all Ceratozetoidea, Phenopelopoidea, Galumnoidea, Oribatellidae, Genavensiidae and Tegoribatidae; it is absent from Oripodoidea, Achipteriidae and Austrachipteria. Legs

The most distinctive leg character of Hypozetes is the absence of solenidion ϕ from tibia IV (Table 2). Similarly, this solenidion is absent from adults of Lamellobates, Paralamellobates, Sacculozetes (Behan-Pelletier and Ryabinin 1991; Behan-Pelletier 1998), and the Phenopelopinae (Grandjean 1964). Whether this loss is independently derived in these taxa is unclear. There are two additional leg characters in Hypozetes which have also been noted in the Phenopelopidae (Norton and Behan-Pelletier 1986). Seta l’ of tibia IV is thick and spinelike in Hypozetes. It is similarly shaped in members of the Phenopelopidae, but in the latter the seta is

55

Valerie M. Behan-Pelletier

shorter. It is also spinelike in Lepidozetes (Tegoribatidae), in Lamellobates and Paralamellobates, but is long and thin in T. americanus, Austrachipteria and Achipteriidae, as in other poronotic Brachypylina. Dorsally on tibia IV and dorsoproximally on tarsus IV of Hypozetes there is a longitudinal carina. It has been observed on the dorsal surface of tibia and tarsus IV of Lepidozetes (Tegoribatidae), Lamellobates and Paralamellobates, and a similar carina occurs on tibia IV in some members of the Phenopelopidae (Norton and Behan-Pelletier 1986). A carina is absent from tibia IV in T. americanus, Austrachipteria and Achipteriidae. Cerotegument

Both immature and adult Hypozetes have a thin layer of cerotegument with a microtuberculate structure. This structure is similar to that of Achipterioidea in that it is easily removed from immatures using lactic acid. Adult Hypozetes lack the thick layer of cerotegument, birefringent in polarised light, which is an autapomorphy of members of the Phenopelopoidea.

DISCUSSION A new diagnosis of Hypozetes incorporating characters of both adults and plicate immatures is presented. Genus Hypozetes Balogh 1959

Poronotic Brachypylina with immatures having weakly plicate, tuberculate integument; opisthosomal dorsum with large tubercles bearing setae in the larva and nymphs. Nymphs with unideficient setation; larva lacking seta h3. Paraproctal atrichosy in larva, protonymph and deutonymph. Seta d retained to the tritonymph, associated with solenidion on genua I to IV and tibiae I to III; solenidion absent from tibia IV of nymphs and adult. Opisthosomal gland in immatures lightly sclerotised; integument surrounding opening of opisthosomal gland non-porose. Adult with medially divided, posterior notogastral tectum with overlapping lobes; with lamella, lamellar cusps, tutorium, pedotectum I, II, and discidium; without genal incision. Notogaster with lenticulus, immovable pteromorphs, 10 pairs of setae and 4 pairs of sacculi. Axillary saccule of the infracapitulum and postanal porose area present. Family placement of Hypozetes

Of the characters discussed above, only the presence of a divided posterior notogastral tectum appears to be shared by Hypozetes and the Ceratozetoidea. This character state is convergently expressed also in the poronotic Adhaesozetidae (Walter and Behan-Pelletier 1993). However, Hypozetes lacks macrosclerites in immatures, the apomorphy for the Ceratozetoidea and Galumnoidea. Among early derivative poronotic Brachypylina, no synapomorphies relate Hypozetes to Austrachipteria, the type-genus of Austrachipteriidae. Similarly, no synapomorphies support a relationship between Hypozetes and Achipteriidae. Similarities in five character states support a relationship between Hypozetes and the Phenopelopoidea: (i) absence of solenidion j from tibia IV in post-protonymphal immatures and adult; (ii) opisthosomal integument of immatures at least partially tuberculate; (iii) presence of the axillary saccule of the subcapitulum; (iv) shape of seta l’ on tibia IV; and (v)

56

carina on the dorsal surface of tibia IV. Absence of solenidion ϕ from tibia IV is unique to Phenopelopinae and Hypozetes, Lamellobates, Paralamellobates and Sacculozetes among poronotic Brachypylina. But this solenidial loss is also expressed in the brachypyline Liodes theleproctus, in the Enarthronota, and in Malaconothrus (Grandjean 1964). Hypozetes lacks the apomorphy unique to the Phenopelopoidea, namely the blocky cerotegument of adults, birefringent in polarised light. Similarity in eight character states supports a relationship between Hypozetes and Tegoribatidae: (i) presence of the axillary saccule of the infracapitulum; (ii) presence of postanal porose area; (iii) absence of a genal incision; (iv) opisthosomal integument of immatures at least partially tuberculate; (v) some opisthosomal setae of immatures carried on large tubercles; (vi) integument surrounding opening of opisthosomal gland non-porose; (vii) shape of seta l’ on tibia IV; and (viii) carina on the dorsal surface of tibia IV. Hypozetes and Tegoribatidae are the only early-derivative poronotic Brachypylina with a post-anal porose area. Evidence strongly suggests a close relationship between Hypozetes and members of the Tegoribatidae. Hypozetes lacks the fused lamella and hinged pteromorphs found in all Tegoribatidae described so far, but the former character state is convergently derived more than once in the Oribatellidae, and the latter in the Ceratozetoidea. A phylogenetic analysis of the relationship between genera in Tegoribatidae and Hypozetes is beyond the scope of this paper, and awaits examination of immatures and adults of all genera within Tegoribatidae.

COMMENTS ON AUSTRACHIPTERIIDAE As noted above, the diagnosis of Austrachipteriidae was based on adult specimens only of Austrachipteria (Luxton 1985). I have examined adults and immatures from Tasmania of species similar to Austrachipteria grandis (Hammer 1967) and A. macrodentatus (Hammer 1967). Immatures are plicate, apheredermous, and similar to those of genera in Achipteriidae, with plication similar to Achipteria nitens (Nicolet) ( Seniczak 1977, 1978). Seta d, lost from the tibiae and genua on legs I to III, is retained on tibia IV in the deutonymph and tritonymph, and is associated with the solenidion in Austrachipteria, as in species of Achipteria (Grandjean 1946), Parachipteria (Seniczak 1978) and Anachipteria (Seniczak 1977). As in adults of species of Anachipteria, the pteromorph of Austrachipteria does not bear anterior projections. Based on adult and immature characters, Austrachipteria is apparently closely related to other genera in the Achipteriidae. No apomorphy defines the family Austrachipteriidae and it is proposed that this family be placed in synonymy with Achipteriidae.

COMMENTS ON LAMELLOBATES, PARALAMELLOBATES AND SACCULOZETES Immatures of Lamellobates and Paralamellobates currently under study indicate that these genera lack the microsclerites of Oripodoidea, the macrosclerites of Ceratozetoidea and Galumnoidea, and the apopheredermous condition of Oribatellidae. Immatures also lack the strong plications of Phenopelopoidea and Achipteriidae. It is possible that, as with Hypozetes, they are most closely related to the Tegoribatidae. Eupathidium acm and the solenidion of the palptarsus are not fused in Lamellobates and Paralamel-

PHYLOGENETIC

lobates, as recorded for members of Tegoribatidae for which the palp has been examined (Grandjean 1954; Nübel-Reidelbach and Woas 1992). It is clear that further analysis is needed to resolve whether Lamellobates, Paralamellobates and Sacculozetes are members of the Tegoribatidae and to assess relationships between its included genera.

ACKNOWLEDGEMENTS My sincere thanks to R.A. Norton, SUNY College of Environmental Science and Forestry for specimens; B. Eamer, and the SEM Centre of Agriculture and Agri-Food Canada for the scanning electron micrographs; B. Flahey for inking the figures; M. Simard for digitising images; and my colleagues R.A. Norton of SUNY and E. E. Lindquist of Research Branch, Agriculture and Agri-Food Canada for their many helpful suggestions.

REFERENCES Aoki, J.-I. (1964). Some oribatid mites (Acarina) from Laysan Island. Pacific Insects 6, 649–664. Balogh, J. (1959). Some Oribatid mites from Eastern Africa (Acari: Oribatidae). Acta Zoologica Academiae Scientiarum Hungaricae 5, 13–32. Balogh, J. (1961). Identification keys of world oribatid (Acari) families and genera. Acta Zoologica Academiae Scientiarum Hungaricae 7, 243-344. Balogh, J. (1963). Identification keys of holarctic oribatid mites (Acari) families and genera. Acta Zoologica Academiae Scientiarum Hungaricae 9, 1–60. Balogh, J. (1965). A synopsis of the world oribatid (Acari) genera. Acta Zoologica Academiae Scientiarum Hungaricae 11, 5-100. Balogh, J. (1972). ‘The Oribatid Genera of the World.‘ (Akademiai Kiadó: Budapest.) Balogh, J., and Balogh, P. (1990). ‘Oribatid Mites of the Neotropical Region II.‘ (Elsevier: Amsterdam.) Balogh, J., and Balogh, P. (1992a). ‘The Oribatid Mites Genera of the World. Volume 1.‘ (Hungarian National Museum Press: Budapest.) Balogh, J., and Balogh, P. (1992b). ‘The Oribatid Mites Genera of the World. Volume 2.‘ (Hungarian National Museum Press: Budapest.) Balogh, J., and Mahunka, S. (1966). New Oribatid (Acari) from Australian Soils. Folia Entomologica Hungarica 19, 553–568. Behan-Pelletier, V. M. (1988). Redefinition of Zachvatkinibates (Acari: Mycobatidae) with description of a new species and immatures of Z. maritimus Shaldybina 1973. Canadian Entomologist 120, 797–813.

RELATIONSHIPS OF

HYPOZETES (ACARI: TEGORIBATIDAE)

Behan-Pelletier, V. (1998). Ceratozetoidea (Acari: Oribatida) of lowland tropical rainforest, La Selva, Costa Rica. Acarologia, 39, 349–382. Behan-Pelletier, V., and Ryabinin, N.A. (1991). Description of Sacculozetes filosus gen. nov., sp. nov. and Guatemalozetes danos sp.nov. (Acari: Oribatida) from grassland habitats. Canadian Entomologist 123, 1135-1147. Fujikawa, T, Fujita, M., and Aoki, J. (1993). Checklist of oribatid mites of Japan (Acari: Oribatida). Journal of the Acarological Society of Japan 2 (Supplement 1), 1–121. Grandjean, F. (1946). La signification évolutive de quelques caractères des Acariens (1re série). Bulletin Biologique France Belge 79, 297–325. Grandjean, F. (1954): Essai de classification des Oribates (Acariens). Bulletin de la Société Zoologique de France 78, 421–446. Grandjean, F. (1964). La solenidiotaxie des Oribates. Acarologia 6, 529–556. Hammer, M. (1967). Investigations on the Oribatid fauna of New Zealand. Part II. Biologiske Skrifter Det Kongelige Danske Videnskabernes Selskab 15, 1–60. Luxton, M. (1985). Cryptostigmata - a concise review. Fauna of New Zealand 7, 1–106. Norton, R. A., and Alberti, G. (1997). Porose integumental organs of oribatid mites (Acari, Oribatida). 3. Evolutionary and ecological aspects. Zoologica. 146, 115–143. Norton, R. A., and Behan-Pelletier, V. M. (1986). Systematic relationships of Propelops, with a modification of family-group taxa in Phenopelopoidea (Acari: Oribatida). Canadian Journal Zoology 64, 2370–2383. Norton, R. A., Alberti, R. A. G., Weigmann, G., and Woas S., (1997). Porose integumental organs of oribatid mites (Acari, Oribatida): 1. Overview of types and distribution. Zoologica. 146, 1–31. Nübel-Reidelbach, E., and Woas, S. (1992). Eimige basale Arten der cepheiden und der pterogasterinen Entwicklungslinie der Höheren Oribatiden (Acari, Oribatei). Andrias 9, 75–119. Seniczak, S. (1977). The systematic position of moss mites of the genus Anachipteria Grandjean, 1935 (Acarina, Oribatei) in the light of ontogenetic studies. Acarologia 18, 740–747. Seniczak, S. (1978). The morphology of juvenile forms of soil mites of the family Achiperiidae (Acari, Oribatei). I. Annales Zoologici 34, 89–99. Tuxen, S. L. (1943). Die zeitliche und räumliche Verteilung der Oribatiden-Fauna (Acar.) Bei Mælifell, Nord-Island. Entomologiske Meddellellser 23, 321–336 + 2 plates and 5 Tables. Walter, D. E., and Behan-Pelletier, V. M. (1993). Systematics and ecology of Adhaesozetes polyphyllos sp. nov. (Acari: Oribatida: Licneremaeoidea), a leaf-inhabiting mite from Australian rainforests. Canadian Journal of Zoology 71, 1024–1040.

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ACAROLOGY

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

SYSTEMATIC RELATIONSHIPS OF NOTHROLOHMANNIIDAE, AND THE EVOLUTIONARY PLASTICITY OF BODY FORM IN ENARTHRONOTA (ACARI: ORIBATIDA) ....................................................................................................

Roy A. Norton College of Environmental Science and Forestry, State University of New York, Syracuse, New York 13210 U.S.A. [email protected].

.................................................................................................................................................................................................................................................................

Abstract Nothrolohmannia, the single nominal genus comprising the oribatid mite family Nothrolohmanniidae, is proposed as the sister group of the enarthronote genus Malacoangelia (Hypochthoniidae), based on 14 shared, derived character-states. By inference, the characteristic transverse notogastral scissure found in Malacoangelia and other hypochthoniid mites has been lost by fusion in Nothrolohmannia. A classification proposed to reflect this hypothesis includes both Nothrolohmannia and Malacoangelia in the Hypochthoniidae, subfamily Nothrolohmanniinae (new status). This relationship is a previously unknown example of the evolutionary plasticity afforded by the serial arrangement of plates in Enarthronota. Most enarthronote genera possess a specialised defensive morphology that includes two rows of erectile dorsal setae in transverse scissures, or else were derived from ancestors that possessed them. Several trends can be seen in two of the derivative taxa, Hypochthonioidea and Protoplophoroidea. One is the evolution of better cuticular armour (including mineralisation) and reduction of vulnerable transverse scissures, thereby replacing erectile setae as a defense mechanism. Another is the defensive ptychoid body form, convergently evolved from similar transitional morphologies in the two superfamilies. Another is a paedomorphic trend in the lineage containing Haplochthoniidae and Pediculochelidae, which has led to the loss of any noticeable predator defense. An appropriate classification of Enarthronota, and of Oribatida in general, will be a compromise that highlights, but does not overemphasise, this diversity in body form.

INTRODUCTION With regard to diversity of body form, few suborders or orders of arthropods can rival the oribatid mites. An important aspect of form is the development and arrangement of major cuticular plates and their separating articulations. Oribatid mites had a ‘clean slate’ for the evolution of such plates, since their common ancestor was almost certainly soft-bodied. As rationale, the closest extant outgroups of oribatid mites – Terpnacaridae, Alicorhagiidae, and the other acariform families that have been loosely grouped as ‘Endeostigmata’ (Grandjean 1939; OConnor 1984; Bernini 1987; Norton et al. 1993) – lack noticeable body plates (Fig. 1a).

58

Plate formation in adult oribatid mites has an extreme spectrum. Acaronychid Palaeosomata have only patches of weak sclerotisation that provide support for setal bases or muscle insertions (Fig. 1b), while some middle-derivative Desmonomata (e.g. Nanhermanniidae, Crotoniidae) are almost encased in hardened cuticle without a major articulation. Most oribatid mites lie near the latter end of the spectrum, as indicated by their common names (beetle mites, armoured mites). An underlying theme may explain this extensive plate development (Norton 1994). Oribatid mites, at least in the traditional sense (excluding Astigmata), generally have long life cycles and low fecundity. Their typical food, decaying plant material and

SYSTEMATIC RELATIONSHIPS

Figure 1

OF

NOTHROLOHMANNIIDAE

(a) Lateral aspect of an endeostigmatid mite, Terpnacarus, showing distinct hysterosomal segmentation but no cuticular plates (from Grandjean 1939). (b) Lateral aspect of an early-derivative palaeosomatan, Acaronychus, showing discrete patch-like hysterosomal plates (from Grandjean 1954b). (c) Schematic lateral aspect of a dichoid body form. (d) Schematic lateral aspect of a trichoid body form. (e) Schematic lateral aspect of a ptychoid body form. (f) Schematic lateral aspect of a holoid body form in Desmonomata. (g) Schematic lateral aspect of a holoid body form in Brachypylina. (h) Lateral aspect of an enarthronote mite, Haplochthonius, showing multiple dorsal plates separated by transverse scissures (from Grandjean 1947). (i) Schematic section of transverse scissure having the form of a narrow articulating band between plates (type E of Grandjean 1947). (j) Schematic section of transverse scissure in which the anterior plate (right) extends as a tectum over a broad articulating band of soft cuticle (type L of Grandjean 1947). (k) Same, upper is contracted, lower is maximally expanded (from Grandjean 1934). (l) Schematic section of complex transverse scissure, type-S of Grandjean (1947), in which an intercalary sclerite lies within the scissure. (m) Same; upper shows contracted scissure with prone seta, lower shows expanded scissure with erected seta (from Grandjean 1931). (n) Dorsal aspect of type-S scissure and setal bases (from Grandjean 1931).

59

Roy A. Norton

fungi, is unlike that of most other arachnids, and perhaps the rather inefficient use of such foods is ultimately responsible for the relatively low metabolic rate of these mites. Rather than being adaptive, traits such as extended development and slow, iteroparous recruitment can be viewed as consequences of metabolic constraints. In turn, low recruitment rate puts a premium on long adult life. In this evolutionary context, defense mechanisms such as extensive cuticular hardening have great importance. (Constraints in digestive physiology were perhaps the major hurdles overcome in the evolution of the Astigmata, in which r-selected life histories are the rule, from oribatid mites with K-style life histories; Norton 1994). The principal body forms of oribatid mites with extensive plate development, outlined by Grandjean (1969; see also Norton 1975), seem to represent different solutions to that essential compromise of cuticular hardening: protection and support versus flexibility. In the dichoid body form (Fig. 1c), the sejugal region remains unhardened and forms a principal plane for the bending and telescoping that is associated with movement and control of body fluid pressure. In trichoid mites, a second transverse articulation (Fig. 1d) defines a postpedal plane of bending for these taxa, which usually inhabit the restricted spaces of mineral soil. In the ptychoid body form (Fig. 1e), extensive soft cuticle in the podosomal region allows the withdrawal of legs into a secondary cavity closed by an operculum-like prodorsum. In the holoid body form (Fig. 1f) the sejugal articulation is not retained ventrally, which promotes ventral rigidity that reaches its maximum in the brachypyline condition (with fused coxisterna IV, aggenital and adanal plates); in this latter case, body volume control shifts to the circumgastric articulation between a cap-like notogaster and the rigid ventral plate (Fig. 1g). Within the major oribatid mite groups recognised by Grandjean (1969) the diversity of form varies. The holoid form has proven very successful and is essentially fixed in the Desmonomata (except in the paedomorphic lineage that includes Astigmata; Norton 1998) and in the most species-rich group, Brachypylina (the ‘higher oribatid mites’). The paraphyletic Mixonomata includes both dichoid and ptychoid taxa, and most Parhyposomata are trichoid. While body forms in the Palaeosomata are usually not characterised, probably due to the low degree of cuticular hardening, they are rather diverse. Acaronychoid mites have no major plates, Palaeacaridae and Ctenacaridae are essentially dichoid, and Aphelacaridae are essentially trichoid. The greatest concentration of body form diversity, however, is found in Enarthronota, the seminal studies of which appeared as a series of papers by Grandjean (1947, 1948, 1950a, 1954a). As Grandjean (1947, see also 1969) first defined the group, enarthronote mites are recognised by having a notogaster composed of a series of plates (e.g. Fig. 1h). Dorsally there are two to four plates (collectively, the notaspis) separated by one to three transverse scissures (narrow bands of soft articulating cuticle). Laterally, a longitudinal suprapleural scissure partly or fully isolates a paired pleuraspis from the dorsal plates. Grandjean recognised the transverse scissures (‘coupures’) as key elements in the evolution of Enarthronota, particularly since they have been specialised in some groups to the point of becoming major body articulations.

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While weak hysterosomal plates of some Palaeosomata and Parhyposomata might be considered serial, only Enarthronota have fully capitalised on the adaptive potential of such an arrangement. Plates have variously regressed or hypertrophied, or have been fused in different ways, and the articulations have been functionally modified. One purpose of this paper is to develop this idea, particularly using examples in two major lineages of Enarthronota, the Hypochthonioidea and Protoplophoroidea. Before that, a previously unrecognised part of this diversity will be discussed: at least one lineage within Hypochthonioidea has abandoned the essence of Enarthronota by fusing all the dorsal plates to create – oxymoronically – a ‘holonotic’ enarthronote.

RELATIONSHIPS OF NOTHROLOHMANNIIDAE The oribatid mite family Nothrolohmanniidae and its only described species, Nothrolohmannia calcarata, were proposed by Balogh (1968), based on adults collected from rainforest soil in New Guinea. No further collections have been reported in the literature and, while the original descriptions of these taxa were sufficient for identification, most morphological details have remained unknown. Relationships of the family were not discussed in the original publication, but several alternatives have since been proposed. Balogh (1972) included Nothrolohmanniidae in Lohmannioidea, along with Lohmanniidae and Xenolohmanniidae, but without discussion. This superfamily was included in Dichosomata (a subgroup of Mixonomata) by Balogh and Mahunka (1979; see also Fujikawa 1991). Lee (1985) proposed a more early-derivative position for Lohmannioidea within the oribatid mites but maintained its internal classification. In a cladistic analysis, Haumann (1991) effectively disbanded Balogh’s internal classification of Lohmannioidea by including Xenolohmannia (the only genus in Xenolohmanniidae) within Lohmanniidae, and by considering Nothrolohmanniidae to be the earliest derivative member of the large taxon Holonota. Like Haumann, Balogh and Balogh (1992) included Xenolohmannia within Lohmanniidae; they also removed Nothrolohmanniidae from Lohmannioidea but transferred it instead to the Desmonomata, as part of Crotonioidea. A different hypothesis is developed below: Nothrolohmannia is the sister taxon of the enarthronote genus Malacoangelia. The latter (with but two nominal species, one with several nominal subspecies) is a pantropical genus whose position within the Hypochthoniidae is well founded (Grandjean 1935a; Norton 1984a). Perhaps the most significant inference from this hypothesis is that a ‘holonotic’ notogaster, i.e. a dorsal opisthosomal sclerite without transverse articulations, has evolved independently at least twice: once in Enarthronota and once in the common ancestor of Holonota (approximately sensu Haumann 1991).

MATERIALS AND METHODS A single topotypic adult of Nothrolohmannia calcarata was studied, taken from the same Berlese-funnel extract as the type series; the series was collected at Lae, in eastern New Guinea (6o 44’S, 147o 0’E). Also studied were 12 adults of an unnamed Nothrolohmannia species (Figs. 2, 3) collected from rainforest litter near

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Figure 2

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Nothrolohmannia n. sp. (a) Dorsal aspect (scale = 20 µm). (b) Ventral aspect; arrow points to grooved line of fusion between anal and adanal plates (scale = 20 µm). (c) Anterolateral aspect of prodorsum (scale = 10 µm). (d) Anterior aspect (scale = 10 µm). Abbreviations: c3 = notogastral seta on humeral tubercle, ro = rostral seta.

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Figure 3

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Nothrolohmannia n. sp. (a) Lateral aspect (scale = 20 µm). (b) Same, enlargement showing legs III and IV retracted into pedofossae; arrow points to suprapleural scissure (scale = 10 µm). (c) Distal part of subcapitulum, ventral aspect; arrow points to hyaline distal part of opposite rutellum (scale = 3 µm). (d) Propodosoma, ventral aspect (scale = 10 µm). (e) Enlargement of rostral margin, showing submarginal denticles in lower left (scale = 3 µm). Abbreviations: or2 = second adoral seta, ru = rutellum (partially hidden dorsal to adoral setae).

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Vanimo (2o 41’S, 141o 18’E), in western New Guinea, by R. W. Taylor, 10-vii-1972 (samples ANIC413, 414, 415 in the Australian National Insect Collection, CSIRO, Canberra). A description is in progress. Specimens of Malacoangelia remigera Berlese (many adults, one tritonymph), used for comparisons, are in the author’s collection and derive from various sites in Florida (USA), Brazil, the Ivory Coast and New Guinea. All instars of Hypochthonius rufulus C. Koch, from various collections in New York (USA) and Germany, and of Eohypochthonius gracilis (Jacot), from various collections in North Carolina (USA), were studied as representatives of their respective genera. Light microscopy observations were of whole and dissected specimens, using bright-field and differential interference contrast illumination. A Robinson backscatter detector was used in scanning electron microscopy. Synapomorphies of Malacoangelia and Nothrolohmannia

Malacoangelia and Nothrolohmannia share 14 characters states that are considered derived within Hypochthoniidae. These synapomorphies are numbered and discussed below, grouped by general body region. Outgroups for assessing character state polarity were selected based on a previous cladistic analysis of the Hypochthonioidea (Norton 1984a). They include the two other genera of Hypochthoniidae, Hypochthonius and Eohypochthonius, as closest outgroups and Eniochthonius (Eniochthoniidae) as the next more distant outgroup. For each character the apomorphic state is given first, followed in parentheses by the state considered plesiomorphic (pl) within Hypochthonioidea. 1. Lateral region of prodorsum and notogaster with pedofossae for coaptation of retracted legs I (pl = without pedofossae). Defensive adaptations that involve retraction of legs into individual ventrolateral cavities (pedofossae) are rare in macropyline (‘lower’) oribatid mites, and were previously known only in Lohmanniidae and Malacoangelia (Grandjean 1935a). Living M. remigera rapidly fold their legs and press them to the body when disturbed (unpublished observations), and the mites are often preserved in this state. To accept retracted legs I and II, the prodorsum has lateral concavities and grooves, the contours of which lend a unique appearance in dorsal aspect. One groove nearly encircles the rostrum and sets off a truncate or hammerhead-like anterior portion that bears the rostral setae. The notogastral pleuraspis has two well defined pedofossae on each side that individually receive retracted legs III and IV. Nothrolohmannia has virtually identical prodorsal and pleuraspal pedofossae (Fig. 3a, b). 2. Limb of rostral tectum with dense, comblike submarginal denticles (pl = without submarginal denticles). It is not rare for the rostral margin of oribatid mites to be dentate, and such structure has clearly evolved independently multiple times. In outgroups the margin is either smooth or weakly and sparsely denticulate. Grandjean (1935a) first noted the very different rostral structure of Malacoangelia: a narrow, dense band of slender, sharp denticles lies submarginally, on the underlying limb of the rostral tectum. Nothrolohmannia has a virtually identical row of submarginal denticles (Fig. 3d, e), as well as a row of smaller denticles on the margin itself. 3. Rostral seta hypertrophied, biramous (pl = setiform, uniramous). The rostral seta of Malacoangelia bifurcates close to the insertion,

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with the two distal branches spreading in opposite directions, one posteriad and one anteroventrad; the result is a vaned, rather Tshaped or reniform seta. Among other body setae, only notogastral setae c2 are similarly biramous in M. remigera (Grandjean 1935a), and in M. similis (Sarkar and Subias 1982) only the lamellar setae are also biramous. Only the rostral seta is biramous in Nothrolohmannia, and its branches are directed as in Malacoangelia (Fig. 2c, d) except, like other body setae, it is longer and less distinctly vaned than that of Malacoangelia. Both taxa often carry a thick, amorphous secretion or deposit on the rostrum, which can obscure these setae. In Sphaerochthonius (an enarthronote mite not closely related to Malacoangelia) most body setae are usually T-shaped; this includes the rostral pair, but they have form and direction different from those described above. 4. Bothridium with ventral saccule having minute lobes (pl = without saccule). Hypochthoniodea and Heterochthoniidae are unique among Enarthronota in having a bothridium with walls that appear densely porose, although the exact nature of this porosity has not been determined by studies of ultrastructure. In Heterochthoniidae and Malacoangelia the bothridium has a purse-like fold, or pouch, on the anteromedial side. In Malacoangelia, but not Heterochthoniidae, the pouch extends ventrally, away from the path of the setal base, and forms a short saccule (Grandjean 1935a; his Fig. 2D). In other Hypochthonioidea the bothridium has no pouch or saccule. Nothrolohmannia has a porose bothridium and a saccule that is virtually identical to that of Malacoangelia. Bothridial saccules are found in several nonenarthronote, macropyline taxa (see Norton et al. 1997), but those of Malacoangelia and Nothrolohmannia n. sp. (not studied in N. calcarata) seem to be unique: a thin cuticular layer above each pore canal (perhaps the epicuticle) bulges away from the bothridium, creating a large number of thin-walled, minute lobes. 5. Notogaster with humeral tubercles that bear setal pair c3 (pl = without humeral tubercles). Among Enarthronota only Malacoangelia is known to have humeral tubercles on the notogaster, and these lend a distinctive truncate appearance to the anterior margin. Nothrolohmannia is the only other genus of macropyline oribatid mite known to have such tubercles (Fig. 2a). 6. Notogaster anteromedially with single or multiple porose areas having unique cuticular structure (pl = without well-defined porose areas). Malacoangelia has been distinctive among Enarthronota in possessing an unpaired, convex notogastral porose area (Grandjean 1935a), which wrongly has been called a ‘lenticulus.’ Nothrolohmannia has an elliptical ring of small, convex porose areas in the same position, lying immediately behind setal pair c1, that seem homologous with the single large area of Malacoangelia. The cuticule of these porose areas is complex and unique (Alberti et al. 2001). By inference, there has been either fusion or subdivision of these porose organs during the evolution of the two genera; both types of changes are well known in Brachypylina (Norton et al. 1997). 7. Suprapleural scissure U-shaped, complete posteriorly (pl = scissure interrupted posteriorly). When a pleuraspis is present in macropyline mites, it is usually not separated from the notaspis posteriorly; i.e. the paired suprapleural scissures end before reaching the

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posterior midline. This is true of the outgroups, but in Malacoangelia the scissures are continuous posteriorly, at least as a distinct line of weakness, which fully separates notaspis and pleuraspis. Nothrolohmannia shares this structure (Fig. 3b). 8. Anal and adanal plates functionally fused (pl = plates articulated). Ancestrally, anal plates fully articulate with adanal plates or their derivatives. This is true of the outgroups and of most other oribatid mites. In Malacoangelia, anal and adanal plates are fused longitudinally, but a groove demarcates their ancestral articulation except anteriorly (Grandjean 1935a). The plates of Nothrolohmannia n. sp. are similar (Fig. 2b), while in N. calcarata the groove is present throughout their length. This synapomorphy is considerably weakened by homoplasy, since anal and adanal plates have fused independently within several clades of macropyline oribatid mites. Examples include Phthiracaroidea, various Euphthiracaroidea and Lohmanniidae, and the enarthronote genus Aploplophora (Mesoplophoridae). 9. Anal plates with interdigitating coaptation zone (pl = without coaptation zone). The anal plates of Malacoangelia possess a short coaptation zone, close to the anterior end, where the closed valves interdigitate (Grandjean 1935a). Those of Nothrolohmannia have a similar structure. Functionally similar, but independently evolved zones of coaptation are found in Phthiracaridae (Wauthy 1984) and Euphthiracaridae (the ‘interlocking triangle’). 10. Leg femora with spinous ventral apophysis (pl = without apophysis). When an individual of Malacoangelia is in defensive posture its legs are folded such that the tarsus, approximately at the level of the antelateral setae, lies behind a small ventral apophysis of the femur. Nothrolohmannia has similar femoral apophyses, and in retracted specimens the folded legs are held in the same way; unlike Malacoangelia, there is also an apophysis on trochanter III, behind which the tip of the tarsus lies. The apophyses therefore serve either in protection, alignment, or both, and seem analogous to the ventral keels that are common on the femora of Lohmanniidae and poronotic Brachypylina. 11. Trochanters I and II with distal, abaxial tectum (pl = without tectum). Trochanters I and II of Malacoangelia are made complex by a lamelliform tectum on the distal abaxial face. This tectum, which appears like a half-collar in lateral aspect, may partially protect the trochanter/femur articulation. Trochanters I and II of Nothrolohmannia have a similar tectum. In various brachypyline mites this articulation is guarded by a retrotectum extending proximally from the femur, but the trochanter type of Malacoangelia and Nothrolohmania seems unique to them. 12. Anterior antelateral seta (a’) of tarsus II hypertrophied, with several branches (pl = setiform, similar to a’ of tarsus I). Several leg setae of Malacoangelia are specialised in being relatively thick, with several prominent barbs or branches. These include v’ of both tarsi I and II, and a’ of tarsus II (but not of tarsus I). The same traits are found in Nothrolohmannia, but not in the outgroups. 13. Proral setae (p) absent from tarsi II and III; p" lost from tarsus IV (pl = proral setae present on all leg tarsi). Grandjean (1935a) suggested that the leg setation of Malacoangelia remigera exactly

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matched that of Hypochthonius rufulus, but there is an important difference. M. remigera consistently lacks the proral setae from tarsi II and III, setae which H. rufulus and most other oribatid mites retain. It also lacks seta p" from tarsus IV in all specimens examined, but p’ is present (usually) or absent. Nothrolohmannia also lacks the proral setae from tarsi II and III and p" from tarsus IV. Seta p’ is present in all specimens examined. Among enarthronote mites, one lineage each of both Mesoplophoridae (lineage XI of Norton 1984a) and Haplochthoniidae (Amnemochthonius; Grandjean 1948) have lost proral setae from tarsi II-IV. However, on tarsus IV the consistent loss of p", combined with the usual presence of p’, is known only in Malacoangelia and Nothrolohmannia. 14. Epicuticule spiculate, with spicules having lumens that are extensions of mineral-filled epicuticular chambers (pl = without noticeable spicules). Malacoangelia differs from its outgroups by having nearly the entire cuticle (articulations, the notogastral porose area and distal region of leg tarsi are exceptions) covered by dense spicules, which cause a matte appearance (Grandjean 1935a). The cuticle of Nothrolohmannia is nearly identical, except the spicules are somewhat larger and more dense (Figs. 2, 3). In each case, the spicule has a lumen continuous with an epicuticular chamber; both are filled with an electron-dense material that appears to be the mineral apatite (Alberti et al. 2001). Epicuticular spicules are unknown elsewhere in oribatid mites, although various taxa have short, tapered cerotegument excrescences that are somewhat similar in external appearance. Some of the characters discussed above, such as the humeral tubercles and the lateral concavities of the prodorsum and pleuraspis, provide Malacoangelia with a facies unique among Enarthronota. But there are other components of this facies. The hysterosoma is relatively broad and short, and most of the notogaster and pleuraspis is made irregular by the presence of depressions or vague ridges. In ventral view, the short legs accentuate the breadth. The anogenital region is relatively short and posteriorly positioned, such that the ano-adanal plates reach the posterior contour of the hysterosoma and even may extend slightly beyond that contour, such that their tip is visible in dorsal aspect. The rosy or orangish yellow color of mature adults is also unusual. Nothrolohmannia shares each of these features. Other characters consistent with the hypothesis

For the hypothesis to be convincing, Nothrolohmannia also should exhibit the derived traits of higher taxa that encompass Malacoangelia. Synapomorphies of Hypochthoniidae (a-g), Hypochthonioidea (h-l), and perhaps of more inclusive groups of Enarthronota (m) are briefly mentioned below in this context (Norton 1984a; Haumann 1991); letter designations distinguish them from characters treated above. Characters a, g, h, j and m were examined only for the new species, since to study them on the single available specimen of N. calcarata would have required its dissection or excessive clearing. a. Alberti et al. (2001) describe the unusual structure of epicuticular chambers in Malacoangelia and Hypochthonius. Although not yet studied in detail, those of Eohypochthonius are probably similar. Thus, Hypochthoniidae probably all share the presence of mineral-filled (probably apatite) epicuticular chambers that form

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as indentations over pore canals. Those of Nothrolohmannia are similar and such chambers are otherwise known only from Lohmanniidae. b. The rutellum of Hypochthoniidae, but not other Hypochthonioidea, is expanded into a hyaline, thin, and apparently rather flexible lobe (cf Grandjean 1935a, b). Nothrolohmannia has the same form of rutellum (Fig. 3c). c. The ultimal pair of setae on the palp tarsus of all Hypochthonioidea are fused. However, in Hypochthoniidae they are joined by the subultimal seta to form a 3–pronged terminal structure. Nothrolohmannia shares this apomorphy. d. Ancestrally in Hypochthonioidea the famulus of tarsus I retains a rather plesiomorphic form, having a lateral bract-like branch. In Hypochthoniidae it has simplified, becoming setiform. Nothrolohmannia shares this apomorphy, though simplification of the famulus is homoplastic in oribatid mites (see discussion by Haumann 1991). e. In oribatid mites the iteral setal pair was ancestrally present on all leg tarsi, and they are always accessory setae, i.e. added after the respective leg is first formed (Grandjean 1941). Some or all iteral setae have been lost in various lineages, and in a variety of patterns that relate to taxa, legs, and instar of development (Grandjean 1961, 1964). Among the rarer patterns is that of Hypochthoniidae, in which iteral setae form on tarsus I but not on tarsi II-IV, and this is the pattern of Nothrolohmannia. f. Ancestrally in oribatid mites, aggenital setae occurred in multiple pairs; most species have lost all but one pair, and some have lost even this. Within Enarthronota the presence and number of aggenital setae is homoplastic (data in Grandjean 1949), but both Hypochthoniidae and Nothrolohmannia lack them. g. An oribatid mite rarely lacks hysterosomal lyrifissure ip, but Hypochthoniidae seem to have lost it. Nothrolohmannia also appears to lack this lyrifissure, although the spiculate and chambered cuticle makes observation difficult. Malacoangelia and Nothrolohmannia also seem to have lost ih but this needs confirmation. h. Hypochthonioidea are unique among Enarthronota in having lyrifissure im inserted on the pronotaspis, rather than on the pleuraspis or in soft lateral cuticle. In Nothrolohmannia, im lies on the dorsal shield, above the pleuraspis and anterior to the indistinct lines representing vestiges of the transverse scissure (see below); therefore it has the apomorphic position. i. Among Enarthronota, Hypochthonioidea are characterised by the lateral fusion of sclerites bearing setae of row e, such that a single intercalary sclerite exists in the transverse notogastral scissure. Although Nothrolohmannia has no scissure, there are vestiges that indicate the apomorphy: two indistinct lines of weakness have paths similar to borders of the intercalary sclerite of Malacoangelia (denoted ct2 and ct3 by Grandjean 1935a, his Fig. 1A). j. An apparent synapomorphy of Hypochthonioidea (present in Hypochthoniidae and Eniochthoniidae, lost in Mesoplophoridae) is that the posterior coxisternal plate (fused coxisterna III/IV) possesses a sternal apodeme. It runs posteriorly from the sejugal

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articulation, ending just beyond the level of leg III, but is sometimes (Malacoangelia) divided into two short sections. The apodeme is made more noticeable by its isolation from the short apodemes arising from the leg insertions. Nothrolohmannia has such a sternal apodeme, as do Lohmanniidae (to be discussed elsewhere). For Heterochthoniidae a similarly placed structure is sometimes drawn, but it represents a medial band of cuticle lacking muscle sigillae, which is therefore slightly darker in transmitted light; there is no true apodeme. k. In Hypochthonioidea the aggenital plates fuse broadly and imperceptibly with coxisterna IV and the same is true of Nothrolohmannia. Haumann (1991) used this fusion as the sole justification for a clade that includes Hypochthonioidea, Heterochthoniidae and Arborichthoniidae, but this is incorrect. Aggenital plates of Heterochthoniidae fully articulate with coxisterna IV, except perhaps at their anterolateral extremity, and the aggenital region of Arborichthoniidae is sclerotised only posterior to the aggenital seta. l. Ancestrally, Hypochthonioidea have a characteristic adoral seta or2. Distally, it is expanded and unilaterally pectinate, with teeth directed medially (Norton 1984a); just basal to this, there is a distinct lateral notch that sets off a relatively large tooth (cf. Grandjean 1957, his Fig. 1C). Nothrolohmannia shares this form (Fig. 3c). m. Nothrolohmannia has a preanal plate—despite the statement by Balogh (1968) to the contrary—which is consistent with membership in Hypochthonioidea (Norton 1984). As in Malacoangelia (Grandjean 1935a), the plate lies in the vertically directed cuticle between anal and genital apertures. In ventral aspect it is overhung by the genital plates and is visible only by dissection. In addition to Hypochthonioidea, two other enarthronote families are known to have a preanal plate—Cosmochthoniidae and Heterochthoniidae (wrongly considered by Norton 1984 to lack a preanal plate; see Grandjean 1928, 1962) — but the relationships among these taxa are poorly understood. No species of Palaeosomata is known to have a preanal plate, but such a plate or its derivative (preanal organ) occurs in all Lohmanniidae and is common in more derived (i.e. ‘glandulate’) oribatid mites, and some amount of homoplasy is likely. Nothrolohmannia as a member of Crotonioidea

Balogh and Balogh’s (1992) transfer of Nothrolohmanniidae from Lohmannioidea to Desmonomata (superfamily Crotonioidea) is difficult to understand, and they offered no supporting discussion. Desmonomata are rather derived oribatid mites and possess a number of apomorphic traits that collectively argue against inclusion of Nothrolohmannia. First, Nothrolohmannia has a dichoid body form, as found in most Enarthronota. The broad sejugal articulation lends considerable independence of movement to the hardened proterosoma and hysterosoma. By contrast, Desmonomata are holoid, with fusion between coxisterna II and III. Malaconothridae are exceptional in having a narrow sejugal band of soft cuticle that allows for slight dorsoventral flexure; this may be a paedomorphic trait (Norton 1998). Second, the gnathosoma of Nothrolohmannia is generally plesiomorphic, typical of most Enarthronota, and is unlike that of Desmonomata (cf Grandjean 1957). For example, the rutellum does

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not have a broad base or a rutellar brush on its dorsal surface. The subcapitulum is anarthric, not stenarthric as in nearly all Desmonomata (Norton 1998). The chelicera is slender, without Trägårdh’s organ. In Desmonomata it is heavily built, and almost always possesses Trägårdh’s organ. The palp tarsus is fully articulated with the tibia; in Desmonomata the tibia is fused to the tarsus dorsally (Norton 1998).

jean 1935a, his Fig. 1C), was counted as a seta of coxisternum III. Thus, there is no reason to place Nothrolohmannia at the base of Holonota. Moreover, the principal reason to include it in Holonota becomes its undivided notaspis, since the famulus shape is made insignificant by its highly homoplastic nature.

Other plesiomorphic traits of Nothrolohmannia that are inconsistent with membership in Desmonomata include the retention of two pairs of exobothridial setae (at least one pair lost in Desmonomata) and the independence of leg genua solenidia from respective setae d (coupled in Desmonomata). Nothrolohmannia also has no paired lateral opisthonotal gland. This is absent in the two most primitive major oribatid mite groups, Palaeosomata and Enarthronota, but present in nearly all Desmonomata (Grandjean 1969; Norton 1998).

Balogh’s (1972) original opinion, that Nothrolohmannia is closely related to Lohmanniidae, is more difficult to dismiss than are the two ideas just discussed. With the absorption of Xenolohmannia into Lohmanniidae (see above), the question becomes: is Nothrolohmannia (i.e. Nothrolohmanniidae) the sister-group of Lohmanniidae? Since the proposal of Nothrolohmanniidae, only Lee (1985) has presented a detailed list of characters purportedly shared by all Lohmannioidea. (The latter is the sole superfamily in Afissurida, one of Lee’s five suborders of oribatid mites.) But, like Haumann (1991), he did not study specimens of Nothrolohmannia.

Last, Nothrolohmannia lacks opisthosomal lyrifissures ian and iad or the homologous cupules. Both pairs exist in nearly all ‘glandulate’ oribatid mites (Parhyposomata, Mixonomata, Desmonomata and Brachypylina). Their consistent absence in all Palaeosomata and Enarthronota (Grandjean 1969) is enigmatic, since a pair of cupules or lyrifissures is typically considered part of the plesiomorphic set of structures on an acariform mite opisthosomal segment (e.g. Evans 1992). However, one might argue from a strict outgroup comparison that the presence of ian is a synapomorphy of glandulate oribatid mites; even though some endeostigmatic mites possess iad, none are known to have ian (Kethley 1990). In such a context, Malacoangelia lacks the apomorphy. Nothrolohmannia as the earliest derivative of Holonota

Haumann (1991) proposed a new use for the higher group name Holonota, which was paraphyletic in its original composition (Balogh 1972). It approximately equals the Mixonomata + Nothroidea + Circumdehiscentiae of Grandjean (1969). Haumann recognised but two synapomorphies; the holonotic condition (i.e. a notaspis without transverse scissures) and a simple, setiform famulus. Nothrolohmannia has both these traits, although Haumann did not know the nature of the famulus (specimens were not studied). He was unable to resolve the relationships of most higher taxa within Holonota, but did isolate Nothrolohmannia as the earliest derivative member. As support for this basal position of Nothrolohmannia, Haumann (1991) cited a single synapomorphy of all remaining Holonota: the presence of a single pair of setae on coxisternum II. Nothrolohmannia was thought to have a plesiomorphic setation of two pairs, but Balogh’s (1968) description and illustration were incorrect on this point. Rather than the published coxisternal formula of 3-2-4-3, N. calcarata (and Nothrolohmannia n. sp.) has a setation of 3-1-3-4, identical to that of Malacoangelia. Balogh’s error in the coxisternum II setation derives from two separate misidentifications. He counted (and illustrated in his Fig. 2) the large subcapitular seta h as a coxisternal seta, and he counted seta 1c (which has its normal position just anterior to the insertion of leg I) as a seta of coxisternum II. The error in the last two numbers of Balogh’s formula derives from a common mistake. Seta 4b, which usually has a very anterior position on coxisternum IV (cf Grand-

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Nothrolohmannia as a member of Lohmannioidea, and the relationships of Lohmanniidae

The characters of Lohmannioidea cited by Lee (1985) fall into two apparent groups. The first includes traits that are not specific to Lohmannioidea; with one exception, they are also found in Hypochthonioidea and in many cases are even more generally distributed. They include the following (Lee‘s terminology is translated to that of F. Grandjean, which is more generally used): paired opisthonotal gland absent; notogastral setation holotrichous or neotrichous; two pairs of exobothridial setae; coxisterna fused to form two plates (pairs I/II and pairs III/IV); Trägårdh’s organ absent; rutella primitive; subcapitulum without labiogenal articulation; leg pretarsi monodactylous; tarsus I with two solenidia; tibia I solenidion flagellate; femora undivided; immature instars similar to adult. The exception noted above is the absence of transverse notogastral scissures; this absence is a general feature of more highly derived oribatid mites, but it is not found in Hypochthonioidea in the context used by Lee. The second group includes two traits that are true of Lohmanniidae, but not of Nothrolohmannia: adoral setae in transverse row, at least the two adaxial pairs being large, flattened (neither is true of Nothrolohmannia); leg genua with two solenidia (there is only one in Nothrolohmannia). None of the traits listed by Lee can be considered a synapomorphy that supports a sister-group relationship between Lohmanniidae and Nothrolohmannia. He did not mention the presence of pedofossae, since the trait was not included in the original description of Nothrolohmannia. Nor did he note the multiple porose areas on the notogaster of Nothrolohmannia and some Lohmanniidae, which are superficially similar, but ultrastructurally different (Alberti et al. 1997, 2001). Faced with the long list of synapomorphies that support a sister-group relationship of Malacoangelia and Nothrolohmannia, the original classification of Balogh (1972) has to be rejected. But that does not mean the relationship of these taxa with Lohmanniidae is a distant one. The relationships of Lohmanniidae has been one of the more interesting and enigmatic problems in oribatid mite systematics. Grandjean (1950b) had discussed the family’s possible phylogenetic ties to Enarthronota, though he later (1969) included these

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Figure 4

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Relationships and body forms in Hypochthonioidea. (a) Cladogram of hypochthonioid families and genera of Hypochthoniidae, suggesting new position of Nothrolohmannia (see text for explanation). (b-e) Schematic lateral views of (b) Hypochthoniidae (except Nothrolohmannia), (c) Nothrolohmannia, (d) Eniochthoniidae, (e) Mesoplophoridae. Setae are represented by dots. The asterisk (*) in d, e indicates comparable points on the tectum of the type-L transverse scissure.

mites in Mixonomata, despite their lacking the opisthonotal glands. The former idea also seems apparent, though not explicitly stated, in his (1953) benchmark treatment of oribatid mite classification: he placed Lohmanniidae immediately after Enarthronota in a list of 11 major taxa that was ostensibly arranged from more primitive to more derived. In a sequenced classification of oribatid mites that included five suborders, Lee (1985) inferentially linked Lohmanniidae with enarthronote mites by inserting Afissurida between two other suborders (his Retrofissurida and Profissurida) that, collectively, equal Enarthronota. A cladistic analysis of the relationships of Lohmanniidae is being developed separately, and the results will be of interest for several reasons. In the present context, if Lohmanniidae are members of Enarthronota then these mites also have lost the notogastral scissures. In a broader context the family has an enigmatic mixture of primitive and specialised traits, it shows considerable internal variation in form (Grandjean 1950b), and it has considerable taxonomic diversity (Balogh and Balogh 1992). Further, lohmanniid mites are abundant and probably ecologically important decomposers of plant residues, especially in tropical systems. Last, they

are of evolutionary interest as one of the large groups of oribatid mites in which sexual reproduction is unknown (Norton and Palmer 1991). New status for Nothrolohmanniidae

If Nothrolohmannia and Malacoangelia are sister taxa, several family-level classifications are possible. Nothrolohmanniidae could be transferred to Hypochthonioidea, leaving Hypochthoniidae with its current constitution (Hypochthonius, Eohypochthonius, Malacoangelia). This is unacceptable since Hypochthoniidae would be paraphyletic. Alternatively, Nothrolohmannia could be included among the Hypochthoniidae, with Nothrolohmanniidae being abandoned. Third, the family-group name Nothrolohmanniidae could be retained to include both Nothrolohmannia and Malacoangelia, either as a sister family to Hypochthoniidae, or as a subfamily within Hypochthoniidae. The latter classification seems to be the best compromise (Fig. 4a), considering the small number of genera involved, yet the considerable differences between Malacoangelia and Nothrolohmannia on the one hand, and Hypochthonius and Eohypochthonius on the other.

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EVOLUTIONARY PLASTICITY OF BODY FORM IN ENARTHRONOTA If the hypothesis developed above is true, Nothrolohmannia has lost the transverse scissures that otherwise characterise Enarthronota. Some other examples of body form diversification to be discussed below involve such losses (i.e. fusion between previously existing plates), but specialisations of scissures are also important. Grandjean (1947) recognised three basic types of transverse scissures in Enarthronota, and no other type that is substantially different has been discovered since. Scissure types, function, and distribution

The ‘type-E’ scissure of Grandjean (1947) is a simple articulation between plates (Fig. 1h, i). Edges of the two adjacent plates are unmodified, and the intervening band of soft cuticle is usually narrow. Small body volume changes can therefore be accommodated by dorsoventral flexure between the plates. If the scissure is wide enough to allow telescoping action (e.g. in Brachychthoniidae), then its soft cuticle seems exposed to potential predators. A specialisation that permits significant telescoping of two plates, while protecting a broad articulating cuticle, is what Grandjean called a ‘type-L’ scissure. One plate edge (in known species this is always the posterior edge of the more anterior plate) is hypertrophied as a tectum with a limb broad enough that no soft cuticle is exposed, even at maximum plate separation (Fig. 1j, k). A very different specialisation, the ‘type-S’ scissure of Grandjean, is actually a compound structure (Fig. 1l-n). In its typical form, the space between two major plates is occupied by a transverse series of four closely adjacent intercalary sclerites, each bearing a seta. These intercalary sclerites can be variously combined, depending on the taxon (Fig. 5). The setae in the scissure usually are hypertrophied and erectile, a trait first noted by Michael (1888) for Cosmochthonius. The mechanism of erection is poorly known, but it seems consistent that setae move in concert, rather than being controlled individually. Grandjean (1931, 1948) envisioned an indirect action in which distension of the hysterosoma caused straightening of an otherwise folded scissure. Setae on an intercalary sclerite point posteriorly when the scissure is folded, and dorsally when the scissure is straightened (Fig. 1m). This opinion derived from the fact that the full range of motion could be induced in preserved specimens as the state of distension was varied by manipulating the fluid observation medium. In the only direct anatomical study known to me, Gerd Alberti (personal communication 1998) found muscles that could act directly on the sclerites bearing the erectile setae of Heterochthonius gibbus Berlese. In Enarthronota, when type-S scissures exist they usually bear the four setal pairs in rows e and f. Rarely (Atopochthonius) a single row (f) is erectile, and in Heterochthonius a third row (d) has been suspected of being erectile (Grandjean 1928). The ancestral distribution of plates and scissures in Enarthronota is not known precisely, but there is evidence that erectile setae appeared early in enarthronote evolution. The oldest oribatid mite fossils, from the Devonian of New York, are enarthronotes representing two extinct families (Norton et al. 1988). The presence of notogastral plates or intercalary sclerites cannot be veri-

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fied, but in each species setal rows e and f are hypertrophied, consistent with their being erectile. Among extant Enarthronota, these setae are always erectile if they are hypertrophied, distinctly longer and thicker than other setae. Erectile setae are also widely distributed among the various extant lineages, which suggests that they existed early (Weigmann 2001). Erectile setae occur in ctenacarid Palaeosomata, but they insert on poorly defined sclerites that are not in distinct scissures, and erectility probably evolved independently from that in Enarthronota, for two reasons. First, only pair e1 is erectile in both groups; other erectile setae belong to non-homologous pairs. Second, the setae of more basal Palaeosomata (Archeonothroidea) are not known to be erectile, though they often are hypertrophied. On the basis of unpublished observations, erectile setae probably have a defensive function. When living adults of Gozmanyina majesta (Marshall and Reeves) are undisturbed, the large, leaf-like setae of rows e and f lie prone; when disturbed by a passing ant or beetle, or by a brush, the setae snap quickly erect. Setae f of Atopochthonius artiodactylus Grandjean respond similarly to these stimuli. So do pairs d2 and e1 of the ctenacarid Palaeosomata Beklemishevia sp. and Ctenacarus araneola Grandjean; these setae have more independent action than those of Enarthronota, and can be directed somewhat laterally, as well as dorsally. Given the early-derivative position of Enarthronota and Palaeosomata, erectile setae were probably the first morphological adaptation for predator defense in oribatid mites. Based on the nature of scissures, extant enarthronotes with two rows of erectile setae fall into two groups. One is loosely referred to herein as the Trichthonius-form, in which three principal dorsal plates are separated by two type-S scissures, respectively bearing setal rows e and f (Fig. 5a). Examples are the unplaced genera Trichthonius and Gozmanyina, which have four intercalary sclerites in each scissure; Nipponiella (another unplaced genus) and Arborichthoniidae are similar, but the intercalary sclerites are modified (Fig. 5b, c). Two other families, Heterochthoniidae (Fig. 5d) and Cosmochthoniidae (Fig. 5e), have a similar morphology but additionally have a type-E scissure between setal rows c and d; herein, this is referred to as the Cosmochthonius-form. At present, no strong evidence supports either form being ancestral to the other. Most members of Enarthronota (Brachychthoniidae and Atopochthonioidea are the possible exceptions) have one of these two forms, or seem derived from ancestors that had one of them. A majority of nominal enarthronote genera, 28 of 47, are included in one of two superfamilies, Hypochthonioidea or Protoplophoroidea, and how their morphological diversity evolved from such plesiomorphic forms, which are ancient yet specialised for defense, is discussed below. Body form evolution in Hypochthonioidea

The monophyly of Hypochthonioidea is well supported and its internal relationships (Fig. 4a) are reasonably well known (Norton 1984a and above), but the identities of its closest relatives are not established with confidence. Haumann (1991) used incorrect information about ventral plate structure (see character k, above) in proposing Heterochthoniidae as the sister-group, but another

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Figure 5

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Schematic dorsal hysterosoma of Enarthronota, showing the distribution of scissure types (only the most dorsal setae are indicated by dots, identified in (k). (a) Trichthonius. (b) Nipponiella. (c) Arborichthonius. (d) Heterochthoniidae. (e) Cosmochthoniidae. (f) Sphaerochthoniidae, Protoplophoridae. (g) Haplochthoniidae. (h) Pediculochelidae. (i) Hypochthoniidae (except Nothrolohmannia). (j) Eniochthoniidae. (k) Nothrolohmannia. (l) Brachychthoniidae.

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character suggests the same relationship. Heterochthoniidae and Hypochthonioidea, but no other known enarthronotes, have a porose bothridial wall (see above, character 4). There are other reasons to consider Arborichthoniidae as a close outgroup (Norton 1984a). Therefore, we can assume that the ancestors of Hypochthonioidea had the two type-S scissures but the ancestral presence of an additional type-E scissure is equivocal; there is no vestige of it in the group. Body form in Hypochthonioidea has evolved along two strikingly different paths. Of the four extant forms, the one prevalent in Hypochthoniidae is the most plesiomorphic (Fig. 4b). Only the anterior type-S scissure remains in this form; the posterior scissure is lost, without vestige, by fusion of adjacent plates. The intercalary sclerites of the middle scissure have fused laterally, to form a single, narrow sclerite (Fig. 5i). Rather than supporting large erectile setae (setal row e is small or vestigial) the intercalary sclerite seems to provide structural support for the scissure. In Hypochthoniinae the intercalary sclerite is usually hidden by the overhanging anterior plate, although there is no tectum formed. In Malacoangelia the sclerite is relatively broader and more exposed. In each case, the breath of the scissure suggests that it is important in allowing changes in hysterosomal volume. The evolution of body form in Hypochthoniidae seems closely linked with mineralisation of the cuticle, which increases cuticular rigidity and, probably, decreases penetrability. In most respects, Hypochthonius is the least specialised of the Hypochthoniidae. In this genus mineralisation occurs on the main cuticular plates (e.g. prodorsum, notaspis) as localised patches of small chambers that are filled with calcium phosphate, probably in the form of apatite (Alberti et al. 2001). These patches lie above the insertions of powerful muscles (e.g. cheliceral retractors, dorsoventral muscles of the hysterosoma), which suggests that they increase rigidity at these points of stress. In adults of other Hypochthoniidae, the distribution of mineral-filled chambers has expanded to cover all exposed plates. Since the general form and behaviour of adults and immatures are similar, the more complete mineralisation is best interpreted as a predator defense, rather than as increased skeletal support. (There is an analogy with the evolution of sclerotisation in oribatid mites, which may have originated as support-providing patches on an otherwise soft cuticle (e.g. Acaronychidae, Fig. 1b), but then expanded to large plates as protection from predation.) If the cladogram in Fig. 4a is correct, the expansion of mineral distribution probably occurred independently in Nothrolohmanninae and in Eohypochthonius. (Immatures of Eohypochthonius have localised chambers, like those of Hypochthonius; immatures of Nothrolohmanniinae have not been studied for this character). As discussed above, many of the unique traits of Nothrolohmanniinae seem to have evolved in relation to a predator defense based on the impenetrability of exposed cuticle and the effective covering of articulations, in particular the sejugal one. The transverse notogastral scissure of Malacoangelia seems to have been a weak point that was eliminated by Nothrolohmannia, which has evolved the dichoid body form to its most effective armoured state (Fig. 2, 3, 4c, 5k). Any advantage of retaining the scissure, e.g. in terms of hysterosomal volume control, seems to have had lesser importance.

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The sister-group of Hypochthoniidae ( Eniochthoniidae + Mesoplophoridae) modified the scissure in a different way, one that had even greater consequence for the evolution of body form. This lineage retained the volume control provided by the scissure, and probably increased it by broadening the articulating band, but by evolving the type-L form the scissure is fully protected. The simplest explanation is that the anterior edge of the intercalary sclerite fused with the anterior plate (which now carries setae e), and the posterior edge of the sclerite expanded to form the tectum. In its most plesiomorphic form this is represented by the monobasic family Eniochthoniidae (Fig. 4d, 5j). As discussed below, the large volume control afforded by such a protected, telescoping articulation probably had much to do with the evolution of its diverse sister-group, the Mesoplophoridae. Both families have a fully mineralised cuticle, but the chambers are structurally different from those of Hypochthoniidae and are filled with calcium oxalate instead of calcium phosphate (Alberti et al. 2001). Mesoplophoridae are characterised by a ptychoid body form (Fig. 4e). While the general appearance is similar to that of the better known ptychoid Mixonomata (e.g. Phthiracaridae, Euphthiracaridae), their body structure is quite different. In Mesoplophoridae the anterior notogastral plate, carrying only setal rows c, d and e, has expanded to cover the dorsal half of the hysterosoma, and the posterior plate (carrying all other ‘notogastral’ setae) has regressed to a similar extent. Ptychoidy is often compared to a folding ‘jackknife’ or to conglobation (rolling into a defensive ball), an adaptation that evolved convergently in many animal lineages. But it is perhaps better compared to the defensive morphology of snails, in which parts of the body that are external when the animal is active are, upon disturbance, withdrawn into a secondary cavity after which a hardened operculum (like the prodorsum of ptychoid mites) covers the opening. The pulling inward of legs and the surrounding podosomal cuticle must require a significant volume displacement in the hysterosoma of a ptychoid mite. To compensate, there must be an expansion in some other location, but one that does not expose soft cuticle. The mechanics have not yet been carefully studied, but the telescoping type-L scissure appears to be the place for such volumetric adjustment. When the mite returns to activity, the legs and podosoma are forced out of the hysterosoma. It seems likely that a contraction of the scissure is responsible for ‘inflating’ the podosomal cuticle. Further, the soft podosomal cuticle must provide little support for the coxisterna when legs are active, and perhaps the continual contraction of the scissure is mostly responsible for maintaining a ‘hydrostatic skeleton’ in the podosomal region. The mineralised cuticle of these mites probably plays two roles: contributing a rigid framework that optimises hydraulic efficiency, and making the general cuticle more difficult for predators to penetrate. While all Mesoplophoridae have a ptychoid body form, and all have a similar type-L scissure, there is considerable variation in how the ventral plates of the hysterosoma have become associated and fused (Norton 1984a). As in the Nothrolohmanniinae, the extensive development of mineralised cuticle seems to combine with fusion of plates to create an effective armour.

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Body form evolution in Protoplophoroidea

The five families of Protoplophoroidea exhibit as much body form diversity as does Hypochthonioidea, though the details are quite different. The relationships of these families, most members of which inhabit arid regions or dry microhabitats, were analyzed by Norton et al. (1983) and are illustrated in Fig. 6. The Cosmochthonius-form (Fig. 5e) exists in all known members of Cosmochthoniidae, and seems ancestral in the superfamily. Other forms may have derived from it, as discussed below. One lineage presents an excellent analogue with the hypochthonioid families Eniochthoniidae and Mesoplophoridae. In Sphaerochthoniidae, both type-S scissures have fused to the major plates, and in some cases suture-like vestiges are present (Fig. 5f). The anterior scissure has been modified from its plesiomorphic type-E form to a telescoping type-L form, and the anterior plate (bearing only setae of row c) is hypertrophied to encompass about half the hysterosomal dorsum. The resulting body form is functionally similar to that of Eniochthonius, although the tectum evolved from a different ancestral scissure. More interesting is that Protoplophoridae, the presumed sister family of Sphaerochthoniidae, is ptychoid, just as the sister-family of Eniochthoniidae (i.e. Mesopolophoridae) is ptychoid. The type-L articulation in Sphaerochthoniidae may have evolved as a simple defensive covering of the single functional hysterosomal scissure but, like that in Hypochthonioidea, it provided the mechanism needed to operate the more effective ptychoid body form. The anterior plate of Protoplophoridae is smaller than that of Mesoplophoridae, but there is analogous variation in the associations and fusions of ventral plates (Grandjean 1932, 1954a). Cuticular mineralisation is present in at least some Protoplophoridae, though it has been studied much less than in Hypochthonioidea and information is highly fragmentary. Adults of some, but not all, Protoplophoridae have birefringent cuticles and in at least one genus (Prototritia) this results from calcium oxalate deposition (Norton and Behan-Pelletier 1991a). Among the outgroups, at least one genus of Cosmochthoniidae (Phyllozetes), has large, thin, birefringent epicuticular plaques (Norton and BehanPelletier 1991b; Alberti et al. 2001). Other members of the family show no birefringence. At least one Australian species of Sphaerochthoniidae (Sphaerochthonius sp.) has rather large, birefringent cuticular plaques (unpublished observation), but most species do not. Since some minerals (e.g. calcium phosphate) show little or no birefringence, and since no ultrastructure information is available for non-birefringent members of these families, no relevant conclusions can be drawn. A lineage of Protoplophoroidea with a very different evolutionary history comprises the families Haplochthoniidae and Pediculochelidae (Fig. 6). Grandjean (1947) saw the rather simple and segmentally arranged hysterosomal dorsum of Haplochthoniidae (Fig. 1h, 5g) as primitive and, to some extent, he used the family as a paradigm of generalised body form in Enarthronota. He viewed the weaker, more restricted sclerotisation of plates in adult Amnemochthonius, the second nominal genus of Haplochthoniidae, as more primitive than the rather complete sclerotisation of adult Haplochthonius. He also considered the striated, unsclero-

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tised cuticle of immatures in both genera to be an ancestral state; perhaps his rationale was that endeostigmatic mites lack noticeable plates in all instars, while most enarthronote immatures possess plates to some extent. But other characters are more consistent with a different hypothesis, that each of these traits is secondary (Norton et al. 1983). How could the simple plates and setal arrangements of Haplochthoniidae evolve from the Cosmochthonius-type body form? Grandjean himself (1947, 1948, his Figs. 2C, 1A, respectively) first noticed that in Haplochthoniidae setal rows e and f are not in the midst of the respective plates, but are very close to their anterior borders, which are usually emarginate near the setae. He questioned whether this arrangement represented incomplete sclerotisation or an early step in the movement of the setae into the scissure (i.e. a precursor to erectile setae). But the close relationship of Haplochthoniidae and Cosmochthoniidae suggests the reverse: setal rows e and f are near the type-E scissures because they were ancestrally on small intercalary sclerites that have fused to the plate behind them (Fig. 5g). This origin would then be quite different from that of the type-E scissures in Brachychthoniidae (‘coupures’ ar2, ar3; Fig. 5l), which Grandjean (1947) had considered homologous. Although larval Cosmochthonius have not yet been described in detail, Grandjean (1931) noted that they have no separate intercalary sclerites; perhaps some type of paedomorphosis was involved in the transition to the haplochthoniid body form. Many other features of Haplochthoniidae appear to be regressive, and can best be explained as paedomorphic (Norton et al. 1983). Especially in terms of sclerotisation and setation, Amnemochthonius is clearly paedomorphic with respect to Haplochthonius. Pediculochelidae seem aberrant as enarthronote mites, and in the past this family was considered variously as a member of Astigmata, Endeostigmata or Heterostigmata. However, their soft, striated hysterosomal cuticle and grooves between certain setal rows, which are not always in accordance with scissures of adult haplochthoniid mites (Figs 5h, 6), are traits found in haplochthoniid immatures (Grandjean 1947, 1948). Overview of trends

Considering the above discussion, two points seem especially noteworthy. First, the evolution of body form diversity in Hypochthonioidea and Protoplophoroidea is reminiscent of how ancestral arthropod lineages purportedly organised different body regions from a series of similar segments. Euphemistically, the evolutionary story of Enarthronota is one of ‘reinventing tagmosis.’ Second, for the most part this diversity did not originate from a simple, serial pattern of transverse dorsal scissures and sclerites. Rather, the antecedent of these many body forms seems to have been the rather specialised Trichthonius- or Cosmochthonius-form, the principal feature of which is defensive erectile setae. Several trends seem to have emerged from this ancient defensive morphology. One is the abandoning of erectile setae and the evolution of more effective cuticular armour. With heavier sclerotisation, or more effective mineralisation, came a fusion of unprotected scissures. Vestiges of scissures can be found in Nothrolohmanniinae, Sphaerochthoniidae and Protoplophoridae, but in other cases

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Figure 6

Relationships of families in Protoplophoroidea (concept from Norton et al. 1983; figures modified from Grandjean 1932, 1947; Krantz 1978; Lee 1982).

Except in Hypochthoniidae, the single retained scissure is a telescoping, type-L scissure. Perhaps due to the volume control it affords, this seems to have been a precondition favorable for what can be considered a second trend (or a continuation of the first): the evolution of ptychoidy. Cuticular mineralisation also may have favored the evolution of ptychoidy in each lineage, though much remains to be learned about the distribution of this trait in Protoplophoroidea. In both superfamilies, taxa with the transitional morphologies (Eniochthoniidae and Sphaerochthoniidae) are homogeneous, while the derivative ptychoid families (Mesoplophoridae and Protoplophoridae respectively) are morphologically diverse. The variety of ventral plate structures in the latter two families (Grandjean 1932, 1954a; Norton 1984) may represent evolutionary ‘experimentation’ with morphologies that improved predator defense, hydrostatic efficiency, or both.

tions of cuticular plates that might promote ptychoidy, but one that he did not mention is some mechanism to allow large changes in body volume. The two ptychoid enarthronote families rely on telescoping, type-L scissures for the control of body space and internal pressure. One family of ptychoid Mixonomata, the Phthiracaridae, has a facies superficially similar to that of Mesoplophoridae, and may function in an analogous way. A broad articulating cuticle lies between the anogenital plates and the notogaster of phthiracarid mites, and a large tectum overhangs this articulation from the notogastral margin. The levation and depression of the anogenital plates may be motions analogous to the contraction and expansion of a type-L scissure. In the other group of ptychoid Mixonomata, Euphthiracaroidea, a rather different mechanism involving lateral compression and relaxation of the notogaster seems to operate (Sanders and Norton, in preparation). There have been a variety of fusions among ventral plates of euphthiracaroid mites (Haumann 1991, Norton and Lions 1992), analogous to those seen in Mesoplophoridae and Protoplophoridae. Cuticular mineralisation (in the form of calcium carbonate) also is widespread in ptychoid Mixonomata (Norton and Behan-Pelletier 1991a), but is not known from dichoid members of the group.

The apparent convergences during the evolution of ptychoidy in Enarthronota can also be looked for in ptychoid Mixonomata. Grandjean (1969) discussed several possible pre-existing condi-

A third trend, paedomorphosis, seems restricted to Protoplophoroidea (Haplochthoniidae and Pediculochelidae). These taxa have eliminated one pre-existing predator defense – erectile setae – and

fusions have to be inferred. In Nothrolohmanniinae all transverse scissures were lost, and the same may be true of Lohmanniidae, should these be shown to be enarthronote mites. In most cases, however, a single functional scissure has remained, and why this is true is unclear. Retention of some hysterosomal flexibility and volume control is a possible explanation, but most oribatid mites lack hysterosomal articulations and pay no obvious costs.

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reduced or eliminated another – sclerotisation. The benefits of this trend are not yet understood. Body form diversity and classification

Oribatid mite classifications have long been perceived as being both over-split and over-ranked (‘upgraded’ or ‘top-heavy’; e.g. Krantz 1978) and probably no group has contributed as much to this perception as has Enarthronota. The concerns seem to be of two types, one being whether the classification itself is a source of information. For enarthronote mites the classifications of Woolley (1958) and Balogh and Mahunka (1979) provide good contrast. The former classification lumps all Enarthronota (except the ptychoid mites) under one family. In the latter, the number of superfamilies almost equals that of families (all but one superfamily is monobasic), such that redundancy is almost complete. In each case, relationships among enarthronote families and their amazing evolutionary histories – of which Grandjean taught us much in the 1940s and early 1950s – are masked. The second concern relates to explanatory or predictive studies of biodiversity (Zhang 1996; Athias-Binche 1997). If Oribatida is ranked internally in a way inconsistent with other comparable groups, then mathematical models that analyse historical trends or predict future results may be rendered ineffectual. What criteria make a classification reasonable? A well-supported phylogeny is the starting point, but subjectivity is still inherent in converting a tree topology into a Linnean hierarchy. We must decide which clades to recognise and what rank to assign them. As in ‘pre-Hennigian’ times, we still seek morphological gaps to help us make the first of these choices, and among oribatid mites perhaps no type of gap is more obvious or impressive than a difference in body form or other aspects of cuticular plate arrangements. The redundant classification of Balogh and Mahunka (1979) was a historical culmination of such emphasis, and this is even reflected in the one nominal superfamily that was not considered monobasic. The Atopochthonioidea (= Phyllochthonioidea) comprises three families whose body forms are not strikingly different. But these mites differ greatly in many other aspects of their morphology – more so than within any other named superfamily in that classification – to the extent that their monophyly is questionable. A reasonable Linnean classification is a compromise that best encapsulates diversity within a group and the relationships among its members. Of the cited extremes, Woolley’s (1958) classification did neither and Balogh and Mahunka’s (1979) stressed differences at the expense of relationships. If body form is an evolutionarily plastic trait, it is not unreasonable to include dichoid mites – both holonotic and arthronotic (with transverse scissures) – in the same superfamily as ptychoid mites. To the contrary, such a grouping (e.g. Hypochthonioidea in the current sense) serves to emphasise the plasticity. At a lower level, the same logic applies to the two ptychoid enarthronote families. Their history is so parallel that one might consider ptychoidy as an evolutionary canalisation, an inevitability, if the immediate ancestor had a telescoping, type-L scissure and cuticular mineralisation. It is the most effective defensive body

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form if these traits exist. But each family was evolutionarily plastic in how lateral and ventral cuticular plates – those posteroventral to the type-L scissure – were modified after the attainment of ptychoidy. So far, there has been no attempt to elevate genera of Protoplophoridae to redundant, monobasic families. By contrast, in Mesoplophoridae the analogous plasticity has caused some authors to do just this (e.g. the proposals of Archoplophoridae and Apoplophoridae), rather than allow intrafamilial variation in the arrangement of ventral plates. If we recognise Protoplophoridae, Lohmanniidae, Oribotritiidae, and other families with a diversity of ventral plate fusions, then why not recognise a broad sense of Mesoplophoridae as well? In quantifying a generally-perceived problem, Athias-Binche (1997) found the distribution of taxa within oribatid mites to be incongruent with that in other mite suborders. Why is this so? As emphasised by Zhang (1996 and included references), patchiness in the richness and diversity of recognised taxa (and their traits) can be due both to the natural results of evolution and to human bias. Certainly, natural patchiness can be expected in a group as old as Oribatida; there are many relictual taxa that either never became diverse or that lost most of their diversity by extinction. But we also have significantly misrepresented the group’s taxonomic, morphological and biological diversity, in two ways. First, diversity has remained undiscovered as a result of wrong hypotheses about relationships. The past failure to include Nothrolohmanniia within Hypochthoniidae (above), or the failure to include Pediculochelidae in Protoplophoroidea , or the failure to recognise Astigmata as a clade within the ‘lower’ oribatid mites (cf Norton 1998) are examples. Second, diversity has been masked by some poor choices about which clades to recognise and what rank to give them. As we continue to improve in each endeavor, the Oribatida will seem less problematic.

ACKNOWLEDGEMENTS Drs Matthew Colloff and Bruce Halliday (CSIRO Entomology, Canberra) provided research facilities and access to specimens in the Australian National Insect Collection. I am grateful to Dr Halliday and to CSIRO for the support of a Sir Frederick McMaster Fellowship during which most of this work was accomplished. The study would not have begun without the help and generosity of Prof. János Balogh, during a visit to Budapest. Prof. Gerd Alberti (University of Greifswald, Germany) kindly shared unpublished information on various mites discussed above, and Sue Lindsay (The Australian Museum, Sydney) provided the scanning electron micrographs. For helpful specimens or discussions I thank Drs Valerie Behan-Pelletier (Agriculture and Agri-food Canada, Ottawa), Ziemowit Olszanowski (Adam Mickiewicz University, Poznan), David Walter (University of Queensland, Brisbane) and Andreas Wohltmann (Freie Universität, Berlin). Dr Behan-Pelletier also provided constructive comments on the manuscript. I am grateful to Dr G. W. Krantz (Oregon State University, Corvallis) and Jenni Thurmer (South Australian Museum, Adelaide) for arranging permission to reproduce parts of Fig. 5.

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REFERENCES Alberti, G., Norton, R. A., Adis, J., Fernandez, N. A., Franklin, E., Kratzmann, M., Moreno, A. I., Weigmann, G., and Woas, S. (1997). Porose integumental organs of oribatid mites (Acari, Oribatida). 2. Fine structure. Zoologica (Stuttgart) 146, 33–114. Alberti, G., Norton, R. A. and Kasbohm, J. (2001). Fine structure and mineralization of cuticle in Hypochthonioidea and Lohmannioidea (Acari: Oribatida). In ‘Acarology: Proceedings of the 10 th International Congress’. (Eds R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff.) pp. 230–241. (CSIRO Publishing: Melbourne). Athias-Binche, F. (1997). Acarine biodiversity. I. A new database. Preliminary examples of its use in statistical biosystematics. Acarologia 38, 331–343. Balogh, J. (1968). New oribatids (Acari) from New Guinea. Acta Zoologica Hungarica 14, 259–85. Balogh, J. (1972). ‘The Oribatid Genera of the World.’ (Akadémiai Kiadó: Budapest.) Balogh, J. and Balogh, P. (1992). ‘The Oribatid Mites Genera of the World, vol. 1.’ (The Hungarian National Museum Press: Budapest.) Balogh, J. and Mahunka, S. (1979). New taxa in the system of the Oribatida (Acari). Annales Historico-Naturales Musei Nationalis Hungarici 71, 279–290. Bernini, F. (1987). Current ideas on the phylogeny and the adaptive radiations of the Acarida. Bolletin Zoologica 53, 279–314. Evans, G.O. (1992). ‘Principles of Acarology.’ (CAB International: Wallingford.) Fujikawa, T. (1991). List of oribatid families and genera of the world. Edaphologia, 46, 1–130. Grandjean, F. (1928). Sur un Oribatidé pourvu d’yeux. Bulletin de la Société Zoologique de France 53, 235–242. Grandjean, F. (1931). Observations sur les Oribates (2re série). Bulletin du Muséum National d’Histoire Naturelle 3, 651–665. Grandjean, F. (1932). La famille des Protoplophoridae (Acariens). Bulletin de la Société Zoologique de France 27, 10–36. Grandjean, F. (1934). Observations sur les Oribates (6e série). Bulletin du Muséum National d’Histoire Naturelle 6, 353–360. Grandjean, F. (1935a). Observations sur les Oribates (8e série). Bulletin du Muséum National d’Histoire Naturelle 7, 237–244. Grandjean, F. (1935b). Observations sur les Acariens (1re série). Bulletin du Muséum National d’Histoire Naturelle 7, 119–126. Grandjean, F. (1939). Quelques genres d’Acariens appartenant au groupe des Endeostigmata. Annales des Science Naturelle, Zoologie 2, 1–122. Grandjean, F. (1941). La chaetotaxie comparée des pattes chez les Oribates (1er série). Bulletin de la Société Zoologique de France 66, 33–50. Grandjean, F. (1947). Les Enarthronota (Acariens). Première série. Annales des Science Naturelle, Zoologie 8, 213–248. Grandjean, F. (1948). Les Enarthronota (Acariens) (2e série). Annales des Science Naturelle, Zoologie 10, 29–58. Grandjean, F. (1949). Formules anales, gastronotiques, génitales et aggénitales du développement numérique des poils chez les Oribates. Bulletin de la Société Zoologique de France 74, 201–225. Grandjean, F. (1950a). Les Enarthronota (Acariens) (3e série). Annales des Science Naturelle, Zoologie 12, 85–107. Grandjean, F. (1950b). Étude sur les Lohmanniidae (Oribates, Acariens). Archives de Zoologie Expérimental et Générale 87, 95–161. Grandjean, F. (1953). Essai de classification des Oribates (Acariens). Bulletin de la Société Zoologique de France 78, 421–446.

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Grandjean, F. (1954a). Les Enarthronota (Acariens) (4e série). Annales des Science Naturelle, Zoologie 16, 311–335. Grandjean, F. (1954b). Étude sur les Palaeacaroides (Acariens, Oribates). Memoirs du Muséum National d’Histoire Naturelle 7, 179–272. Grandjean, F. (1957). L’infracapitulum et la manducation chez les Oribates et d’autres Acariens. Annales des Science Naturelle, Zoologie 11, 234–281 Grandjean, F. (1961). Nouvelles observations sur les Oribates (1re série). Acarologia 3, 206–231. Grandjean, F. (1962). Nouvelles observations sur les Oribates (2e série). Acarologia 4, 396–422. Grandjean, F. (1964). Nouvelles observations sur les Oribates (3e série). Acarologia 6, 170–198. Grandjean, F. (1969). Considérations sur le classement des Oribates. Leur division en 6 groupes majeurs. Acarologia 11, 127–153. Haumann, G. (1991). ‘Zur Phylogenie Primitiver Oribatiden, Acari: Oribatida.’ (Verlag für die Technische Universität Graz: Graz, Austria.) Kethley, J. B. (1990). Acarina: Prostigmata (Actinedida). In ‘Soil Biology Guide.’ (Ed. D. L. Dindal.) pp. 667–756. (John Wiley and Sons: New York.) Krantz, G. W. (1978). ‘A Manual of Acarology.’ (Oregon State University Book Stores: Corvallis, Oregon.) Lee, D. C. (1982). Sarcoptiformes (Acari) of South Australian soils. 3. Arthronotina (Cryptostigmata). Records of the South Australian Museum 18, 327–359. Lee, D. C. (1985). Sarcoptiformes (Acari) of South Australian soils 4. Primitive oribate mites (Cryptostigmata) with an extensive unfissured hysteronotal shield and aptychoid. Records of the South Australian Museum 19, 39–68. Michael, A. D. (1888). ‘British Oribatidae, Vol. 2.’ (The Royal Society of London: London.) Norton, R. A. (1975). Elliptochthoniidae, a new mite family (Acarina: Oribatei) from mineral soil in California. Journal of the New York Entomological Society 83, 209–216. Norton, R. A. (1982). Arborichthonius n. gen., an unusual enarthronote soil mite (Acarina: Oribatei) from Ontario. Proceedings of the Entomological Society of Washington 84, 85–96. Norton, R. A. (1984a). Monophyletic groups in the Enarthronota (Sarcoptiformes). In ‘Acarology VI, vol. 1’. (Eds D. A. Griffiths and C. E. Bowman.) pp. 233–240. (Ellis Horwood: Chichester.) Norton, R. A. (1984b). Book review: Primitive Oribatids of the Palaearctic Region (J. Balogh and S. Mahunka). Systematic Zoology 33, 472–474. Norton, R. A. (1994). Evolutionary aspects of oribatid mite life-histories and consequences for the origin of the Astigmata. In ‘Mites: Ecological and Evolutionary Analyses of Life-History Patterns’. (Ed. M. Houck.) pp. 99–135. (Chapman and Hall: New York.) Norton, R. A. (1998). Morphological evidence for the evolutionary origin of Astigmata (Acari: Acariformes). Experimental and Applied Acarology 22, 559–594. Norton, R. A., Alberti, G, Weigmann, G., and Woas, S. (1997). Porose integumental organs of oribatid mites (Acari, Oribatida). 1. Overview of types and distribution. Zoologica (Stuttgart) 146, 1–31. Norton, R. A. and Behan-Pelletier, V. M. (1991). Calcium carbonate and calcium oxalate as cuticular hardening agents in oribatid mites (Acari: Oribatida). Canadian Journal of Zoology 69, 1504–1511. Norton, R. A., and Behan-Pelletier, V. M. (1991). Epicuticular calcification in Phyllozetes (Acari: Oribatida). In ‘Modern Acarology’. (Eds Dusbábek and V. Bukva.) pp. 323–324, pl 33. (SPB Academic Publ.: The Hague.)

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Norton, R. A., Bonamo, P. M., Grierson, J. D., and. Shear,W. M. (1988). Oribatid mite fossils from a terrestrial Devonian deposit near Gilboa, New York State. Journal of Paleontology 62, 259–269. Norton, R. A., Kethley, J. B., Johnston, D. E., and OConnor, B. M. (1993). Phylogenetic perspectives on genetic systems and reproductive modes of mites. In ‘Evolution and Diversity of Sex Ratio in Insects and Mites’. (Eds D. L. Wrensch and M. A. Ebbert.) pp. 8–99. (Chapman and Hall: New York.) Norton, R. A., and Lions, J.-C. (1992). North American Synichotritiidae (Acari: Oribatida). 1. Apotritia walkeri n.g., n. sp., from California.. Acarologia 33, 285–301. Norton, R. A., OConnor, B. M., and Johnston, D. E. (1983). Systematic relationships of the Pediculochelidae (Acari: Acariformes). Proceedings of the Entomological Society of Washington 85, 493–512. Norton, R. A., and Palmer, S. C. (1991). The distribution, mechanisms and evolutionary significance of parthenogenesis in oribatid mites. In ‘The Acari: Reproduction, Development and Life-History Strategies’. (Eds R. Schuster and P. W. Murphy.) pp. 107–136. (Chapman and Hall: London). OConnor, B. M. (1984). Phylogenetic relationships among higher taxa in the acariformes, with particular reference to the Astigmata. In

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‘Acarology VI, vol. 1’. (Eds D. A. Griffiths and C. E. Bowman.) pp. 19–27. (Ellis Horwood: Chichester). Sarkar, S., and Subias, L. S. (1982). Some new Macropylines Oribates (Acarida) from India (Hypochthoniidae, Cosmochthonoidea and Epilohmanniidae). Eos, Revista Español de Entomologia 58, 311–318. Wauthy, G. (1984). Observations on the ano-genital region of adult Phthiracarus nitens (Oribatida: Mixonomata). In ‘Acarology VI, vol. 1’. (Eds D. A. Griffiths and C. E. Bowman.) pp. 268–275. (Ellis Horwood: Chichester.) Weigmann, G. (2001). The body segmentation of oribatid mites from a phylogenetic view. In ‘Acarology: Proceedings of the 10 th International Congress’. (Eds R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff) pp. 43–49. (CSIRO Publishing: Melbourne). Woolley, T. A. (1958). A preliminary account of the phylogeny of the Oribatei (Acarina: Sarcopt.). ‘Proceedings of the 10 th International Congress of Entomology, vol. 1.’ (Ed E. C. Becker.) pp. 867–873. (Mortimer Publishers: Montreal). Zhang, Z.-Q. (1996). Korcak patchiness exponent and distribution of taxonomic richness in the Oribatida (Acari: Acariformes). Systematic and Applied Acarology 1, 145–150.

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

HISTORICAL ECOLOGY OF THE ACARIDAE (ACARI): PHYLOGENETIC EVIDENCE FOR HOST AND HABITAT SHIFTS

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Barry M. OConnor Museum of Zoology, University of Michigan, Ann Arbor, Michigan 48109-1079 USA

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Abstract Phylogenetic analysis of generic relationships in the mite family Acaridae allows hypotheses to be formulated concerning shifts in habitat preferences and host utilization over evolutionary time. The results of historical ecological analysis suggest that early derivative Acaridae inhabit vertebrate nests and use nidicolous insects for dispersal. A shift into the nests of primarily solitary bees and wasps resulted in the radiation of the Horstiinae. A second shift into the nests of primarily social insects (bumblebees, honey bees, ants and termites) resulted in the radiation of the Tyrophaginae. From a possibly termite-associated ancestor, a subsequent radiation of mites evolved away from close associations with host insects and into a wide variety of moist temporary habitats. Within the resulting radiation of the subfamily Rhizoglyphinae, habitat and host generalists, secondary specialists in very specific microhabitats as well as associations with particular insect groups have evolved.

INTRODUCTION The Acaridae is among the most interesting groups of mites and contains the most abundant and economically important species that inhabit stored food and root crops, inflicting millions of dollars in damage annually (Hughes 1976). It is telling that one of these species is Acarus siro, the very first mite named by Linnaeus (1758). This species and many related taxa in this family are also of considerable interest to human and veterinary medicine in that the fauna of stored products also occurs in house dust. Many Acaridae, notably Tyrophagus putrescentiae and related species, are important members of the house dust ecosystem, causing dermatitis and respiratory allergy in humans (Fain, et al. 1990). Such ‘stored product mites’ also inflict losses in animal husbandry by contaminating feed and by causing skin lesions and digestive ulcers in domestic stock. In addition to their direct economic importance, acarid mites are of considerable interest to basic evolutionary biology and ecology. Many exhibit specific associations with their insect carriers, most notably among the Hymenoptera

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and Coleoptera. Examples of strict associations with particular host taxa include the genera Horstia with the bee genus Xylocopa, Naiadacarus with the fly family Syrphidae, and Passaloglyphus with the beetle family Passalidae. Such systems provide good models for historical ecological studies. The family Acaridae (=Tyroglyphidae) was last revised over 50 years ago. Zakhvatkin (1941) included 24 genera arranged as the subfamilies Tyroglyphinae (with tribes Tyroglyphini and Tyrophagini) and Rhizoglyphinae (with tribes Acotyledonini and Rhizoglyphini), but he did not place genera known only from deutonymphs into any higher category. Contemporaneously, Nesbitt (1945) included 11 genera and 3 additional subgenera, arranged similarly as subfamilies Acarinae (=Tyroglyphinae) (with tribes Acaridini [sic] and Tyrophagini) and Rhizoglyphinae (with tribes Caloglyphini and Rhizoglyphini). Since those revisions, an additional 70 genera have been proposed or included in the family, new subfamilies were proposed (Naiadacarinae, Horstiinae, Myrmolichinae, Fagacarinae), and a new tribe

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(Lasioacarini) was added to Acarinae. Additionally, the family Pinoglyphidae (Mahunka 1979) clearly belongs to this lineage, and OConnor (1982) included the previously recognised family Ewingiidae within the Acaridae. Historical ecology is a field of study which combines phylogenetic analysis of evolutionary relationships among organisms with knowledge of ecological parameters such as habitat or host associations to formulate hypotheses explaining the origin, maintenance or shifts in those parameters (Brooks and McLennan 1991). Because relatively few groups of mites have been subjected to rigorous phylogenetic analysis using modern methodologies, applications of historical ecological methodology to acarine groups have been relatively rare (OConnor 1985, 1987). This paper is a preliminary report on the phylogeny and historical ecology of the family Acaridae.

METHODS Historical ecological analysis begins with phylogenetic analysis. In the Acaridae, as with other taxa of free living Astigmata, such studies are complicated by their dimorphic life cycle. Deutonymphs are highly specialised morphologically and behaviorally for dispersal and/or withstanding adverse environmental changes (Houck and OConnor 1991). Having two more or less independent sets of morphological characters is beneficial in providing more data for analysis; however, difficulty arises in that most species of acarid mites are described from either adults or deutonymphs, but not both. The Acaridae presently contains approximately 350 species arranged in 90 recognizable and currently valid genera. Of these genera, only 25 contain at least one species known from both adult and deutonymphal morphologies. Another 24 are known only from the adult, with the remaining 41 known only from the deutonymph. In order to obtain character information for analysis, my associates, Drs Kimiko Okabe, Ronald Ochoa and Ariel Diaz, and I have examined museum specimens of mites, made new collections of phoretic deutonymphs from museum specimens of insect hosts, and have made new field collections of living mites in North and Central America and in Africa. Living mites have been reared in the laboratory on a variety of substrates, including natural ones such as decaying wood and dead insects, as well as colonies of the fungi Botrytis cinerea and Flammulina velutipes. So far we have succeeded in obtaining deutonymphs for 3 genera previously known only as adults and adults of 8 genera previously known only as deutonymphs. In addition, we have collected a number of new species which represent new genera. We used the PAUP program for phylogenetic analysis (Swofford 1993), to develop hypotheses of generic relationships in the family, and species relationships in selected genera. I present herein the results of an analysis of 180 characters in 30 genera for which we have been able to examine at least one species in both adult and deutonymphal morphologies. Two genera previously described from both forms (Mycetoglyphus and Neoacotyledon) are not included because we have not been able to obtain deutonymphal specimens and published descriptions are inadequate. Outgroup taxa used in hypothesizing character state polarities include the

related acaroid families Suidasiidae and Lardoglyphidae, and the early derivative genus Megacanestrinia in the family Canestriniidae, all known from both adult and deutonymphal forms. The latter was included to provide a better estimate of ancestral states in the deutonymph because deutonymphs of Suidasiidae and Lardoglyphidae all possess a number of apparent specializations not seen in the Acaridae. Because this analysis is preliminary, and we expect to add additional taxa, the complete data set will be published elsewhere. For the present, we regard the cladogram presented in Fig. 1 as a framework for discussing the evolution of host and habitat associations in the Acaridae.

RESULTS In trying to hypothesise the ancestral habitat for the Acaridae, closely related families were used as outgroups. I have previously included five families in the superfamily Acaroidea: Acaridae, Glycacaridae, Gaudiellidae, Suidasiidae and Lardoglyphidae (OConnor 1982). Of these, the monobasic Glycacaridae is hypothesised to be the sister group of the Acaridae; the single known species, Glycacarus combinatus, was collected from the nest of a bird (Griffiths 1977). The few known species of Gaudiellidae have been described from the nests of social bees (Bombus, Meliponini) (OConnor 1992). Species of Lardoglyphidae are specifically associated with beetles in the genus Dermestes, with some species restricted to the nests of carnivorous birds (Philips and Norton 1979, Iverson, et al. 1996). Suidasiid mites are associated with the nests of solitary Hymenoptera (Tortonia), vertebrate nests (Suidasia, Sapracarus, one unnamed genus), and soil habitats (Sapracarus, Namibacarus). Finally, the genus Scatoglyphus, known from a single species associated with bird nests and previously included in the Acaridae, does not share the diagnostic characteristics of that family and appears to represent an earlier derivative lineage of Acaroidea. Ecological associations of these groups related to the Acaridae suggest that the ancestral habitat for the Acaridae was likely either a vertebrate or hymenopteran nest, and since the closest related groups, Glycacaridae and Scatoglyphus, are vertebrate associated, I hypothesise that the ancestral acarid habitat was similar. The first derivative lineage in the preliminary acarid phylogeny (Fig. 1) is represented by the genus Acarus. Species of Acarus are best known as human associates, infesting stored food products. However a number of species are known only as deutonymphs collected from fleas (Siphonaptera), and they are presumably vertebrate nidicoles. This habitat association is compatible with the previous hypothesis that the ancestral acarid mite was a vertebrate nidicole. OConnor and Pfaffenberger (1987) provided a genus level phylogeny for Acarus and two related genera known only as deutonymphs phoretic on fleas. Recently, Fain et al. (1990) described a new, flea-phoretic genus, Psyllacarus, which they considered related to Lackerbaueria. Since this genus actually shares more characteristics with the Acarus clade, I include it here. Relationships among these genera, which can be ranked as a subfamily Acarinae in a restricted sense, are illustrated in Fig. 2. The next branch of the cladogram (Fig. 1) indicates an ecological shift. The genera Cerophagopsis, Sennertionyx, Horstia and Medeus are all associated with the nests of solitary Hymenoptera, almost exclusively bees. The subfamily name Horstiinae is available for this

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Acarinae

Horstiinae

Tyrophaginae

Rhizoglyphinae

Figure 1

Phylogenetic framework for the mite family Acaridae. Cladogram of relationships among genera known from both adult and deutonymphal instars (Mycetoglyphus and Neoacotyledon not included). Subfamilies include many other genera. Asterisks indicate genera for which adult or deutonymph has been newly correlated during this study. Data used to generate phylogeny will be published elsewhere.

lineage. Based upon deutonymphal morphology, I include some other genera here, all associated with solitary, but communally nesting bees. A preliminary phylogeny for these taxa based on deutonymphal characters is presented in Fig. 3, along with a phylogeny for the bee hosts derived from Roig-Alsina and Michener (1993). Host specificity varies among horstiine genera, with some apparently very specific to a particular lineage of host bees. The monobasic Neohorstia has been collected only from the anthidiine megachilid genus Archianthidium. Although described originally from a bee identified as a Euglossa, we have found species of Horstiella only on the centridine apid genus Epicharis (Ochoa and OConnor, 2000). Horstia has been collected only from the xylocopine apid genus Xylocopa (with one species known from human associations). We have collected the single known species of Sennertionyx from a wide variety of species in several genera of anthidiine

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Acarus Cerophagopsis Sennertionyx* Horstia Medeus Lackerbaueria Kuzinia Forcellinia Tyrophagus Acotyledon Viedebanttia Cosmoglyphus Sancassania Ctenocolletacarus Rhizoglyphus Mezorhizoglyphus* Boletacarus Bromeliaglyphus* Boletoglyphus Schwiebea Troupeauia Naiadacarus Naiacus* Stereoglyphus* Lamtoglyphus* Lasioacarus Passaloglyphus* Calvoliella Histiogaster Thyreophagus

Megachilidae, while Megachilopus has been collected only from the megachiline genus Chalicodoma. Most of our collections of Cerophagopsis have also been associated with Chalicodoma, although a species has been described from the meliponine genus Trigona, and we have seen an undescribed species from a nest of Apis mellifera. An additional species, C. indicus, is known from human associations (Potter and Olsen 1987, Fain 1988). We have collected species of both Medeus and Diadasiopus from the anthophorine apid genus Anthophora and the emphorine apid genus Diadasia. However, most collections of Medeus come from Anthophora, and most Diadasiopus from Diadasia. A comparison of the cladograms of horstiine genera and their host bees suggests that at the generic level host switching, rather than cospeciation, has been the rule. None of the relationships among mite

HISTORICAL ECOLOGY OF THE ACARIDAE

Psyllacarus Paraceroglyphus Trichopsylopus Acarus Figure 2

Cladogram of relationships among genera of the subfamily Acarinae (modified from OConnor and Pfaffenberger 1987)

genera is mirrored in the host phylogeny, and most bees do not harbor horstiine mites. Within genera, however, historical associations (co-speciation) may explain some relationships. To date, we have analysed species level relationships only in the genus Horstiella (Ochoa and OConnor, 2000). Although no modern phylogeny is available for the Epicharis bee hosts, species of Horstiella are specific to particular recognised subgenera, suggesting that historical associations may explain these relationships. The next branch of the framework cladogram (Fig. 1) includes genera associated with both solitary and social Hymenoptera. The subfamily name Tyrophaginae is available for this lineage. The first branch contains Lackerbaueria, associated with solitary wasps in the family Sphecidae. A closely related genus, Schulzea, is known only from deutonymphs collected from both solitary wasps and bees. Aleuroglyphus, known only from adults collected in human associations (stored products, house dust) also appears related to Lackerbaueria on the basis of adult characteristics. The other genera of Tyrophaginae are associated with social insects: Kuzinia with bumblebees (Bombus), Forcellinia with honey bees (Apis) and ants (Formicidae), and Tyrophagus with ants. Tyrophagus is unusual in that, while clearly related to the ant-associated genus Forcellinia, and one species (T. formicitorum) still retains obligate ant-associations (Fain and Chmielewski 1987), most species have shifted away from ant associations into many different habitat types. Species of Tyrophagus are commonly found in litter habitats and on vegetation. They are perhaps best known in human associations where they infest a variety of materials (Hughes 1976). Not included in Fig. 1 are some taxa associated with termites (Isoptera). This fauna is poorly known, with only one species known from both adult and deutonymphal forms. ‘Acotyledon’ formosani was described from the subterranean termite, Coptotermes formosanus (Philipsen and Coppel 1977). We have seen additional related species which form an unnamed genus that is the sister group of the remaining acarid lineage, the Rhizoglyphinae. We hypothesise that termite nests are the ancestral habitat for the Rhizoglyphinae. Two early derivative rhizoglyphine genera are included in Fig. 1, Acotyledon and Viedebanttia. The former is characterised by a modified deutonymph which has a highly regressive attachment organ. The common species A. paradoxa occurs in tree holes, arboreal bird and mammal nests and in human associations. Viedebanttia is more poorly known, with the

only species described from both adult and deutonymph, V. schmitzi, having been collected from soil habitats (Türk and Türk 1957). We have collected undescribed species of Viedebanttia from decaying wood (deutonymphs phoretic on Diplopoda) and from fruiting bodies of the xylariaceous fungus Xylaria. The next lineage, the genus Cosmoglyphus, is primarily termite associated, but some deutonymphs have been collected from ants (Lombert et al. 1982). The lineage containing Cosmoglyphus and the remaining rhizoglyphine mites is characterised by, among other things, the evolution of male polymorphism, with heteromorph males possessing modifications for fighting (Türk and Türk 1957, Woodring 1969). Another shift from termite associations lead to the genus Sancassania (=Caloglyphus). This large lineage will certainly prove to incorporate a number of genera described only as deutonymphs, as well as the nominal genus Ctenocolletacarus. Most species of Sancassania are associated with scarab beetles in various habitats. Dung beetles carry species living in dung, and wood inhabiting scarabs such as the Dynastinae carry species which live with the beetle larvae in galleries. Species associated with the Melolonthinae disperse as deutonymphs in the soil, attaching to beetle larvae feeding on roots. They remain with the host until it dies (as a larva or adult) at which time they consume the carcass. Such soil associations have led to host shifts into the nests of ground-nesting bees. Species of Ctenocolletacarus which is cladistically part of Sancassania, are specifically associated with Australian stenotritid bees of the genus Ctenocolletes (Houston 1987). Sancassania boharti is specific to associations with the halictid bee genus Acunomia (Cross and Bohart 1969), and other species have been collected from other ground nesting Halictidae. Other Sancassania species occur in fungal fruiting bodies, root crops and human associations. In the laboratory, early derivative rhizoglyphine mites (Acotyledon, Cosmoglyphus, Sancassania) can be reared easily on a variety of food substrates including fungi, grain, and dead insects. Having evolved this ability to feed on different forms of decaying organic matter, mites in the remaining rhizoglyphine lineage are characterised by a wide spectrum of habitats. Correlated with these habitat shifts is the ability to utilise a variety of arthropod hosts for dispersal. The Rhizoglyphus lineage contains good examples of both species that are generalist phoretics and other species that are habitat specialists. The four nominal genera included here form a single lineage. The large genus Rhizoglyphus is apparently paraphyletic with respect to the other three, and we are beginning phylogenetic analysis of this entire lineage (OConnor and Diaz, unpublished). Species included in Rhizoglyphus are best known as pests of root crops, bulbs and tubers. Deutonymphs of these species may be found on many arthropod hosts including Coleoptera, Diptera and Myriapoda. Adults of Mezorhizoglyphus and Boletacarus are known only from fungal fruiting bodies. My colleagues and I have collected a number of species from similar habitats which demonstrate the relationship between these nominal genera and Rhizoglyphus. Bromeliaglyphus is currently monotypic, but we have collected several new species and have obtained the deutonymphs through rearing. All species in this small genus have been collected from Neotropical Bromeliaceae in which they inhabit the leaf axils. Adult morphology in this genus ranges from

79

Barry M. OConnor

Horstiine mites

Host bees Xylocopa

Medeus Diadasia Horstia Anthophora Horstiella Epicharis Diadasiopus Eulaema N. Gen.

Euglossa Sennertionyx Apis Cerophagopsis Trigona Megachilopus Chalicodoma N. Gen.

Anthidium Neohorstia Archianthidium Figure 3

Relationships among genera of the subfamily Horstiinae, compared with relationships among host bees. Most bee genera are not hosts, and are not included.

very similar to Rhizoglyphus for species living in the ‘soil’ formed in bromeliad leaf axils, to highly modified species with very long legs and body setae which live an aquatic existence in ‘tank’ bromeliads. Associations with fungal fruiting bodies also characterise the next lineage, the genus Boletoglyphus. Adults and other feeding stages inhabit the spore tubes of several species of polypore fungi, and deutonymphs are specifically associated with boletophagine Tenebrionidae (OConnor 1984). Species we have collected are each associated with a single species of fungus: the Palaearctic B. boletophagi with Fomes fomentarius, the Nearctic B. ornatus with Ganoderma applanatum, and several undescribed Oriental species from different polypore species. The Schwiebea lineage, like the Sancassania lineage, will likely incorporate a number of previously known deutonymphal genera. The genus Schwiebea, as presently constituted, is a paraphyletic grouping. Few species in this large genus are known from both adult and deutonymphal morphologies and as more species

80

are reared and correlated, additional generic synonymies will be revealed. Species of Schwiebea near the type species, S. talpa, have been collected from soil habitats and from fungal fruiting bodies. Other species placed here are common in decaying wood (species related to the type species of Troupeauia). Others are completely aquatic, living in a variety of temporary aquatic habitats. Among these are the ‘obesa-group’ of Schwiebea and the nominal genera Naiadacarus and Naiacus. Naiadacarus inhabits water-filled tree holes in North America, and Naiacus lives in bromeliads in Central America. Students in my laboratory have reared a species of Naiacus and obtained the deutonymph; both adult and deutonymphal morphologies suggest this group should be incorporated into Naiadacarus. The unusual adult features of these aquatic mites, notably their large size, long legs and body setae, which caused Fashing (1974) to propose a new subfamily, Naiadacarinae, are also seen in other aquatic astigmatid mites in the families Algophagidae, Histiostomatidae and, as noted above, in the acarid genus Bromeliaglyphus. This common suite of characters appears to represent adaptation to the aquatic environment.

HISTORICAL ECOLOGY OF THE ACARIDAE

Three other nominal genera are included in the Schwiebea lineage, each having specialised habitat associations. Stereoglyphus (including Troglocoptes) species are heavily sclerotised mites, but otherwise retain the adult morphology of Schwiebea. All described and several undescribed species have been collected in cave habitats, but I have obtained new species from tree holes in North America and compost in Australia. I have obtained a deutonymph for one species, and it has a completely regressive morphology (‘inert’ type). Passaloglyphus species are currently described only as deutonymphs collected from passalid beetles in the Neotropical and Afrotropical regions. Ronald Ochoa and I have reared a species in Costa Rica whose adults have a number of striking autapomorphies (including enlarged forelegs and reduction of para-anal suckers in the male), but whose other characteristics are typical for this lineage. Lasioacarus was originally described from adults collected from an ant nest, but newer collections have been made from honey bee colonies. My students and I have collected deutonymphs from several Asian species of Apis, on which they attach almost exclusively to the hind tarsi of the bees. Fain and Chmielewski (1987) proposed a new tribe, Lasioacarini, in the subfamily Acarinae for this genus, however, both adult and deutonymphal morphologies are typical of the Schwiebea lineage. The final acarid lineage in Fig. 1 includes the genera Calvoliella, Histiogaster and Thyreophagus. Almost all species in these genera are associated with woody substrates, either decaying logs, bark crevices, fungal fruiting bodies or the nests and galleries of wood boring insects. Like many species in the previous lineage, most show little specificity to particular tree or fungal species or to their insect carriers. OConnor (1991) reported Calvoliella cyclopis deutonymphs from 20 species of insects and those of Histiogaster arborsignis from 15 species of Coleoptera, Hymenoptera and Diptera. There remains one lineage not included in Fig. 1 which demonstrates a unique shift in habitat/host utilization. Mites formerly included in the family Ewingiidae are all associated with terrestrial or freshwater crustaceans, on which they live their entire lives. As with other astigmatid mites which have adopted a permanent parasitic or ecto-commensal relationship with a host, these mites apparently do not form deutonymphs for dispersal. Thus, they were not included in the analysis producing Fig. 1. The nominal genera Ewingia, Askinasia and Hoogstraalacarus live on hermit crabs of the genus Coenobita, while Kanekobia is known from the freshwater crab now known as Geothelphusa dehaani. The extreme morphological specializations of these mites, notably the modifications of the legs for attaching to the host, caused previous authors to elevate the rank of this group. If autapomorphies are ignored, however, the lineage clearly belongs in a relatively basal position within the Rhizoglyphinae. The group was previously diagnosed by the modified hind legs used in attachment. However, closer examination of all of these taxa and of two undescribed genera indicates that only Ewingia and Hoogstraalacarus have homologous attachment structures. Still, the monophyly of the group is suggested by the unique form of the chelicerae, which is shared by all species. In conclusion, the family Acaridae exemplifies an adaptive radiation whose included lineages have been able to exploit a wide vari-

ety of habitats and hosts. From ancestral lineages which were dependent upon hosts to create the required habitat (vertebrate and insect nests), acarid mites ultimately colonised many preexisting patchy habitats. Later specialization on such habitats as fungal fruiting bodies, decaying wood and phytotelmata was accompanied by loss of specific phoretic associations, such that some species may use a very wide variety of insects for dispersal (OConnor 1991). The best known habitat for acarid mites, human food stores and house dust, was invaded by species from multiple acarid lineages. Some of these colonizations are simply the result of human exploitation of the natural habitats of the mites, such as in bulb mites of the genus Rhizoglyphus. Ancestrally nest-inhabiting species of the genus Acarus probably made the transition easily, especially after the domestication of poultry. Tyrophagus species had already shifted from ancestral ant-associations to relatively dry organic substrates such as grassland/savanna litter. Colonization of human food stores from such semi-natural substrates as haystacks was an easy transition. While the natural origins of such species as Horstia longa and Cerophagopsis indica are clearly in the nests of solitary bees, the connection with anthropogenic habitats is less obvious for these species. Studies on the feeding habits of these mites and their nidicolous relatives may shed light on the factors involved in the transition.

ACKNOWLEDGEMENTS Funding for this project comes from a grant from the US National Science Foundation (NSF DEB 9521744). I thank my associates Drs Kimiko Okabe, Ronald Ochoa, and Ariel Diaz, and students Ethan Kane, Gerald Daneshvar, Jason Steinberg, Camille Angelys, Jennifer Maigret, Ali Khaleel, George Kallingal, Pedro Tan, and Laura Krueger, who have assisted in this project. I also thank the numerous museum curators and colleagues who have provided specimens for study.

REFERENCES Brooks, D. R., and McLennan, D. A. (1991). ‘Phylogeny, Ecology and Behavior: A Research Program in Comparative Ecology.’ (University of Chicago Press: Chicago.) Cross, E. A., and Bohart, G. E. (1969). Phoretic behavior of four species of alkalai bee mites as influenced by season and host sex. Annals of the Entomological Society of America 77, 725–732. Fain, A. (1988). The identity of Rhypoglyphus indicus Potter & Olsen, 1987 (Acari). Bulletin et Annales de la Société royalê belge d’Entomologie. 124, 65–66. Fain, A., Bartholomaeus, F., Cooke, B., and Beaucournu, J. C. (1990). Two new species of phoretic deutonymphs (Acari, Astigmata) from Australian fleas. Bulletin de l’Institut royal des Sciences Naturelles de Belgique, Entomologie 60, 97–101. Fain, A., and Chmielewski, W. (1987). The phoretic hypopi of two acarid mites described from ants’ nest: Tyrophagus formicetorum Volgin, 1948, and Lasioacarus nidicolus Kadzhaja and Sevastianov, 1967. Acarologia 28, 53–61. Fain, A., Guérin, B., and Hart, B. J. (1990). ‘Mites and Allergic Disease.’ (Allerbio: Varennes en Argonne.) Fashing, N. J. (1974). A new subfamily of Acaridae, the Naiadacarinae, from water-filled treeholes (Acarina: Acaridae). Acarologia 16, 166–181.

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Barry M. OConnor Griffiths, D. A. (1977). A new family of astigmatid mites from the Iles Crozet, sub-Antarctica; introducing a new concept relating to ontogenetic development of idiosomal setae. Journal of Zoology, London 182, 291–308. Houck, M. A. and OConnor, B. M. (1991). Ecological and evolutionary significance of phoresy in the Astigmata (Acari). Annual Review of Entomology 36, 611–636. Houston, T. F. (1987). The symbiosis of acarid mites, genus Ctenocolletacarus (Acarina: Acariformes) and Stenotritid bees, genus Ctenocolletes (Insecta: Hymenoptera). Australian Journal of Zoology 35, 459–468. Hughes, A. M. (1976). ‘The Mites of Stored Food and Houses.’ Ministry of Agriculture, Fisheries and Food, Technical Bulletin No. 9, 2 nd ed. (Her Majesty’s Stationery Office: London.) Iverson, K., OConnor, B. M., Ochoa, R., and Heckmann, R. (1996). Lardoglyphus zacheri (Acari: Lardoglyphidae), a pest of museum dermestid colonies, with observations on its natural ecology and distribution. Annals of the Entomological Society of America. 89, 544–549. Linnaeus, C. (1758). ‘Systema naturae per regna tria naturae, secondum classes, ordines, genera, species cum characteribus, differentiis, synonymis, locis.’ 10th ed. (Laurentii Salvii: Holmiae.) Lombert, H. A. P. M., Lukoschus, F. S., and OConnor, B. M. (1982). The life-cycle of Cosmoglyphus inaequalis Fain and Caceres, 1973, with comments on the systematic position of the genus. Results of the Namaqualand-Namibia expedition of the King Leopold III Foundation for the exploration and protection of nature (1980). Bulletin de l’Institut royale des Sciences Naturelles d’Belge, Entomologie. 54 (10), 1–17. Mahunka, S. (1979). The examination of myrmecophilous Acaroidea mites based on the investigations of Dr C. W. Rettenmeyer (Acari: Acaroidea) II. Acta Zoologica Academiae Scientiarum Hungaricae 25, 311–342. Nesbitt, H. H. J. (1945). A revision of the family Acaridae (Tyroglyphidae), order Acari, based on comparative morphological studies. Part I. Historical, morphological, and general taxonomic studies. Canadian Journal of Research, series D. 23, 139–188. Ochoa, R. and OConnor, B. M. (2000). Revision of the genus Horstiella (Acari: Acaridae): mites associated with neotropical Epicharis bees (Hymenoptera : Apidae). Annals of the Entomological Society of America 93, 713–737. OConnor, B. M. (1982). Acari: Astigmata. In ‘Synopsis and Classification of Living Organisms, vol. 2.’ (Ed S. B. Parker.) pp. 146–169. (McGrawHill: New York.) OConnor, B. M. (1984). Acarine-fungal relationships: the evolution of symbiotic associations. In ‘Fungus-Insect Relationships: Perspectives

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in Ecology and Evolution’. (Eds Q. Wheeler and M. Blackwell) pp. 354–381. (Columbia University Press: New York.) OConnor, B. M. (1985). Hypoderatid mites (Acari) associated with cormorants (Aves: Phalacrocoracidae), with description of a new species. Journal of Medical Entomology 22, 324–331. OConnor, B. M. (1987). Host associations and coevolutionary relationships of astigmatid mties of New World Primates I. Families Psoroptidae and Audycoptidae. Fieldiana (Zoology) New Series 39, 245–260. OConnor, B. M. (1991). A preliminary report on the arthropod-associated Astigmatid mites (Acari: Acariformes) of the Huron Mountains of Northern Michigan. Michigan Academician 24, 307–320. OConnor, B. M. (1992). Ontogeny and systematics of the genus Cerophagus (Acari: Gaudiellidae), mites associated with bumblebees. Great Lakes Entomologist 25, 173–189. OConnor, B. M., and Pfaffenberger, G. S. (1987). Systematics and evolution of the genus Paraceroglyphus and related taxa (Acari: Acaridae) associated with fleas (Insecta: Siphonaptera). Journal of Parasitology 73, 1189–1197. Philips, J. R. and Norton, R. A. (1979). Lardoglyphus falconidus n. sp. (Acarina: Acaridae) from the nest of an American kestrel (Falco sparverius L.). Acarologia 20, 128–137. Phillipsen, W. J., and Coppel, H. C. (1977). Acotyledon formosani sp. n. associated with the Formosan subterranean termite, Coptotermes formosanus Shiraki (Acarina: Acaridae-Isoptera: Rhinotermitidae). Journal of the Kansas Entomological Society 50, 399–409. Potter, R. W., and Olsen, A. R. (1987). Description of a mite, Rhypoglyphus indicus, new genus, new species (Acari: Acaridae) found in foods from the Oriental Region. International Journal of Acarology 13, 271–275. Roig-Alsina, A., and Michener, C. D. (1993). Studies of the phylogeny and classification of long-tongued bees (Hymenoptera: Apoidea). University of Kansas Science Bulletin 55, 124–162. Swofford, D. L. (1993). ‘PAUP: Phylogenetic analysis using parsimony. version 3.1.’ (Computer program distributed by the Illinois Natural History Survey: Champaign.) Türk, E., and Türk, F. (1957). Systematik und Ökologie der Tyroglyphiden Mitteleuropas. In ‘Beiträge zur Systematik und Ökologie Mitteleuropäischer Acarina, vol. 1.’ (Ed H.-J. Stammer.) pp. 1–231. (Akademische Verlagsgesellschaft, Geest & Portig K.-G.: Lepizig.) Woodring, J. P. (1969). Environmental regulation of andropolymorphism in tyroglyphids (Acari). In ‘Proceedings of the 2 nd International Congress of Acarology’. (Ed G. O. Evans.) pp. 433–440. (Adadémai Kaidó: Budapest.) Zakhvatkin, A. A. (1941). ‘Tyroglyphoidea (Acari). Fauna SSSR, Arachnoidea v. 6, no. 1.’ (English translation by A. Ratcliff and A.M. Hughes.) pp. 1–573. (A.I.B.S.: Washington.)

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

ORGANISMAL PATTERNS CAUSING HIGH POTENTIAL FOR ADAPTIVE RADIATION IN PARASITENGONAE (ACARI: PROSTIGMATA)

1

Freie Universität Berlin, Institut für Zoologie, Königin-Luise-Strasse 1-3, D-14195 Berlin, Germany, Email: [email protected] 2 Universität Bremen, FB2/ Nw II, Leobener Strasse, D-28357 Bremen, Germany 3 To whom correspondence should be sent

....................................................................................................

Andreas Wohltmann1, 3, Harald Witte 2, Ronald Olomski 2

.................................................................................................................................................................................................................................................................

Abstract It seems to be a common evolutionary phenomenon that closely related systematic groups display strong differences with regard to species numbers, diversity of inhabited biotopes and intensity of adaptive radiation. Parasitengonae (Acari: Prostigmata) provide apt examples for the examination of this phenomenon. These mites are known to inhabit a great variety of biotopes ranging from xeric to aquatic. Moreover, they display a considerable species-richness and diversity of organisation patterns. However, whereas some taxa (e.g. Erythraeoidea, Trombidiidae) are highly successful, others (e.g. Calyptostomatoidea, Johnstonianidae) are represented by low species numbers and they inhabit only a few biotope types. We here focus on the question of which organismal patterns have caused the evolutionary success of the whole group as well as of some subgroups, and which patterns have restricted the potential for adaptive radiation in others? Features that facilitate adaptations to different biotope types and modes of living are (1) Emancipation of the internal milieu from external conditions. This may be achieved by glands that seal body-openings by means of secretions, by morphological internalisation of body regions, by mechanisms allowing regulation of of the water- and ionic balance in a wide range of environmental conditions, by protective egg- or spermsheaths and by spermatophores having a stable water balance at various humidity conditions; (2) mechanisms allowing regulation of the water- and ionic balance in a wide range of environmental conditions; (3) a complex life-cycle including a parasitic larva and two calyptostatic nymphs. The parasitic larva increases the potential to disperse and to colonise patchy and/or temporary biotopes. Calyptostases allow complex metamorphoses and the development of strongly heteromorphic active instars which enable species to use different resources during ontogeny. A restricted potential for adaptation to new environmental conditions may be caused by the evolutionary loss of emancipatory structures and functions and the decrease of regulatory potentials. This may have evolved in the course of adaptation to a particular type of biotope (e.g. as in the hygrophilous Johnstonianidae). It may be also due to a character pattern that causes exclusion from many resources and habitat types as may be the case in the Calyptostomatoidea, being in some respects ‘living fossils’ when compared to its sister group Erythraeoidea.

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Andreas Wohltmann et al.

Figure 1

Original life-cycle of Acari and the complex life-cycle of Parasitengonae

INTRODUCTION The Parasitengonae are an evolutionarily quite successful group, with respect to both species diversity and inhabited biotope types. With more than 8,000 species described up to now (Welbourn 1983; Moritz 1993) the Parasitengonae comprise nearly 10% of the known Chelicerata. With regard to the intensity of adaptive radiation, Parasitengonae have colonised a great variety of biotope types ranging from xeric and amphibic to a wide range of aquatic habitats. In these they cope with a wide range of selection regimes derived from microclimatic or hydrographic conditions, soil or substrate conditions and the particular features of prey, hosts and predators. The evolution of a complex life-cycle (Fig. 1), which includes a parasitic larva as well as a predatory deutonymph and adult, has not only led to different life styles of ontogenetic instars, but was frequently correlated with adaptive changes of morphology, behaviour, microhabitat demands and usage of resources. The variety of selection regimes present in the inhabited biotopes, as well as the complex life-cycle, and the remarkable adaptive transformations of the instars in the course of evolution, qualify the Parasitengonae as an apt example for analyses of the causes for evolutionary success and great adaptive potential. In this paper we will focus on the questions: I.

Which organismal properties have facilitated the remarkable adaptive radiation in Parasitengonae and most of its subgroups?

II. Which organismal and developmental properties have caused a wide potential for ontogenetic transformation,

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and how did the evolution of different modes of life of the ontogenetic instars influence the evolutionary potential for adaptation to different biotopes and to different resources? III. Which characters have restricted the adaptive potential in groups represented by only few species, such as the Calyptostomatoidea and Johnstonianidae? In order to reconstruct the main causes and key characters that have enabled the adaptive radiation of the Parasitengonae and its subgroups, we will refer first to the probable organisation and the life habits of the common ancestor of Parasitengonae and its probable sister group. Next, we will describe the transformations of organisation and ontogenetic development which took place in the stem lineage of the Parasitengonae. Then, we will reconstruct key innovations facilitating the adaptive radiation of the main parasitengone subgroups Hydrachnidia, Trombidioidea and Erythraeoidea (Fig. 2). Finally, we will discuss the organismal patterns that have restricted the potential for adaptive radiation in some groups.

I. LIFE HISTORY FEATURES, HABITAT CONDITIONS AND PROBABLE ORGANISATION OF THE ANCESTORS OF

PARASITENGONAE The Parasitengonae were probably derived from the stock of anystoid mites (Lindquist 1976; Witte 1991a). Their sister-group within the Anystoidea seems to be either the Anystidae (shared potential synapomorphy according to Olomski 1995: macrofi-

ADAPTIVE RADIATION IN PARASITENGONAE

Figure 2

Phylogenetic relationships of selected genera of Parasitengonae, according to Welbourn (1984) and Witte (1991).

brillae in subcuticle) or even only the Anystinae (shared potential synapomorphy according to Olomski 1995: eugential setae of male are uniform and simply shaped). The common stem species of Parasitengonae and its anystid sister group was probably provided with a set of characters which occur not only in the Anystinae and Anystidae (Otto 1992; Olomski 1995) but in most Anystoidea and in other Prostigmata as well (Evans 1992). The life-cycle (Fig. 1) retains the ancestral state of the Acari, including a calyptostatic prelarva followed by five active predatory instars. Recent species of Anystidae display life-cycles with only one or, in some species, few generations per year, fairly synchronised by a hibernating or aestivating egg or prelarva

(Lange et al. 1974a; Golovach 1989; Olomski 1991b, 1995; Otto and Halliday 1991; Otto and Olomski 1994). Life-cycles with more than one generation are also not reported for the outgroups Teneriffiidae and Caeculidae. A life-cycle with only one generation per year thus may be assumed hypothetically for the stem species of Parasitengonae and Anystidae. The active ontogenetic instars of this stem species probably displayed an organisation of body appendages and mouthparts similar to that of recent species of Anystidae, and probably also had a similar predatory behaviour. They were not specialised on a particular type of prey. Several characters and physiological mechanisms which are known from Anystidae and Parasitengonae, and frequently also

85

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Figure 3

Structures and functions of the osmoregulatory system in Anystis baccarum. The dotted glands produce lipidaceous secretions. (redrawn from Olomski 1995)

from earlier derived groups of Prostigmata, may indicate that the common stem species Andreas Wohltmann et al.

ADAPTIVE RADIATION IN PARASITENGONAE

Table 1

Development at different humidity conditions in Trombidia. Minimum relative humidity (r.h.) at which development to the subsequent instar took place. Humidities tested: 33%, 55.5%, 76%, 93.5%, 98%, 100% r.h., submerged in water. Prl = prelarva, Lau = unfed larva, Lap = postparasitic larva after leaving the host, Pn = protonymph, Dn = deutonymph; n.t. = not tested, Numbers in brackets = instar survived but stopped development. Data in part from Wohltmann (1998)

Species

Egg to Prl

Prl to Lau

Lap to Pn

Pn to Dn

Johnstoniana errans

submerged

100% r.h.

submerged

100% r.h.

Johnstoniana parva

submerged

100% r.h.

n.t.

n.t.

Johnstoniana tuberculata

n.t.

n.t.

submerged

100% r.h.

Eutrombidium trigonum

98% r.h.

98% r.h.

n.t.

n.t.

Microtrombidium fasciatum

98% r.h.

98% r.h.

n.t.

n.t.

Microtrombidium parvum

98% r.h.

98% r.h.

n.t.

n.t.

Platytrombidium sylvaticum

98% r.h.

98% r.h.

n.t.

n.t.

Campylothrombium barbarum

98% r.h.

98% r.h.

n.t.

n.t.

Trombidium holosericeum

98% r.h.

98% r.h.

98% r.h.

98% r.h.

Allothrombium fuliginosum

98% r.h.

98% r.h.

n.t.

n.t.

Calyptostoma velutinus

n.t.

n.t.

98% r.h.

98% r.h.

Hirstiosoma ampulligera

98% r.h. (76% r.h.)

76% r.h.

n.t.

n.t.

Erythraeus sp.

98% r.h. (76% r.h.)

76% r.h.

76% r.h.

76% r.h.

Leptus ignotus

98% r.h. (76% r.h.)

76% r.h.

76% r.h.

76% r.h.

Charletonia cardinalis

n.t.

76% r.h.

76% r.h.

76% r.h.

of both groups was well adapted to changing humidity conditions, and already displayed a certain drought resistance. In particular, the following shared characters support this hypotheses: (1) glands in the region of the body openings which may seal the internal milieu by means of lipidaceous secretions. In Anystis, this type of gland includes accessory glands of the distal male and female genital tracts, and, moreover, the intercheliceral gland which probably protects the salivary pathway along the cervix as well as the opening of the podocephalic ducts and the pharynx opening (Witte 1978; Olomski 1995). There is, additionally, a pair of labial glands which in Anystis produces no lipidaceous secretion (Olomski 1995). In Parasitengonae all these glands produce lipids, and the anal opening is also protected by lipids produced by rectal glands or glandular epithelia (Witte and Olomski 1999); (2) coxal glands (Fig. 3; = podocephalic glands 4) which may produce a hyposmotic urine (Olomski 1995). In Anystis, the coxal glands are provided with a sacculus which is closely connected with the ventricle epithelium (Alberti and Storch 1977). In the case of the digestion of hyposmotic prey, hyposmotic urine seems to be transported rapidly via this region into the coxal gland and to be released soon thereafter at the tip of the gnathosoma (Olomski 1995). In Parasitengonae the sacculus of the coxal gland is reduced and a secretory urine is produced (Alberti and Storch 1977); (3) the podocephalic canal in anystids is a nearly closed duct with overlapping margins. It is not detached from the propodosomal cuticle (Olomski 1995); (4) the colon produces droplets of hyperosmotic faeces. Since this character is found in Anystis (Olomski 1995) and in ticks (Kaufman et al. 1981), it is probably ancestral character; (5) the haemolymph osmolality is about 350–380 mOsm/ kg (Olomski 1991a), which is typical for terrestrial arthropods; (6) the spermatophores are able to main-

tain a stable water balance at quite low relative air humidities by taking up water vapour passively from the air into the matrix secretion of the spermatophore droplet. In species of Anystis as well as in several Parasitengonae the spermatophores are able to tolerate humidities as low as 33% r.h. (relative humidity) (Witte 1991b); (7) in the spermatophores of Anystis and Parasitengonae, the single sperm cells are provided with a sheath which protects them against the loss of water to the strongly hygroscopic matrix secretion (Witte 1991b); (8) mechanisms which may prevent desiccation of the eggs and the developing animal during the moulting phases are reported for species of Anystis. According to Golovach (1988) development takes place optimally at 75% r.h., whereas Sorensen et al. (1976) observed in Anystis agilis development down to 47% r.h.. Among Parasitengonae, development down to 76% r.h., or tolerance of this humidity level, was observed so far only in erythraeids (Table 1). In these, lower humidities were tolerated for a short time only; at permanent exposure to 55% r.h. eggs and protonymphs dried out (Wohltmann 1998). However, there remain doubts whether the comparably high drought resistance of immobile stages of Anystis and erythraeoid species existed in their common ancestor. Reasons for this include (a) the structural components serving drought resistance of the eggs are only known for erythraeids. In these the eggs are covered by an additional layer of proteinaceous secretions and lipid-secretions, which are produced by accessory glands of the distal female genital tract (Witte 1975). In Anystis the protective mechanisms of the eggs are not yet known; (b) in the outgroups of the Erythraeoidea, the Trombidioidea and Calyptostoma, development of immobile instars is possible only at humidities of 98% r.h. or above (Wohltmann 1998). This may be an indication that the high desiccation resistance of immobile instars is a derived fea-

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Andreas Wohltmann et al. Table 2

Development times in days of calyptostatic and active nymphs in Parasitengonae. Minimum - maximum development time of the respective instar, * = mean development times; rearing temperature in °C, ? = not mentioned. PN = calyptostatic protonymph, DN = predatory deutonymph, TN = calyptostatic tritonymph, AD = predatory adult

Species

PN to DN

DN to TN

TN to AD

[°C]

Reference

Trombidioidea Neoschoengastia americana*

7.5

15.6

7.5

32

Everett et al. 1973

Johnstoniana errans

15–19

25–97

17–23

15

Wohltmann 1996

Johnstoniana rapax

9–11

8–21

9–14

15

Wohltmann et al 1999

Johnstoniana tuberculata

7–14

8–46

11–16

20

Wohltmann et al. 1994

Johnstoniana parva

8–13

10–19

10–14

20

Wendt et al. 1994

Ceuthothrombium cavaticum

14–21

37–74

14–21

24

Webb et al. 1977

Eutrombidium trigonum

23–27

21–220

24–28

20

Wohltmann et al. 1996

Eutrombidium locustarum

10–20

13–50

10–23

?

Severin, 1944

Neotrombidium beeri

11–20

10–214

11–21

22

Singer 1971

Allothrombium fuliginosum

20

28–35

16–28

21

Robaux 1971

Trombidium holosericeum

16–26

30–33

20

Wohltmann unpublished

21

Robaux 1971

Trombidium holosericeum

8–120

Erythraeoidea Balaustium putmani

4–6

4–8

4–5

24

Putman 1970

Charletonia cardinalis

8–12

9–13

8–12

20

Wohltmann unpublished

Erythraeus spec

8–11

11–19

13–21

20

Wohltmann unpublished

Erythrites urrbrae

15–18

11–39

15–16

?

Southcott 1961

Leptus fernandezi

Diapause

41–52

13–18

20

Wohltmann 1995

Leptus trimaculatus

13–18

17

21–22

20

Wendt et al. 1992

Limnochares aquatica

9–13

45–270

18–22

Böttger 1972

Eylais discreta

3–4

6–7

4–5

18–22

Böttger 1962

7–14

3–4

20

Wohltmann unpublished

Hydrachnidia

Eylais setosa Thyas barbigera

9–16

Months

10

20

Mullen 1977

Hydrodroma despiciens

1–3

-30

3–8

20–25

Meyer 1985

Hydrachna cruenta*

5

14

6

18–22

Böttger 1972

Piona nodata

3–4

21–28

3–4

18–22

Böttger 1962

ture in the Erythraeoidea; (9) the red colour of the mites, which has been identified as carotinoids in water mites (Czezuga and Czerpak 1968) and as lipopigments in Anystidae (Olomski 1995), probably protect them against UV-light when active on the soil surface. Although the organisation described above has allowed the Anystidae to tolerate a wide range of external conditions, and although anystids are quite successful predators (Olomski 1995), the group falls far short of the species richness and the diversity of structures, functions and life styles that are observed in the Parasitengonae. One may therefore hypothesise that characters which evolved in the stem lineage of the Parasitengonae strongly increased the potential for adaptive radiation.

II. EVOLUTIONARY TRANSFORMATIONS AND INNOVATIONS IN THE STEM LINEAGE OF

PARASITENGONAE In the stem lineage of the Parasitengonae the following main transformations took place, which probably increased the poten-

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tial for adaptive radiation (1) the larva changed to a parasitic way of life on insects; (2) the proto- and tritonymph became calyptostases; (3) the sacculus of the coxal glands was reduced and urine production probably became secretory (Alberti and Storch 1977); (4) the podocephalic canal became internalised (Witte 1991a); (5) there evolved an indirect mode of protraction of the chelicerae (Mitchell 1962; Witte 1991a). It is probably the evolution of characters (1) and (2) that considerably increased the potential of the Parasitengonae for adaptive radiation. Parasitism of the larva

Parasitism by parasitengone larvae is probably directly derived from predatory behaviour. At least there is no evidence for a phoretic intermittent step, as hypothesised by Houck (1994) for the evolution of parasitism in other acarine taxa. The main advantages of larval parasitism in the Parasitengonae probably are (1) the increased possibilities for dispersal via the flying host, and thus to inhabit even patchily distributed or ephemeral biotopes; and (2) the enlarged food resource gained by detection of a single host, which usually facilitates the whole growth of the larva. On the

Figure 4

Diagrammatic representation of the development from deutonymph to adult in Anystidae and Parasitengonae. Shaded areas indicate apolysis/ histolysis; formation of cuticle indicated through dashed lines.

ADAPTIVE RADIATION IN PARASITENGONAE

89

Figure 5

Structures and functions of the osmoregulatory system in the stem species of Parasitengonae (reconstruction by Olomski 1995). Abbreviations: aag = anterior accessory gland, an = anus, ch = chelicera, cv = cervix, dt = distal tubule, es = esophagus, geo = genital opening, hgt = hindgut, icg = intercheliceral gland, isg = intercalary segment, lag = labial gland, pgc = progenital chamber, pcc = podocephalic canal, ph = pharynx, pt = proximal tubule, s.s. = sealing secretions. The dotted organs indicate the orifical glands, which produce sealing secretions.

Andreas Wohltmann et al.

90

ADAPTIVE RADIATION IN PARASITENGONAE

other hand, these advantages are partly compensated by some selective disadvantages: (1) larval parasitism is usually correlated with increased specialisation to a restricted host range (Welbourn 1983). This specialisation is surely paid for by reduced chances for host detection, and results in increased larval mortality (Wohltmann 1999); (2) larval parasitism obviously causes selection for a strongly synchronised life-cycle due to the different availability of suitable hosts throughout the year (Smith and McIver 1984). This, in turn, usually allows only an univoltine life-cycle (Wohltmann 1999). As support of this hypothesis, secondary loss of larval parasitism in Parasitengonae is correlated with a tendency towards the evolution of multivoltine life-cycles (Smith 1998). Because of these risks associated with larval parasitism, it seems rather unlikely that the original main selection pressure for the evolution of parasitism in Parasitengonae was provided by an enlarged food resource. More likely, it was the increased opportunity for dispersal. We believe that larval parasitism on flying hosts, which allowed rapid long-distance colonisation of formerly unoccupied locations, was the real ‘key innovation’ at the base of the Parasitengonae. As a result of this change in life-style, the selective conditions changed dramatically for the larval stage. Compared with the postlarval instars, parasitic larvae became heterotypic in behaviour, and often larvae and the postlarval instars became heteromorphic in structure and inhabit different microhabitats. In most cases the larval instar displays more conservative character states, with respect to morphology as well as to habitat requirements, than do the postlarval stages. In water mites, larvae remained aerial for long phylogenetic periods, while the postlarval instars had already become truly aquatic. In the Trombidioidea the larvae remained epigaeic in those groups characterised by endogaeic occurrence of all other instars. In Calyptostoma and Erythraeoidea the larvae retained the original hook-like chelicerae, whereas the chelicerae in the postlarval instars became styliform. Calyptostatic instars

The question of which selection pressure may originally have favoured the transformation of the ancestrally active proto- and tritonymphs to calyptostases is still not satisfactorily resolved. One may imagine that evolution of calyptostases passed through elattostases. However, no such intermittent step is conserved in early-derived Parasitengonae. An original selective pressure for evolution of calyptostases may have been the need for a synchronised annual life-cycle. Such a synchronised life-cycle is required, on the one hand, in order to ensure simultaneous appearance of the larvae and potential hosts at times of optimal host availability, during a limited period of the year. On the other hand, insemination of females requires simultaneous appearance of both sexes during the mating period. Synchronisation of the life-cycle of a mite population is usually achieved by the obligate diapause of a particular ontogenetic instar, such as the egg (Johnstonianidae; Eggers 1994), the protonymph (Leptus ignotus, Leptus sp.; Wohltmann 1994) or the pre-reproductive adult (Eutrombidium trigonum; Wohltmann et al. 1996). When comparing development times, the minimum duration of calyptostatic and active instars is about the same. However, calyptostases facilitate synchronisation since their developmental time at a particular temperature is rather constant. By contrast, development times vary greatly in the active instars due to the variable success in predation (Table

2). Thus, it is surely easier to synchronise two events in species having only 3 active instars than in species having 5 active instars. As with the parasitic larva, the advantages of calyptostatic instars are partly compensated by some disadvantages. Although specimens of all parasitengone species try to hide in the soil or in cavities before going into calyptostasis, the inability to move surely increases the risk of being preyed upon. Moreover, to have only three feeding instars capable of substantial growth decreases and restricts the growth ability during ontogeny. This, in turn, obviously acts as phylogenetic constraint which fixes the size ratio of adults to eggs and limits fecundity (Wohltmann 1999). On the other hand, in several groups the calyptostatic instars have secondarily obtained an important role, in that they allowed the evolution of strongly heteromorphic mobile instars and thus increased the adaptive potential of parasitengone mites. The role of calyptostases for enabling radical repatterning of the organisation of subsequent active instars, as takes place in the Erythraeoidea, is twofold (Fig. 4). First, in the course of moulting from an active instar to the subsequent calyptostasis, an intense histolysis of the tissues of legs and gnathosoma takes place, and both are reduced to tissue buds. Shortly after, the cuticle of the calyptostatic instars is secreted and then again epidermis and tissue buds retract from the cuticle (Henking 1882; Witte 1978). During the development of the successive active instar within the apoderma of the calyptostasis, the tissue buds of limbs and gnathosoma may develop to a radically transformed organisation and are not limited by the morphological design of the previous active instar. This is true especially of the body appendages and the gnathosoma, whereas most internal organs show no histolysis. Second, in the course of moulting from a calyptostatic instar to the subsequent active instar no histolysis takes place. Thus, the time for development of the active instars is much greater than in mites which lack calyptostases. Protected by the cuticle of the calyptostase, which lacks body openings, the development of the active instar begins soon after formation of the calyptostatic cuticle, and it usually proceeds for most of the duration of the calyptostatic period (Witte 1978, 1998). By contrast, in the Anystidae the moulting phases are comparatively short. They seem to be correlated with little or no dedifferentiation of the tissues of legs and gnathosoma (Fig. 4). During the moulting phases the legs remain inside the exuvial appendages and are retracted out of these just before eclosion. Thus, this type of development probably does not allow extensive repatterning of the organisation. Coxal glands

The adaptive meaning of the loss of the sacculus of the coxal glands (Fig. 5) and of the assumed change of the mode of urine production from filtration to secretion (Alberti and Storch 1977) is not yet really understood. Since probably even in Parasitengonae the coxal glands produce a hyposmotic urine (Olomski 1995), and since this type of urine could probably be produced less expensively by filtration than by secretion of ions followed by passive transport of water and reabsorption of the ions, a satisfactory answer to this problem is still needed. For soft-skinned mites like the Parasitengonae,

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Andreas Wohltmann et al.

however, it may be advantageous that for excretion of a secretory urine there is no need for a filtration pressure. Indirect mode of protraction of chelicerae

The chelicerae, which articulate with the tip of the sigmoid pieces, have become protractible for a short distance. Protraction is achieved indirectly by action of cheliceral protractor 1, the ‘sigmoid muscle’ (Mitchell 1962; Witte 1995), which runs from the posterior part of the chelicera to the proximal part of the sigmoid piece. Contraction of this muscle causes a forward-rotation of the tip of the sigmoid pieces, which, in turn, leads to protraction of the chelicerae. The evolution of this protraction mode was apparently the initial step for the evolutionary transformation of cheliceral protractor 1 to a directly acting protractor. This evolutionary change took place convergently in Hydrachnidae (Mitchell 1962) and in the stem-lineage of Calyptostomatoidea and Erythraeoidea (Witte 1995, 1998), in which styliform and widely protractible chelicerae evolved. This, in turn, has probably enabled the adaptation to new types of prey. Internal podocephalic canal

The internalisation of the podocephalic canal has probably increased the protection of the pathway of salivary secretions to the gnathosoma. During the calyptostatic instars the internal podocephalic canal develops from an epidermal groove (Witte 1978).

III. THE SUBGROUPS OF PARASITENGONAE Hydrachnidia

The switch of the Hydrachnidia (water mites) to an aquatic way of life was probably achieved by non-swimming ancestors which colonised temporary pools (Wiggins et al. 1980; Wohltmann et al. 1999). Such biotopes are still inhabited by several groups of early-derivative water mites, such as Piersigiidae, Hydryphantidae and Thyasidae (Viets 1936, 1978; Imamura and Mitchell 1967; Wiggins et al. 1980). Many species of these groups are still able to survive and to crawl under terrestrial conditions (Olomski personal observation; Wohltmann 1991). Adaptation to the aquatic environment was probably enabled by several characters and mechanisms which had already evolved in the terrestrial ancestors of the water mites, either in the stem-lineage of the Parasitengonae or even earlier. These characters and mechanisms include (1) parasitism on flying insects, which enabled colonisation of patchily distributed and temporary habitats. By contrast to the eggs and other ontogenetic instars, the larval instar of Hydrachnidia retained its terrestrial life style; (2) lipid glands or glandular epithelia in the region of body openings, which protect the internal milieu of the animals against water uptake and loss of ions; (3) secretion of a hyposomotic urine via the coxal glands, which eliminates excess water and saves ions (Olomski 1995); (4) protection of the individual sperm cells by a sheath, which obviously hinders osmotic water uptake and loss of ions by the sperm cells. This is important because the spermatophores are deposited in a strongly hyposmotic milieu. In the stem lineage of the Hydrachnidia further adaptive features evolved which either enabled a widened usage of resources, or opti-

92

mised the protection against the strongly hyposmotic external milieu or the protection against predators. These characters include (1) cells of the transport epithelia of genital papillae and Claparède organs transformed in the Hydrachnidia to chloride-cells, which probably function in active uptake of ions (Alberti 1979) and thus serve osmoregulation. A similar functional change of these organs probably took place in limnic Halacaridae (Bartsch 1973); (2) in adaptation to limnic waters the haemolymph osmolality of deutonymphs and adults decreased to less than 300 mosm/kg (Olomski 1991a); (3) the postlarval active instars adapted to predation under aquatic conditions. Terrestrial Parasitengonae such as Johnstoniana spp. are also capable of moving under aquatic conditions and of surviving under submerged conditions for up to two weeks; however, they never prey in water (at 20°C, Wohltmann unpublished). By contrast, Hydrachnidia always prey in aquatic conditions only, even those species capable of moving in terrestrial conditions (e.g. Thyas spp. , Hydryphantes spp.); (4) an increased starving tolerance of several months. This is found in a number of early derivative Hydrachnidia (Wohltmann 1991) and can therefore be assumed present in the stem species of water mites. It may be an adaptation to the amphibic character of the original habitat, in which food was available only during a limited period of the year; (5) adaptation of mating and the mode of indirect sperm transfer to aquatic conditions, and the loss of hygroscopic properties of spermatophores (Witte 1991b); (6) evolution of an additional egg sheath, which originally covers each single egg (Sokolow 1924, 1925, 1977). The sheath does not protect eggs from drying out within a short time when exposed to unsaturated air humidities, and even at 100% r.h. eggs do not develop (Wohltmann unpublished). Possibly the additional sheath has an anti-predator function; (7) glandularia evolved in the deutonymphs and adults, these apparently have an anti-predator function (Schmidt 1936; Kerfoot 1982). The glandularia release a whitish secretion when the mite is grasped by a predator; which usually stops the attack immediately and allows the mite to escape. The recent diversity of the Hydrachnidia, however, is mainly a result of adaptations which evolved within this taxon. Some of the most important evolutionary changes are (1) the ability to swim enabled the deutonymphs and adults to use the whole threedimensional space of their habitat and was a necessary pre-requisite for using pelagic prey such as cladocerans. It is likely that the ability to swim evolved at least three times convergently within the Hydrachnidia. This may be inferred from (a) the particular type of swimming, which is different in Limnochares americana (propulsion mainly with legs IV, legs surface enlarged through setal blades, Smith 1979), Eylais spp. (Propulsion with legs I-III, provided with prolonged setae) and Euhydrachnidia (Propulsion with legs I-IV, provided with prolonged setae), and (b) from the phylogenetic distribution of ‘swimming ability’ which shows that the closest related taxa of swimming mites are non-swimmers (remaining Limnocharidae in relation to L. americana Limnocharidae; and Piersigiidae in relation to Eylais spp.; Thyasidae in relation to Hydrodroma and Neohydrachnidia); (2) at the base of Neohydrachnidia, before the derivation of Hydrachna, aquatic larvae evolved. These larvae do not leave the water after hatching but search for potential hosts in their aquatic habitat. Later on in evolution, moreover, the mode of preparasitic attendance evolved

ADAPTIVE RADIATION IN PARASITENGONAE

in the larvae of ‘higher’ Hydrachnidia (Lebertoidea, Arrenuroidea plus Hygrobatoidea). The larvae encounter the pupa of the host (Chironomidae) and wait for emergence of the host imago in order to start parasitism (Smith and Oliver 1976). This behaviour probably reduced larval mortality and increased the chance of locating a suitable host; (3) the reproductive behaviour changed to deposition of large spermatophore fields, and copulation evolved several times convergently (Proctor 1991; Witte 1991b; Witte and Döring 1999). Trombidioidea

In the stem lineage of the Trombidioidea the post-larval instars evolved a subterranean life-style (Robaux 1971), which is interrupted only by the mating period. Indirect sperm-transfer (Witte 1991b) still occurs at the soil surface. Eggs are deposited within the soil. The active postlarval instars are capable of active digging. The larvae, however, remain epigaeic during their host searching and parasitic phases. The endogaeic mode of life led to an emancipation from unfavourable surface conditions and has enabled the colonisation of even xeric habitats (e.g. Dinothrombium spp., Newell and Tevis 1960). The eggs and calyptostatic instars still need water vapour uptake for their development, which is limited to comparably high air humidities (above 93.5% r.h.) in the Trombidioidea hitherto observed (Wohltmann 1998). The evolution of a reduced desiccation resistance in the stem-lineage of the Trombidioidea is indicated, moreover, by the reduction of the intercheliceral gland (tracheal gland), which in most groups of Parasitengonae, Anystidae and Prostigmata protects the pathway of salivary secretions along the dorsal surface of the infracapitulum by means of a lipidaceous secretion (Witte 1978). Probably in correlation to the evolution of an endogaeic life-style, a dense setation of the idiosoma evolved. This type of setation bears the following advantages: (a) The backward directed setation supports mobility in the soil by peristaltic movements, and (b) the setation prevents direct water contact by holding an air film. In Platythrombium sylvaticum this air film persists for more than a month in adults kept submerged under a gauze net (at 5°C, Wohltmann unpublished). Members of the Trombidioidea, which secondarily display a less endogaeic life-style (such as the active postlarval instars of Allothrombium spp. , Zhang 1998), again increased desiccation resistance by the protection of the dorsal surface of the gnathosoma. This was through the transformation of the dorsal ridges of the lateral keels to folds formed of a soft cuticle, which appress to the chelicerae (Witte 1978). Within the Trombidioidea, the switch of the trombiculid larvae to parasitism on vertebrate hosts, in particular, has obviously led to an intense number of speciation events. Finally, in some groups (e.g. Vatacarus ipoides, Audy et al. 1972, Eutrombidium trigonum and Trombidium spp., Wohltmann 1999) there evolved secondary growth of the cuticle, which occurs during the parasitic phase of the larva. This character, named neosomy (Audy et al. 1972), allowed a reduction of the egg-size and has enabled a considerably increased fecundity and is also assumed for water mites of the genera Hydrachna and Eylais (Wohltmann 1999).

Erythraeoidea

In the stem-lineage of the Erythraeoidea a series of characters evolved which made this group of predators well adapted to xeric environmental conditions. Most erythraeids are reported from dry and arid biotopes (Southcott 1961), only few species secondarily colonised hygric habitats (e.g. some Callidosoma spp., Welbourn 1983; Charletonia cardinalis, Wohltmann 1998) or the supralittoral and the upper fringe of the eulittoral of marine and estuarine rocky shores (e.g. Abrolophus spp. , Halbert 1920; Pugh and King 1985). Some transformations mainly concerned the mouthparts and the potential for predation (1) the greatly protractible styliform chelicerae of deutonymphs and adults, which had already evolved in the common stem-lineage of Calyptostomatoidea and Erythraeoidea, lost the movable digit, which is still present in Calyptostoma. Moreover, there evolved a longitudinal dovetailing between the two chelicerae, thus completing the functional unit of these (Witte 1978, 1998); (2) in deutonymphs and adults the chelicerae and the dorsal surface of the infracapitulum became internalised by fusion of the lateral keels above the chelicerae. In the course of ontogeny this transformation takes place during the calyptostatic protonymphal period. Consequently, the pathway of salivary secretions along the elongated dorsal surface of the infracapitulum has become well protected, and, moreover, the longitudinal movements of the styliform chelicerae have become effectively guided. The evolution of a calyptostatic protonymph obviously was a necessary prerequisite for the radical ontogenetic change from the original cheliceral condition (as maintained in the erythraeoid larva) to the styliform chelicerae, as well as to the internalisation of the dorsal region of the gnathosoma. Further evolutionary novelties concern the tolerance of fluctuating humidity conditions. They mainly eased adaptive radiation of the surface dwelling Erythraeoidea in xeric environments; (3) the eggs have an additional protection, in that they are ensheathed by proteinaceous secretions produced by the dorsal accessory gland and by a lipidaceous secretion produced by the lipid gland of the vagina (Witte 1975). Eggs of Erythraeoidea tolerate exposure to constant humidities between 76% r.h. to 100% r.h.. At humidities below 98% r.h. a reversible cessation of egg development occurs; development to prelarvae continues only when such eggs are exposed to 98% r.h. or above for at least 24 h (Wohltmann 1998); (4) the calyptostatic instars develop to the successive instars at constant humidities down to 76% r.h. (Wohltmann 1998). As in Trombidioidea and Calyptostomatoidea, the cuticle of the preceeding active instar is extended to a maximum at the beginning of the calyptostatic instars, however, no weight increase due to water vapour uptake occurs in protonymphs of Erythraeidae (Fig. 6); (5) the larva has lost the anal opening and the Claparède organs. In all probability this reduction increases desiccation resistance; (6) the attachment of the larva to the host is modified. It is achieved by means of a gluing secretion (Abro 1988), which enables a quick attachment even to quite mobile insect hosts like cicadas. A stylostome, as it is found in Hydrachnidia (Davids 1973; Lanciani and Smith 1989) and in some Trombidioidea (Voigt 1970; Pflugfelder 1977; Hase et al. 1978), is lacking in Erythraeoidea.

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Andreas Wohltmann et al.

Figure 6

Fresh weight increases as a result of water uptake in terrestrial Parasitengonae. Generalised curve of relative fresh mass changes in the Trombidioidea, Calyptostomatoidea and Erythraeoidea. Larva post I = larva just after leaving the host; Larva post II = postparasitic larva after becoming immobile; Protonymph I = start of the protonymph, set as 100%; Protonymph II = protonymph, a short time before emergence of the deutonymph; Deutonymph = freshly emerged deutonymph. Original data from Wohltmann (1998).

In the course of the adaptive radiation of the Erythraeoidea, this character-pattern was largely maintained. Nevertheless, some important evolutionary changes took place (1) a greatly elongated gnathosomal sheath (armilla) evolved in the Smarididae. This allows extensive protraction of the gnathosoma, which may be useful in probing confined spaces when searching for prey. It also allows complete retraction of the gnathosoma into the idiosoma. Thus the gnathosoma may be protected against mechanical damage caused by moving in the litter layer of smaridid habitats (Witte 1998); (2) erythraeids adapted to using a wide spectrum of prey, including mobile instars of insects (e.g. ants by Erythraeus phalangioides). Balaustium florale became at least partly phytophagous, as it ingests pollen (Grandjean 1946). A good example of diversification in food resources, even within a genus, is seen in the deutonymphs and adults of the littoral inhabiting representatives of Abrolophus. Abrolophus rubipes and A. araneipes feed on oribatid and hyadesiid mites having a hard cuticle, whereas A. passerini and A. halberti are specialised predators of larvae of Chironomidae. A further species of Abrolophus, inhabiting the littoral fringe in northern Spain, preys on young barnacles of the genus Chthamalus (Witte 1978 and unpublished); (3) the loss of larval parasitism in some erythraeid groups probably enabled life in

94

biotopes where potential hosts are extremely rare (e.g. rocks and artificial hard substrates in Balaustium murorum), or in which parasitic larvae would have a high risk of drifting into unsuitable biotopes (e.g. the marine littoral in Abrolophus spp. ). Even in species having returned to predatory larvae, the biphasic life-cycle is partly maintained. As an example, larvae of littoral species of Abrolophus feed mainly on the ‘soft-cuticled’ instars of Nanorchestidae, whereas the active postlarval instars use different food resources and display considerable diversification among species (see above).

IV. GROUPS WITH RESTRICTED POTENTIAL FOR ADAPTIVE RADIATION

Within the Parasitengonae some groups, i.e. Calyptostomatoidea and Johnstonianidae, have undergone a comparatively limited adaptive radiation, which is expressed by low species diversity and low diversity of inhabited biotope types. Calyptostomatoidea

The Calyptostomatoidea are represented by a single genus including only a few species. When compared to the sister group Erythraeoidea, Calyptostomatoidea may be termed living fossils. Their

Figure 7

Organismal properties and their biological role and evolutionary consequences in Parasitengonae.

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styliform chelicerae still run in an open groove formed by the dorsal wall of the infracapitulum, and they have retained a movable cheliceral digit. The evolution of styliform chelicerae has obviously caused a trade-off, in which the selective advantage of the styliform chelicerae for predation was bargained against a decreased protection of the salivary pathway, along the dorsal surface of the infracapitulum, against desiccation. This decreased protection is due to the elongation of the cervix as well as to the reduced fit of stiletto-shaped chelicerae for protection compared to the ancestral cheliceral bases of earlier derived Parasitengonae such as Trombidioidea (Witte 1978). This was possibly one cause for the restriction of the Calyptostomatoidea to relatively humid biotopes, ranging from the litter layer of forests (Theis 1974) to amphibic biotopes (Wainstein 1977). The rather slow locomotion of active instars, which evolved in this type of habitat, probably hindered adaptation to surface habitats. Additionally, the switch of the parasitic larva to tipulid hosts, as well as the maintenance of a relatively ancestral type of styliform chelicerae, have probably led to exclusion of the Calyptostomatoidea from many habitat types and resources, to which species of the sister-group Erythraeoidea have adapted. Johnstonianidae

All Johnstonianidae are restricted to extreme hygric biotopes that provide saturated air humidity and free water all during the year (Wohltmann et al. 1999). Important adaptations are (1) the spermatophores are deposited on wet ground. In the genus Johnstoniana signalling stalks are deposited instead of signalling threads, which occur in most terrestrial Parasitengonae that deposit spermatophores at unsaturated air humidities. The signalling stalks are provided with an apical droplet containing no sperm cells but only the matrix secretion of the sperm. The droplets probably are provided with pheromones (Witte 1991b); (2) in the course of adaptation to hygric biotopes, the Johnstonianidae have lost several of those adaptations that originally served in desiccation resistance, e.g. rectal glands and the anterior accessory gland of the male genital tract. This has surely reduced energy costs. However, as a result, active postlarval instars display strong preference for saturated air humidity and have short survival at unsaturated air humidities (Wendt 1994); (3) the haemolymph osmolality is lowered and reaches values even below those of water mites (Wendt 1994). This also has reduced energy costs in hygric biotopes; (4) eggs and calyptostatic instars are very sensitive to desiccation. Moreover, in Johnstoniana spp. they have completely lost the ability to absorb water vapour. This leads to death of eggs and calyptostatic instars if no free water is available (Wohltmann 1998); (5) in the stem lineage of Johnstonianidae, the larva switched to Tipulidae as a highly abundant host resource. In correlation, preparasitic attendance evolved, which increased the chance of finding a host. Moreover, the risk of being dispersed into unsuitable biotopes is minimised when using hygrophilic hosts (Wohltmann 1996; Wohltmann et al. 1999). All these adaptations led to specialisation and limitation of the Johnstonianidae to hygric biotopes, and they restricted the ability to recolonise non-hygric biotopes.

CONCLUSIONS A series of protective structures and physiological properties that were present in the common ancestor of Parasitengonae and 96

Anystidae, already led to an effective emancipation of the internal milieu, as well as of the reproductive mechanisms, from environmental inflictions. This ancestral pattern enabled colonisation of a wide spectrum of biotopes ranging from xeric to hygric. Moreover, it provided necessary preconditions for the colonisation of the aquatic realm by the Hydrachnidia. The intense adaptive radiation of the Parasitengonae, however, was enabled and promoted by key innovations as indicated in Fig. 7. The evolutionary switch of the larva to parasitism on insects has increased their dispersal ability, and thus was the most important precondition for the colonisation of patchily distributed or ephemeral biotopes. The most obvious example is the Hydrachnidia, which certainly would not have undergone such an impressive adaptive radiation without this dispersal ability. Moreover, the resulting complex life-cycle with parasitic larvae and predatory postlarval instars led to differentiation of these ontogenetic instars and favoured heteromorphosis. Larvae and postlarval instars adapted not only to different food resources but frequently also to different microhabitats, as happened, for example, in the Hydrachnidia and the Trombidioidea. The evolution of calyptostatic proto- and tritonymphs, which originally may have facilitated synchronisation of populations, was probably the key developmental event which enabled the evolution of strongly heteromorphic ontogenetic instars. The intense histolysis in the course of moulting of an active instar to a calyptostatic instar, combined with the increased time available for developmental processes inside the calyptostatic apoderma, allowed radical structural transformation of the subsequent instar. Most obviously this happens in the Erythraeoidea during the metamorphosis of the larval to the deutonymphal gnathosoma. In combination, the biphasic life-cycle and the calyptostatic instars greatly influenced the intensity of adaptive radiation and speciation of Parasitengonae. They favoured divergent adaptation of larval and postlarval instars and led to differences in nutritional resources, feeding modes, modes of locomotion and microhabitats. The parasitic association of the larva has surely promoted speciation in many groups (Wohltmann 2001), and in this way has contributed to and stimulated the evolutionary success of Parasitengonae. In other groups, in which the larvae switched to an abundant host group such as the larvae of ‘higher’ water mites parasitic on Chironomidae (Smith and Oliver 1976), speciation may have been favoured mainly by adaptation of the postlarval active instars to new resources. The evolutionary success of the Parasitengonae was also facilitated by a further emancipation of their internal milieu from environmental effects, by the dispersal ability of the larva, and by particular adaptations of the subgroups. The latter include the evolution of the endogaic life style of Trombidioidea, and the evolution of a new type of chelicerae and an increased desiccation resistance in Erythraeoidea.

ACKNOWLEDGEMENTS We thank Mrs. Gundula Sieber for technical assistance, Mrs. Gerlinde Gust for managing the manuscript and Jens Bücking for interesting discussions. We wish to express our thanks to Roy A. Norton and an anonymous reviewer for critical comments and valuable suggestions on an earlier draft of this manuscript.

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ASSESSMENT OF THE USEFULNESS OF RIBOSOMAL 18S AND MITOCHONDRIAL COI SEQUENCES IN PROSTIGMATA PHYLOGENY

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Jürgen C. Otto and Kate J. Wilson Australian Institute of Marine Science, PMB 3, Townsville MC, QLD 4810, Australia

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Abstract The phylogenetic relationships among prostigmatid families are far from being resolved. Previous analyses have focused entirely on morphological characters. The current paper is an attempt to identify a gene which can provide useful molecular data to address these relationships. DNA was extracted from mites representing 12 prostigmatid families. The polymerase chain reaction was used to amplify the V4 region of the nuclear 18S rRNA gene and two regions of the mitochondrial cytochrome oxidase I (COI) gene, and these fragments were sequenced. Phylogenetic inference using a variety of algorithms revealed strong support for nodes linking taxa within the same family but support for interfamily relationships was not significant. An exception is the close relationship of the Trombidiidae and Erythraeidae which was well supported. In a separate analysis the 18S rRNA sequences of the Prostigmata were combined with those of other chelicerates available in public databases. This analysis showed strong support for the monophyly of the Prostigmata.

INTRODUCTION The Prostigmata comprises about 14,000 named species in 127 families (Norton et al. 1992). This diversity makes homologous character states across families and superfamilies hard to find and the reconstruction of phylogenetic relationships difficult. Thus it is perhaps not surprising that detailed hypotheses on the phylogenetic relationships among prostigmatid families are rare and those that exist (Krantz 1978; Norton et al. 1992) disagree substantially. Molecular data can provide homologous characters across widely divergent taxa – even across phyla (Turbeville et al. 1991; Schlegel 1994). Thus such data may be useful for reconstructing the phylogenetic relationships between prostigmatid families and superfamilies and may also contribute to the discussion of whether Acarina is a monophyletic or polyphyletic taxon. The first and most crucial step in construction of a molecular phylogeny is the identification of a suitable gene which provides clear phylogenetic infor-

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mation at the taxonomic level being considered. This requires sufficient variation to provide useful character differences, but not so much that the sequence is plagued by homoplasious substitutions. It is not possible to assume that a gene which provided useful phylogenetic information in one group will do the same in another. Rather, it is a matter of informed trial and error to select a gene with the appropriate phylogenetic information. The 18S ribosomal RNA (rRNA) gene is the most widely used molecule for analysing the phylogenetic relationships of organisms (Hillis and Dixon 1991). Among the Acarina, 18S sequences were previously used to infer tick phylogeny. Crampton et al. (1996) sequenced the variable region V4 and Black et al. (1997) sequenced the entire 18S rRNA gene and in both cases they were able to infer inter-family phylogenies with high bootstrap values. Since the V4 region appears to contain sufficient conserved sequence for accurate alignment and also sufficient variable nucleotides to provide useful phylogenetic information within phyla (Hillis and Dixon 1991) and lower catego-

RIBOSOMAL 18S AND MITOCHONDRIAL COI SEQUENCES IN PROSTIGMATA PHYLOGENY

ries such as superfamilies (Blair et al. 1998), the same V-4 region was targeted in the present study.

Polymerase chain reaction

MATERIALS AND METHODS

PCR reactions were set up in a volume of 50 µl and contained: 10 mM Tris pH 8.7, 50 mM KCl, 1.5 mM MgSO4, 200 µM each dNTP, 1 µM each of the appropriate forward and reverse primer, 1 µl genomic DNA extracted as above and 2.5 units Taq Polymerase (Promega). Primer combinations and sequences are shown in Table 2. Negative controls in which no DNA template was added were always run to check for contamination of reagents. The PCR annealing temperature was varied while testing different primers, but the most common program used was 94oC 1 min, then 30 cycles of 94oC 20 secs, 50oC 30 secs, 72oC 1 min 30 secs, with a final cycle bringing the temperature down to 25oC. PCR products were analysed on a 1% agarose gel. Successful PCR reactions were cleaned up using either the Promega Wizard PCR clean-up kits, followed by further purification with a Sepharose CL-6B spin column, or using the Qiagen PCR Qiaquick kit. After purification, products were quantified using a Biorad Fluor-S gel imager, and 30–60 ng were sequenced using the Perkin Elmer Ready Reaction kit with AmpliTaq FS or the Perkin Elmer BigDye kit, both according to manufacturer’s instructions. All PCR products were sequenced with both the forward and the reverse PCR primers to verify sequence from both strands.

Taxa analysed

Sequence analysis

Cytochrome oxidase forms part of the respiratory chain in the mitochondrion, and the cytochrome oxidase subunit I (COI) shows strong sequence conservation across taxa (Simon et al. 1994; Lunt et al. 1996). Moreover, the fact that it is a protein coding gene enables ready alignment and taxonomic analysis of amino acid, as well as nucleotide, sequences. COI is known to show a faster rate of sequence divergence than the 18S rRNA gene (Hillis and Dixon 1991; Simon et al. 1994). However, as with the 18S rRNA gene, there is considerable heterogeneity in the rate of substitutions within the gene and amino acid sequence, enabling comparisons to be made at different phylogenetic levels using different regions of the gene (Lunt et al. 1996; Zhang and Hewitt 1996). In the current paper we describe sequencing and analysis of the V4 region of the nuclear 18S rRNA gene and two fragments of the mitochondrial COI gene to evaluate their ability to shed light on the phylogeny of the Prostigmata.

Table 1 lists the prostigmatid mite taxa for which 18S rRNA or COI sequences were obtained. It also includes other acarine and chelicerate species for which sequences were available in public databases and which were also included in parts of our analyses. All specimens for which we obtained sequence were collected in northern Queensland, Australia, mostly in the vicinity of Townsville, except Hydrodroma sp. which was obtained from a pond near Brisbane (southeastern Queensland). All material used for sequencing was identified by J. C. Otto, except Hydrodroma sp. and Anagarypus australianus, which were identified by Heather Proctor (Griffith University) and Mark Harvey (West Australian Museum) respectively. Slide-mounted voucher specimens may be obtained from J. C. Otto on request. The families or higher taxa to which the sequenced specimens belong are highlighted in Fig 3. All sequences obtained in this work have been deposited in Genbank and the accession numbers are given in italics in Table 1.

The corresponding forward and reverse sequences were first aligned using the program Gap (Genetics Computer Group 1994), and any discrepancies were checked on the chromatograms. Sequences were then edited using WebFM programs available on ANGIS and were aligned using Pileup or Eclustalw. Phylogenetic inference

Phylogenetic analysis was conducted using parsimony, distance and maximum likelihood methods as they are implemented in the phylogeny inference programs PAUP 3.1 (Swofford 1991), MEGA 1.0 (Kumar et al. 1993) and PHYLIP (Felsenstein 1993). For bootstrap analyses 500 replicates were used. As outgroup for the 18S analysis we used the scorpion Androctonus australis as it gave the most clear alignment with the Prostigmata of all available chelicerate sequences. For the cytochrome oxidase I analysis we used the mosquito Anopheles quadrimaculatus as outgroup. Abbreviations

Extraction of DNA

A standard CTAB extraction procedure was used (Black et al. 1997). One to 20 mites (depending on size and availability of specimens) were crushed in 400 µl extraction buffer (100 mM Tris-HCl pH 8.0, 1.4 M NaCl, 50 mM EDTA, 2% w/v CTAB) plus 2 µl 1 M DTT in a microfuge tube using a plastic pestle. This was incubated at 60oC for 60 min and then extracted by mixing with 400 µl chloroform to remove proteins and carbohydrates, followed by centrifugation for 5 min to separate the phases. The supernatant was transferred to a fresh tube and 350 µl of isopropanol added to precipitate the genomic DNA. The tube was spun in a microfuge for 5 min, the supernatant discarded and the pellet washed with 250 µl 70% ethanol, and, after respinning and removing the residual 70% ethanol with a pipette, the pellet was dried briefly before resuspending in 20 µl TE (Tris pH 8.0 10 mM, EDTA 1 mM).

ANGIS, Australian National Genomic Information Service; DTT, dithiothreitol; EDTA, ethylene diamino tetra acetic acid; CTAB, hexadecyltriammonium bromide.

RESULTS AND DISCUSSION Potential of the V4 region of the 18S rRNA gene for inferring Prostigmata phylogeny Conserved PCR primers were designed based on the alignment of the tick sequences in Black et al. (1997) and by comparison with other available arthropod sequences. These successfully amplified a single PCR product in all species tested. In the majority of species the product was approximately 480 base pairs (bp) long, as predicted from the tick sequences. However, in three species, Tarsotomus sp., Adamystis sp. and Hydrodoma sp., the PCR products were 500, 540 and 650 bp respectively. This most likely indicates

101

Jürgen C. Otto et al. Table 1

Accession numbers of sequences used in phylogenetic analysis. Sequences obtained in this work are shown in italics.

Non-acarine Chelicerate

18S V4 region

Acarina Prostigmata

COI – region 1

COI – region 2

Adamystidae

Adamystis sp.

AF142104

Anystidae sp. 1

Erythracarus sp.

AF142109

Anystidae sp. 2

Tarsotomus sp.

AF142122

Bdellidae sp. 1

Bdellodes sp. A

AF142118

Bdellidae sp. 2

Bdellodes sp. B

AF142119

Caeculidae sp. 1

Microcaeculus sp.

AF142110

AF142125

Caeculidae sp. 2

Neocaeculus sp.

AF142111

AF142126

AF142134

Erioryhnchidae

Eriorhynchus sp.

AF142116

AF142127

AF142135

Erythraeidae sp. 1

Erythrites sp.

AF142105

AF142129

AF142137

Erythraeidae sp. 2

Erythroides sp.

AF142106

AF142130

AF142138

Halacaridae sp. 1

Agaue sp.

AF142107

Halacaridae sp. 2

Halacaropsis sp.

AF142108

Hydrodromidae

Hydrodroma sp.

AF142112

AF142131

AF142141

Pterygosomatidae sp. 1

Geckobia sp. A

AF142113

Pterygosomatidae sp. 2

Geckobia sp. B

AF142114

AF142139

Rhagidiidae

unidentified genus

AF142117

AF142142

Teneriffiidae

Austroteneriffia sp.

AF142115

AF142143

Trombidiidae

unidentified genus

AF142123

Ixodidae

Rhipicephalus sanguineus

L76342

Ixodidae

Hyalomma rufipes

L76349

Ixodidae

Amblyomma maculatum

L76344

Ixodidae

Aponomma latum

L76347

Ixodidae

Amblyomma tuberculatum

L76345

Ixodidae

Amblyomma variegatum

L76346

Ixodidae

Ixodes affinis

L76350

Ixodidae

Ixodes cookei

L76351

Ixodidae

Ixodes kopsteini

L76352

Ixodidae

Haemaphysalis inermis

L76338

Ixodidae

Dermacentor andersoni

L76340

Ixodidae

Hyalomma dromedarii

L76348

Ixodidae

Haemaphysalis leporispalustris

L76339

Argasidae

Argas persicus

L76353

Argasidae

Argas lahorensis

L76354

Argasidae

Ornithodoros moubata

L76355

Argasidae

Otobius megnini

L76356

Laelapidae

Cosmolaelaps trifidus

L76343

Megisthanidae

Megisthanus floridanus

L76341

Allothyridae

Allothyrus sp.

AF018655

Garypidae

Anagarypus australianus

AF142121

Opiliones sp. 1

unidentified

AF142120

Opiliones sp. 2

Odiellus troguloides

X81441

Ixodida

Mesostigmata

Holothyrida Pseudo-scorpiones

Aranae

Theraphosidae

Aphonopelma sp.

X13457

Scorpiones sp. 1

Buthidae

Androctonus australis

X74761

Scorpiones sp. 2

Buthidae

Mesobuthus martensi

AB008465

Xiphosura

Limulidae

Limulus polyphemus

X90467

Insecta

Culicidae

Anopheles quadrimaculatus

102

AF142132 AF142128

AF142136

AF142124

AF142133

AF142140

L04272

L04272

RIBOSOMAL 18S AND MITOCHONDRIAL COI SEQUENCES IN PROSTIGMATA PHYLOGENY

Table 2

PCR primers used for amplification of fragments of the 18S rRNA and COI genes; W = A or T;Y = C or T; R = A or G; D = A G or T; I = inosine (a base analog which base pairs weakly with all four nucleotides).

Primer name

Sequence

Gene

Source

Mite18S -1F

ATA TTG GAG GGC AAG TCT GG

18S V4 – F

This paper

Mite18S -1R

TGG CAT CGT TTA TGG TTA G

18S V4 – R

This paper

CI-J-1751

GGW GCW CCW GAY ATR GCW TTY CC

COI – region 1

Simon et al. 1994

CI-N-2191

GGW ARA ATT AAA ATA TAW ACT TC

COI – region 1

Simon et al. 1994

Mite COI – 2F

TTY GAY CCI DYI GGR GGA GGA GAT CC

COI – region 2

This paper

Mite COI – 2R

GGR TAR TCW GAR TAW CGN CGW GGT AT

COI – region 2

This paper

phologically based hypothesis (Fig. 3). In all trees obtained from our 18S rRNA data set only the relationships of Erythraeidae + Trombidiidae and of the species belonging to a single family (e.g. Bdellidae sp. 1 + Bdellidae sp. 2) had high bootstrap support, while all other relationships were inadequately supported. This indicates that, except in the Parasitengona, phylogenetic signal is weak or absent between families and superfamilies.

the presence of independent insertions in these three species as the V4 region was a different size in each case, compared to the constant size of the V4 in the other species examined. The alignment of the 18S rRNA sequences appeared straightforward except for the three species with insertions, for which alignment of most sections was unreliable, and they were therefore excluded from the analysis. Fig. 1 shows the sequence of the V4 region for 15 species of Prostigmata and the scorpion Androctonus australis. The aligned region contains 378 nucleotides, of which, excluding the outgroup, 107 are variable and of these 78 are parsimony informative. The values for this region are very similar to those obtained for the 18 tick species sequenced by Black et al. (1997) (see Table 3). The sequence alignment (Fig. 1) shows that most parts of the sequenced fragment are identical in the mites and in the scorpion and that potentially informative sites are restricted to a few regions.

Prostigmatid 18S rRNA data and chelicerate phylogeny

Our Prostigmata 18S rRNA gene sequences add a significant number of chelicerate sequences to those already in public databases and thus may contribute to the discussion of the monophyly / polyphyly of the Acarina and the phylogeny of the Chelicerata. We have aligned our sequences with those of all other chelicerate 18S rRNA sequences, as well as with an opilionid and pseudoscorpion sequenced by us, and performed distance and parsimony analysis on this data set, defining Limulus polyphemus as the outgroup. The distance analysis resulted in a tree (Fig. 4) which shows the suborder Prostigmata as a well supported clade (bootstrap value of 97%) which is the sistergroup to a clade comprised of Parasitiformes and, surprisingly, the pseudoscorpion. A similar result was obtained by parsimony analysis. However, in the latter

We performed maximum likelihood, parsimony and distance analyses on these aligned sequences, the latter using Tamura-Nei, JukesCantor, Kimura 2-parameter, and p-distance algorithms. Fig. 2 shows examples of cladograms obtained using the parsimony and the distance methods. The distance tree (Fig. 2a) differs significantly from the parsimony tree (Fig. 2b) and both differ from the latest morTable 3

Number of variable and parsimony informative sites in sequence fragments used in multiple sequence alignments. Outgroups are excluded.

DNA sequence

Total nucleotides

No of variable nucleotides

Parsimony informative nucleotides

18S V4 Prostigmata (15 sp)a

378

106

79

18S V4 Ixodida (18 sp)b

387

119

89

COI-1 Prostigmata (9 sp)

429

224

161

COI-2 Prostigmata (12 sp)

546

300

229

Protein sequencec

Total amino acids

No of variable amino acids

Parsimony informative amino acids

COI-1 Prostigmata (9 sp)

143

54

36

COI-2 Prostigmata (12 sp)

182

89

56

a) b) c)

this excludes the V4 region from Tarsotomus sp., Adamystis sp. and Hydrodoma sp. as these sequences were not included in the final multiple sequence alignment or phylogenetic analysis data from Black et al. (1997) derived from conceptual translation of the corresponding nucleotide sequences

103

Figure 1

Alignment of the V4 region of the 18S rRNA gene of 15 prostigmatid species and the scorpion Androctonus australis. Nucleotides highlighted in black indicate no variation, in grey indicate little variation and those that are not highlighted indicate high variation. Eryth. = Erythraeidae; Tromb. = Trombidiidae; Halac. = Halacaridae; Anyst. = Anystidae; Caecu. = Caeculidae; Ptery. = Pterygosomatidae; Tener. = Teneriffiidae; Erior. = Eriorhynchidae; Rhagi. = Rhagidiidae; Bdell. = Bdellidae; Scorp. = Scorpiones

Jürgen C. Otto et al.

104

RIBOSOMAL 18S AND MITOCHONDRIAL COI SEQUENCES IN PROSTIGMATA PHYLOGENY

a

99

92 100

36

100

45

12 21

100 53 100

66

17

b

7 100

11

31

96

26 99 46 100

Erythraeidae sp. 1 Erythraeidae sp. 2 Trombidiiae Anystidae sp. 1 Pterygosomatidae sp. 1 Pterygosomatidae sp. 2 Halacaridae sp. 1 Halacaridae sp. 2 Teneriffiidae Caeculidae sp. 1 Caeculidae sp. 2 Eriorhynchidae Rhagidiidae Bdellidae sp. 1 Bdellidae sp. 2 Scorpiones sp. 1

50% majority rule bootstrap consensus trees obtained from the analysis of the 18S rRNA V4 region of 15 prostigmatid species and the scorpion Androctonus australis as outgroup; a, tree obtained using distance analysis (Jukes Cantor distance and neighbour joining treebuilding algorithms); b, tree obtained using parsimony analysis.

the bootstrap value for the position of the pseudoscorpion within the Parasitiformes was insignificant (37%). If this position for the pseudoscorpion was borne out by further analysis it would support the hypothesis that the Acari may be polyphyletic. Potential of Mitochondrial cytochrome oxidase I gene for inferring Prostigmata phylogeny

As part of the exploration for phylogenetically informative sequences, two regions of the mitochondrial cytochrome oxidase I (COI) gene were sequenced. Initially two primers (CI-J-1751 and CI-N-2191) from the set of conserved mitochondrial primers described by Simon et al. (1994) were used to amplify and sequence part of the 5’ region of the gene. However, these primers were only successful in amplifying products from half of the mite species tested. These products were sequenced, but both the nucleotide and amino acid sequences proved phylogenetically uninformative at the level being studied. Subsequently two further primers were designed to amplify a region corresponding to the UEA5 / UEA8 region described by Lunt et al. (1996) and Zhang et al. (1996) as being the region most suitable for longer range phylogenetic comparisons. The forward primer, Mite COI-2F, was designed from the mite sequences that had been obtained from the first COI region sequenced, and the reverse primer, Mite COI-2R, from an alignment of four available arthropod COI sequences. PCR products

ELEUTHERENGONA

20

Figure 2

98

EUPODINA

57

ANYSTINA

46

Erythraeidae sp. 1 Erythraeidae sp. 2 Trombidiidae Halacaridae sp. 1 Halacaridae sp. 2 Caeculidae sp. 1 Caeculidae sp. 2 Anystidae sp. 1 Pterygosomatidae sp. 1 Pterygosomatidae sp. 2 Teneriffiidae Eriorynchidae Rhagidiidae Bdellidae sp. 1 Bdellidae sp. 2 Scorpiones sp. 1

Figure 3

Anystidae Parasitengona Teneriffiidae Caeculidae Adamystidae Labidostommatidae Eupodoidea Tydeoidea Eriophyoidea Bdelloidea + Halacaroidea? Tetranychoidea Cheyletoidea Raphignathoidea Pterygosomatoidea Pomerantzioidea Pseudocheylidae Heterostigmata Stigmocheylidae Paratydeidae

Most recent morphology based cladogram of Prostigmata (Norton et al. 1992). Taxa for which we obtained sequence data are highlighted. The Parasitengona contains the families Erythraeidae and Trombidiidae. The families Eriorhynchidae and Rhagidiidae belong to the Eupodoidea.

and DNA sequences were obtained from 12 mite species and the alignment of amino acid sequences from this region is shown in Fig. 5. However, as with the first COI region sequenced, it was not possible to obtain trees with high bootstrap support for any of the clades, other than the node leading to the two Erythraeid species (these were the only two COI region 2 sequences obtained from species within the same family). This was the case both for analysis of the nucleotide sequence, including analysis only of synonymous substitutions (those which do not alter the encoded amino acid) and the translated amino acid sequence. The reason for this lack of support for any of the trees generated using the COI data appears to be homoplasy due to saturation of possible substitutions. This is supported by the low transition/transversion ratios obtained for all pairwise comparisons (most being less than 1), which indicates saturation of substitutions (Wakely 1996). Second, the number of variable nucleotides is very high, even between members of the same family – for example comparison of the sequence of COI region 1 between Caeculid species 1 and Caeculid species 2 shows that they differ at 86 nucleotides out of 429 (although the prevalence of synonymous substitutions means that only 7 amino acids out of 143 differ), indicating a substantial rate of nucleotide substitution. By contrast, these two species differ by only two nucleotides out of all 378 nucleotides aligned for the 18s rRNA region. Third, the overall pattern of amino acid variation was very similar to that

105

Jürgen C. Otto et al.

81 100 99

46 100

Parasitiformes

100

30

71 Mesostigmata

Prostigmata

Figure 4

97

50% majority rule consensus tree of a bootstrap distance analysis (500 replicates, using Jukes Cantor distance and neighbour joining treebuilding algorithms) of Prostigmata, Parasitiformes and other chelicerates. * Although Pseudoscorpiones appears on the branch indicated in this particular phylogenetic tree, it does not belong to either the Mesostigmata or the Parasitiformes.

described by Lunt et al. (1996) for this region of COI sequence from nine insect species spanning three orders (Diptera – six species, Orthoptera, two species and Hymenoptera, one species), with three areas of high variation surrounding more conserved regions of the protein. However, the actual extent of variation is considerably greater at individual positions between the mite families sampled than between the different orders of insects (Fig. 6). This latter observation indicates either that the mite families diverged well before the insect orders, or that the mites show accelerated rates of substitution. The inability of COI sequence to resolve family relationships within the prostigmatid family Tetranychidae was also observed by Navajas et al. (1996).

CONCLUSIONS We obtained DNA sequence from the 18S rRNA gene V4 region and two fragments of the mitochondrial COI gene from a number of mite species representing different prostigmatid fami-

106

56

Rhicicephalus sanguinensis Hyalomma dromedarii Hyalomma rufipes Dermacentor andersoni Haemaphysalis leporispalustris Haemaphysalis inermis Amblyomma tuberculatum Amblyomma variegatum Aponomma latum Amblyomma maculatum Ixodes cookei Ixodes affinis Ixodes kopsteini Argas lahorensis Argas persicus Ornithodoros moubata Otobius megnini Allothyrus sp. Cosmolaelaps trifidus Megisthanus floridanus Pseudoscorpiones* Erythraeidae sp. 1 Erythraeidae sp. 2 Trombidiidae Halacaridae sp. 1 Halacaridae sp. 2 Caeculidae sp. 1 Caeculidae sp. 2 Anystidae sp. 1 Teneriffiidae Bdellidae sp. 1 Bdellidae sp. 2 Rhagidiidae Eriorhynchidae Pterygosomatidae sp. 1 Pterygosomatidae sp. 2 Scorpiones sp. 1 Scorpiones sp. 2 Aranae Opiliones sp. 2 Opiliones sp. 1 Limulus polyphemus

lies and superfamilies. The sequences obtained from both of these gene sequences gave support to the monophyly of families (see Fig. 2 for the 18S results) and the 18S sequence gave support to the monophyly of the suborder Prostigmata within the Chelicerata (see Fig. 4). By contrast neither sequence was able to resolve relationships between families or superfamilies of Prostigmata. The one exception was the relationship between the families Trombidiidae and Erythraeidae, each representing a different superfamily within the Parasitengona, which was supported by a bootstrap value of 92% in the distance tree. The fact that the close relationship of species belonging to the same family is consistently reflected in the molecular data, and that bootstrap values for these clades are very high, suggests that 18S V4 and COI may be useful for testing the monophyly of families. The reason for the lack of resolution of family / superfamily relationships appears to be that most parts of the sequenced

Figure 5

Alignment of COI region 2 amino acid sequences. Eryth. = Erythraeidae; Rhagi. = Rhagidiidae; Erior. = Eriorhynchidae; Caecu. = Caeculidae; Halac. = Halacaridae; Hydro. = Hydrodromidae; Anyst. = Anystidae; Adamy. = Adamystidae; Tener. = Teneriffiidae; Bdell. = Bdellidae; Anoph. = Anopheles (outgroup); Ptery. = Pterygosomatidae. Amino acids highlighted in black indicate no variation, in grey indicate little variation and those that are not highlighted indicate high variation.

RIBOSOMAL 18S AND MITOCHONDRIAL COI SEQUENCES IN PROSTIGMATA PHYLOGENY

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Jürgen C. Otto et al.

Figure 6

Amino acid variability in region 2 of the COI gene: a, insect sequences, including six Diptera, two Orthoptera and one Hymenoptera species (data from Lunt et al. 1996); b, the 12 species of prostigmatid mites indicated in Table 1.

fragments are either so highly conserved that all investigated taxa are identical, or they are so variable that nucleotide changes have reached saturation and have overwritten any phylogenetic signal. By contrast, within families, the phylogenetic signal at the variable nucleotides has not yet been obscured by homoplasy, and at the level of suborders there is sufficient variation in the more highly conserved segments of the V4 region to generate useful phylogenetic signal. To obtain the desired phylogenetic resolution between families, it will therefore be necessary to sequence more conserved gene regions. This is possible with the 18S rRNA gene, as the V4 region is one of the more variable regions of this gene. However, there are no regions of the COI gene that are more conserved than those already sequenced, and hence the COI gene will not prove useful for this level of phylogeny.

ACKNOWLEDGEMENTS We thank Mark Harvey for identifying the pseudoscorpion, Heather Proctor for providing the specimens of Hydrodroma and David Blair for discussions on molecular phylogeny. In part this work made use of the facilities of ANGIS. This publication is contribution 953 of the Australian Institute of Marine Science.

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REFERENCES Black, W. C., Klompen, J. S. H., and Kierans, J. E. (1997). Phylogenetic relationships among tick subfamilies (Ixodida:Ixodidae:Argasidae) based on the 18S nuclear rDNA gene. Molecular Phylogenetics and Evolution 7, 129–144. Blair, D., Bray, R. A., and Barker, S. C. (1998). Molecules and morphology in phylogenetic studies of the Henmiuroidea (Digenea: Trematoda: Platyhelminthes). Molecular Phylogenetics and Evolution 9, 15–25. Crampton, A., McKay, I., and Barker, S. C. (1996). Phylogeny of ticks (Ixodida) inferred from nuclear ribosomal DNA. International Journal for Parisitology 26, 511–517. Felsenstein, J. (1993). PHYLIP (Phylogeny Inference Package). (Department of Genetics, University of Washington, Seattle.) Genetics Computer Group (1994). ‘Program manual for the Wisconsin Package. Version 8.0. (Genetics Computer Group: Madison, Wisconsin.) Hillis, D. M., and Dixon, M. T. (1991). Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly Review of Biology 66, 411–453. Krantz, G. W. (1978). ‘A Manual of Acarology.’ (Oregon State University Book Stores: Corvallis.) Kumar, S., Tamura, K., and Nei, M. (1993). ‘MEGA: Molecular Evolutionary Genetics Analysis. Version 1.0.’ (The Pennsylvania State University: Philadelphia.)

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Lunt, D. H., Zhang, D.-X., Szymura, J. M., and Hewitt, G. M. (1996). The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Molecular Biology 5, 153–165. Navajas, M., Gutierrez, J., and Lagnel, J. (1996). Mitochondrial cytochrome oxidase I in tetranychid mites: a comparison between molecular phylogeny and changes of morphological and life history traits. Bulletin of Entomological Research 86, 407–417. Norton, R. A., Kethley, J. B., Johnston, D. E., and OConnor, B. M. (1992). Phylogenetic perspectives on genetic systems and reproductive modes of mites. In ‘Evolution and diversity of sex ratio in insects and mites’. (Eds D. L. Wrench and M. A. Ebbert.) pp. 8–99. (Chapman and Hall: New York.) Schlegel, M. (1994). Molecular phylogeny of eukaryotes. Trends in Ecology and Evolution 9, 330–335.

Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., and Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–686. Swofford, D. L. (1991). ‘PAUP: Phylogenetic Analysis Using Parsimony. Version 3.1.1. (Illinois Natural History Survey: Champaign.) Turbeville, J. M., Pfeifer, D. M., Field, K. G., and Raff, R. A. (1991). The phylogenetic status of the arthropods as inferred from 18S rRNA sequences. Molecular Biology and Evolution 8, 669–686. Wakely, J. (1996). The excess of transitions among nucleotide substitutions: new methods of estimating transition bias underscore its significance. Trends in Ecology and Evolution 11, 158–163. Zhang, D.-X. and Hewitt, G. M. (1996). Assessment of the universality and utility of a set of conserved mitochondrial COI primers in insects. Insect Molecular Biology 6, 143–150.

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ACAROLOGY: PROCEEDINGS OF THE 10TH INTERNATIONAL CONGRESS

ACARINE BIOGEOGRAPHY AND BIODIVERSITY

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

ACHILLES AND THE MITE: ZENO’S PARADOX AND RAINFOREST MITE DIVERSITY

Department of Zoology and Entomology, The University of Queensland, St Lucia, Queensland 4072, Australia, [email protected]

....................................................................................................

David Evans Walter

.................................................................................................................................................................................................................................................................

Abstract The belief that small size is positively correlated to high diversity has sustained a hypothesis of hyperdiversity in the Acari that has not been supported by studies of Northern Hemisphere acarofaunas. If mites are ‘megadiverse’, then acarine species richness in the tropics must be significantly higher than in other climatic zones. Based on studies in subtropical to tropical rainforests in Australia, this does appear to be true. Even extensive collections within strictly defined habitats do not adequately estimate local species richness, and sampling the same habitat across the landscape results in the continual accumulation of new species. The reasons for higher levels of acarine diversity in subtropical to tropical systems are not immediately apparent. Local assemblages of mites are characterised by small body size (e.g. adults of 52% of 415 species from a subtropical rainforest were less than half a millimetre in length), but this is also true of temperate zone assemblages. However, geographical and microhabitat distributions in tropical assemblages appear to differ significantly from those in temperate zone. These differences may reflect different levels of host diversity, host specificity, and microhabitat specificity in tropical mites.

INTRODUCTION May (1978, 1988) speculated that insects were highly diverse because they were small, and that very small species such as mites may be even more diverse than insects. Although the number of described species of mites is similar to that of their much larger relatives, the spiders, recent estimates of true acarine diversity are up to twenty times higher, i.e. one million species (Hammond 1992; Walter and Proctor 1998). Thus, any attempt to estimate global biodiversity must face the spectre of mite megadiversity (Walter and Proctor 1998). Or perhaps, poltergeist would be a better allusion, because more noise than hard data exists to support these claims. In temperate regions, the acarofaunas are certainly diverse, but not exceptionally so. For example, Canada is estimated to have fewer than 10,000 species of mites (Lindquist 1979), and America north of Mexico only 30,000 (OConnor 1990). If the Acari is a hyperdiverse group (i.e. >100,000 species,

Hammond 1992), then the bulk of acarine biodiversity must reside in the tropics. The species diversity of any group has two major components (Colwell and Coddington 1994). The first is the number of species in a particular habitat (local richness), and the second is the distinctness of assemblages in different habitats, sites or times (complementarity). Both rich and complementary assemblages of mite species are prerequisites of global mite megadiversity. However, assessing the local richness of mites is difficult, because we tend to define habitats in terms of much larger organisms. For example, determining the species richness of birds in a patch of rainforest would not be an especially daunting task. Three major habitats immediately come to mind – the leafy canopy, the understorey, and the ground – and mist nets and counts (visual and aural) suggest themselves as appropriate sampling methods. However, attempts to tally the mite species

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in the same forest patch immediately founder on the question of what habitats to sample. For very small organisms such as mites, there may be no simple answer to this question. Consider the birds themselves, as one obvious mite habitat in this hypothetical forest patch. Birds are not one, but a complex of mite habitats, e.g. nests, internal body, outer surface. On closer examination, however, each of these can be further subdivided, e.g. the outer body into skin, leg scales and feathers; feathers into body contour, wing and tail; each feather into quill and barbules. The more closely one looks at a presumed mite habitat, the more microhabitats one finds – a seemingly limitless subdivision of space, rather like the gap between Achilles and the Tortoise in Zeno’s paradoxical race (Grünbaum 1967). Presumably there are limits to the degree that mites can partition habitat space, but these may be pre-empted by the limits of the investigator’s imagination. Until they were first discovered, who would have thought to look for mites inside feather shafts, turtle cloacae, crab gills, bee tracheae, moth ears, the stink glands of bugs or any of the myriad other unexpected microhabitats exploited by mites? Given the limits of my own imagination, I have been assessing the microhabitat and size distributions of mites in subtropical to tropical rainforests in Queensland, Australia. For practical reasons, I have limited my explorations to a minute proportion of the possible microhabitats used by mites, and I have concentrated on those taxa that I know well enough to be reasonably sure that I am able to recognise specific differences. In this paper, I investigate microhabitat partitioning and size distributions of mites in temperate to tropical Australia, and their relationship to estimates of global mite diversity.

MATERIALS AND METHODS My study sites were rainforests in three regions of eastern Australia: warm-temperate rainforest in Victoria (38°S), subtropical rainforest in south east Queensland (26–28°S), and tropical rainforest in far north Queensland (17°S). Mite identifications were based on specimens cleared in Nesbitt’s solution, mounted in Hoyer’s or Heinze PVA medium on glass slides and studied under differential interference microscopy using a Zeiss Axioskop. Voucher specimens are maintained in the University of Queensland Insect Collection, St Lucia, Queensland 4072, Australia. Mites on leaves of tulip oak

Tulip oak, Argyrodendron peralatum (Bailey) Edlin ex I.H. Boas, is a large sterculiaceous tree growing in rainforests in Far North Queensland. Its trifoliate leaves are leathery and have a smooth, glossy upper surface and a lower surface covered with appressed scales. Using extendable pole-pruners, I sampled 12 leaves from the lower to mid crowns of each of 15 tulip oaks at various sites on the Atherton Tablelands in far north Queensland. Each leaf was examined under a microscope (to 40×) and all mites were identified to morphospecies and counted. Mesostigmatans were collected into alcohol for later slide-mounting. Temperate vs tropical foliar mite assemblages

The diversity of mite species on leaves with smooth surfaces was compared to that on leaves covered with a dense tomentum of

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erect hairs at one temperate and one tropical rainforest site in eastern Australia. The temperate site was a pocket of warm-temperate rainforest along Chinaman Creek in Wilson’s Promontory National Park, Victoria (38° 55'S, 146° 23'E). In late November (late spring), extendable pole pruners were used to sample leaves from the mid to upper crowns of two small evergreen tree species: the blue olive-berry, Elaeocarpus reticulatus Smith (Elaeocarpaceae), with smooth leaves with pocket domatia and hazel pomaderris, Pomaderris aspera Sieb. ex DC (Rhamnaceae), with leaves covered in a dense stellate tomentum. The tropical site was located in a remnant pocket of tropical rainforest at the Curtain Fig Research Tower maintained by the CSIRO near Yungaburra on the Atherton Tablelands (17°17'S, 145°35'E). In April, lower crown samples from tulip oak were obtained with pole pruners, and the tower allowed access to the mid to upper crowns (to ca. 35 m) of both tulip oak and tamarind, Diploglottis diphyllostegia (F. Muell.) (Sapindaceae). The latter has large (> 50 cm), pinnately compound leaves covered with a dense tomentum of erect hairs. Mesostigmata in fungal sporocarps on logs

Over a four year period, samples of 250–500 cm3 of decaying fungal sporocarps on logs and stumps in subtropical rainforests in south east Queensland were collected, placed on paper towelling in plastic tubs, and incubated at room temperature for 4–6 weeks. As populations of mesostigmatans developed, representative individuals were collected and slide mounted for identification. At the end of the incubation period, remnants of sporocarps and towelling were placed in simple Berlese funnels under 40 watt incandescent bulbs and any remaining mites were extracted into 80% ethanol. Size distribution of Acari from Lamington National Park

Body sizes of adult female mites from subtropical forest in the Green Mountains (28°15'S, 153°08'E) section of Lamington National Park, Queensland were estimated to the nearest 5 µm by measuring along the midline with an ocular micrometer at 100×. If a series of specimens was available, then the median length was used. Mites were collected over a 10-year period using a variety of collecting techniques including pyrethrum knockdown, bark spraying, leaf and stem collections, rearings from fungal sporocarps, hand collection of large arthropods, kick sampling in stream, and Berlese funnel extraction of litter (Kitching et al. 1993; Walter and Proctor 1998; Walter et al. 1998). Statistical analyses

Summary statistics are presented as means ± one standard error. Local richness was evaluated using collector’s curves, i.e. graphing accumulated species number versus accumulated sampling effort. The program EstimateS 5.0 (available from R. K. Colwell, Department of Ecology and Evolutionary Biology, University of Connecticut, U-42, Storrs, CT 06269-3042, USA or [email protected]) was used to generate points based on 50 randomisations of sampling order. The second component of species richness, complementarity, was calculated as the percentage of species unique to a collection (C = [unique species / total

ACHILLES AND THE MITE: ZENO’S PARADOX AND RAINFOREST MITE DIVERSITY

Figure 1

Collector’s curve for foliar mite species from 15 tulip oaks Argyrodendron peralatum (Bailey) Edlin ex I.H. Boas from tropical rainforest sites on the Atherton Tablelands in far north Queensland, Australia. Each point is the mean ± standard error cumulative species per leaf for a 12 leaf sequential sample and is plotted against the average number of individual mites per leaf.

species] × 100) (see Colwell and Coddington 1994). These values potentially range from zero, when the species sampled from two habitats are identical, to completely distinct biotas (C = 100%). Histograms were based on 10 size classes, beginning with the smallest species.

RESULTS Mites of leaves of Argyrodendron peralatum

The 180 leaves taken from tulip oak at 15 sites contained 1379 mites, and an average leaf was inhabited by 7.7 ± 0.5 mites representing 3.8 ± 0.2 species (range = 0–10). An average sample of 12 leaves contained 92 mites representing 15 species. Considering the steep slope of the collector’s curve in Figure 1, it is clear that a dozen leaves is not enough to estimate the number of species of foliar mites on tulip oak at a site. Larger samples would continue to accumulate new species, but how many is impossible to say because the curve does not approach an asymptote. Comparing species identities across the entire sample of 15 tulip oaks was not possible, but I did determine ST (total species) for the Mesostigmata. On average, 20 ± 1% of the species collected from a single tree were Mesostigmata. Across all 15 trees, a total of 16 species in six genera (Asca – 3 spp. , Lasioseius – 3 spp. , Amblyseius s.l. – 7 spp, Paraamblyseius sp., Neoseiulella sp. Caliphis sp.) were identified. If the remainder of the foliar mite fauna of tulip oak

was similarly diverse, then about 80 species of mites would have been present on the 180 leaves from these 15 trees. Temperate vs tropical foliar mite assemblages

Nearly tripling sample size to 35 leaves from the tulip oaks at the Curtain Fig Tower collected nearly five times as many mites and almost twice as many species as the average from a 12 leaf sample (Table 1). The average number of mites per leaf at Curtain Fig was more than a third higher than the average from the 15 other samples from the Atherton Tableland, but the mean number of species per leaf, and its range, were similar. The collector’s curve for 50 randomisations of these samples is shown in Figure 2. Although no asymptote is reached, the rate of climb does appear to be gradually decreasing. In comparison, the collector’s curve for the tamarind growing next to the tulip oak climbs less steeply, but is continuing to climb even after 1431 mites have been examined. An average tamarind leaf (N = 15) contained about seven times as many mites and twice as many species as a tulip oak leaf (Table 1). In total, 27 species of mites were identified from the tamarind tree, but only 8 of these species (in the Tarsonemidae, Tydeidae, Cunaxidae, and Symbioribates sp. in the Oribatida) were also collected from the tulip oak. Therefore, the 50 leaves sampled from the leaves of these two adjacent trees contained 1884 mites representing

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Figure 2

Collector’s curves for foliar mites from tulip oak (Argyrodendron peralatum (Bailey) Edlin ex I.H. Boas) and tamarind (Diploglottis diphyllostegia (F. Muell.)) from tropical rainforest and blue olive-berry (Elaeocarpus reticulatus Smith) and hazel pomaderris (Pomaderris aspera Sieb. ex DC) from warm-temperate rainforest in eastern Australia. Each curve represents the average cumulative number of species plotted against average number of individuals per leaf for 50 randomisations of collection order (EstimateS 5.0).

47 species of mites, and the assemblages collected from the two trees were 85% complementary. Results from the two species of warm-temperate rainforest tree sampled at Chinaman Creek are similar in that the mite faunas of the two trees are highly complementary (78%). Also, leaf by leaf diversity of foliar mites was similar to that on the tropical trees, and the hairy-leaved trees averaged about twice as many species per leaf as the smooth-leaved species (Table 1). However, other aspects of foliar mite diversity at this site are quite different. Although 2771 mites were collected from the 110 leaves examined, i.e. 887 more mites than in the tropical samples, only 27 species of foliar mites were identified (vs 47 species in the tropical samples). Also, the collector’s curves for both temperate species are approaching asymptotes, i.e. most of the foliar mites on these trees at this site were collected. Table 1

Mesostigmata in fungal sporocarps on logs

A total of 43 species of Mesostigmata representing 10 described families (Ascidae, Celaenopsidae, Cercomegistidae, Digamasellidae, Laelapidae, Macrochelidae, Ologamasidae, Sejidae, Triplogyniidae, Uropodidae) and one new family in the Cercomegistina were identified from the 40 samples of rotting fungal sporocarps. An average sample contained 3.4 ± 0.5 species (range = 0–12). As with the tropical samples from leaves, the collector’s curve (Figure 3, top curve) climbs steeply and does not reach an asymptote; therefore, the true number of species of mesostigmatans associated with sporocarps in south east Queensland is likely to be much higher. Excluding 11 species of Uropodidae as taxonomically intractable, the remaining species of mites of rotting fungal sporocarps were compared to the author’s extensive collections from many different habitat types in Queensland and northern New South Wales. Most of these 32 species fall into three distinct

Abundance and diversity of foliar mites on leaves of trees at a tropical and a warm-temperate rainforest site in Australia. Tulip oak (Argyrodendron peralatum (Bailey) Edlin ex I.H. Boas) and blue olive berry (Elaeocarpus reticulatus Smith) have smooth leaf surfaces, while tamarind (Diploglottis diphyllostegia (F. Muell.)) and hazel pomaderris (Pomaderris aspera Sieb. ex DC) have dense tomenta. Means ± standard errors (range).

Rainforest/tree

Mites/leaf

Total Mites

Species/leaf

ST

N

tulip oak

13 ± 0.2

453

3.9 ± 0.6 (0–9)

28

35

tamarind

95.4 ± 3.2

1431

8.1 ± 0.2 (2–14)

27

15

Tropical

Warm-temperate blue-olive berry

21.3 ± 4.6

1277

2.6 ± 0.2 (0–9)

15

60

hazel pomaderris

29.9 ± 4.3

1494

4.1 ± 0.2 (1–8)

18

50

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ACHILLES AND THE MITE: ZENO’S PARADOX AND RAINFOREST MITE DIVERSITY

Figure 3

Collector’s curves for all species of Mesostigmata and for confirmed mycetophiles (i.e. specialists on decaying fungal sporocarps) reared from rotting fungal sporocarps in subtropical rainforest in south east Queensland, Australia. Each curve represents the average cumulative number of species plotted against average number of individuals per leaf for 50 randomisations of collection order (EstimateS 5.0).

groups. Half (16) of these species were found in only a single sample of rotting fungi, and of these, half appear to have strayed from more general soil-litter habitats (e.g. species of Antennolaelaps, Asca, Cosmolaelaps, Gamasiphis, Laelaspis, and Proctolaelaps). The remaining eight unique species, however, included a specialist on living polypores (Hoploseius australianus Walter) and seven species that are characteristically found associated with tree trunks, logs and fungal sporocarps (species of Celaenopsis, Cercomegistus, Dendrolaelaps, and Lasioseius). Most of the 16 species found in two or more samples form phoretic associations with insects associated with dead wood or fungi (species of Dendrolaelaps, Digamasellus, Funkotriplogynium, Lasioseius, Macrocheles, Sejus, and Zerconopsis). However, four species (Asca, Acugamasus, and Cosmolaelaps) are not known to form phoretic associations with insects, and may represent soil mites that readily colonise more exposed habitats on dead wood or bark. Therefore, excluding Uropodina, the Hoploseius that feeds on living sporocarps (Walter 1998), and the dozen species that may represent more general elements of the soil-litter fauna, 19 ‘mycetophilic’ species of Mesostigmata were found associated with Table 2

40 samples of rotting fungi on logs in south east Queensland. The collector’s curves for these mycetophiles (Figure 3, lower line) rises less steeply than the curve for all species, but still does not reach an asymptote. Therefore, even eliminating species that may be accidental or transient in the log-sporocarp habitat does not result in a clear estimate of ST. Size distribution of Acari from Lamington National Park

I obtained body length estimates for 415 species of mites from the Green Mountains section of Lamington National Park. Parasitiform mites were significantly larger than either sarcoptiform or trombidiform mites (Table 2), primarily because acariform mites dominated the small end of the size range and because of the relatively large size of the beetle-associated mesostigmatans and of ticks. For example, the six largest species of mites were equally divided between the passalid-associated genus Megisthanus and the tick genus Ixodes. Only one of the 27 species less than 250 µm in length was a mesostigmatan, the remainder were Eriophyoidea,

Size distributions (in µm) of adult females of 415 species of Acari from rainforest habitats in Lamington National Park, Queensland, Australia. Mean ± SE

Minimum

Maximum

N

All Acari

588 ± 22

140

5000

415

Parasitiformes

693 ± 41

240

5000

183

Acariformes Sarcoptiformes

485 ± 19

180

1300

153

Trombidiformes

543 ± 47

140

2120

79

117

Figure 4

Number of species per size class for adult mites from subtropical forest in the Green Mountains section of Lamington National Park, Queensland, Australia. Body lengths were measured along the midline to the nearest 5 µm and each distribution was partitioned into 10 size classes.

David Evans Walter

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ACHILLES AND THE MITE: ZENO’S PARADOX AND RAINFOREST MITE DIVERSITY

Tarsonemidae and Oribatida. Size distributions of major taxa are shown in Figure 4. Overall, more than half (52%) of all mite species were < 500 µm in length and diversity decreased with increasing size, at least above the penultimate size class.

habitat specificity appears to be a major component of mite diversity (Walter et al. 1998; Walter and Behan-Pelletier 1999). Leaf surfaces are further enriched by a host of small insects that add structural components (e.g. scale insects and psocids), and a larger diversity of possible prey.

DISCUSSION

Most mites truly are small. The median body length at Lamington was 480 µm, and 79 species (19%) were less than 317 µm in length. They fell below the smallest size class that May (1978, 1988) used in his famous analysis of size distribution in terrestrial animals. To animals this small, even seemingly simple habitats such as the surface of a leaf or passalid beetle (Seeman, this volume) may contain a cornucopia of microhabitats. Therefore, May (1978, 1988) was right to suggest that tropical mites contain an untold wealth of biological diversity, but just how rich is the acarine branch on the tree of life? This question cannot be seriously addressed until we know more about host and microhabitat specificity in tropical mites. Focussing on these issues is not as esoteric as it may sound, because these factors are of overwhelming importance in the use of mites as biological control agents and in understanding the potential for tropical species to become pests.

I have used one of Zeno of Elea’s more famous paradoxes to emphasise the highly fractal nature of mite microhabitat use, i.e. attempting to quantify mite microhabitats becomes bogged down in their seemingly infinite reduction. Although Zeno’s arguments addressed the reality of motion (Faris 1996), the image of Achilles endlessly narrowing the gap between himself and the tortoise, but never catching up, seems especially appropriate for those who attempt to assess mite species richness in tropical rainforests. Even when habitats are strictly defined and assemblages are purged of possible transients (e.g. the lower curve in Figure 3), asymptotes on collector’s curves remain elusive. When these samples are from across the landscape (Figs 1, 3), then the restricted geographical distribution of species is likely to be a major contributing factor (Walter and Proctor 1998). The same pattern within a site (Figure 2) is less easy to explain. Obviously, any particular site and habitat must have a true species richness at any point in time and, given enough effort, collector’s curves must eventually reach an asymptote. Approaching this level is possible in temperate forests (Fig. 2). In the Australian tropics, however, the amount of effort needed to bring a collector’s curve to an asymptote is extraordinary, and provides strong support for the hypothesis that tropical mites are hyperdiverse. Host specificity is one possible factor influencing high levels of tropical mite diversity. Because more host species are present in tropical areas, more mite species can exist. However, I controlled for host diversity by examining only two species of trees at each site. In this case, the number of plant-parasitic species per host does not appear to be higher in the tropical samples, because only two of the 47 tropical species (4%) were herbivores, both from the tamarind. The thick-skinned tulip oak leaves appear to be immune to plant-parasitic mites (none were found on the 15 tulip oaks sampled at other sites either). In the temperate samples, five of the 27 species of foliar mites (19%) were plant-parasites, two species from pomaderris and three from olive-berry. From these limited samples, therefore, one can hypothesise that most forest trees in Australian rainforests are likely to have 2–3 species of plant-parasitic mites living on their leaves; other plant-parasites are likely to be found in buds, small stems and other sites (Walter et al. 1994; Walter and O’Dowd 1995). Because tree species diversity is much greater in tropical Australia, overall plant-parasitic mite diversity should be greater as well. The vast majority of foliar species assemblages on these four species of trees were predators and scavenger-microbivores (Walter et al. 1994; Walter and O’Dowd 1995), and these mites appear to be more than twice as diverse per ‘host’ in the tropics. Why should tropical predatory and scavenging mites inhabiting leaves be so much more diverse? One possible answer is that tropical leaves have more microhabitats than temperate leaves because they accumulate a more diverse range of epiphylls (fungi, algae, lichens and bryophytes). Micro-

ACKNOWLEDGEMENTS This paper summarises research conducted over a number of years in collaboration with several students and colleagues. I’d especially like to thank Heather Proctor, Owen Seeman, Denis Rodgers, Roger Kitching, Dennis O’Dowd, and Jenny Beard for their help. This research was supported by the Australian Research Council.

REFERENCES Colwell, R. K., and. Coddington, J. A. (1994). Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London B 345, 101–118. Faris, J. A. (1996). ‘The Paradoxes of Zeno.’ (Avebury: Sydney.) Grünbaum, A. (1967). ‘Modern Science and Zeno’s Paradoxes.’ (George Allen and Unwin: London.) Hammond, P. M. (1992). Species inventory. In ‘Global Biodiversity, Status of the Earth’s Living Resources.’ (Ed. B. Groombridge.) pp. 17–39. (Chapman and Hall: London.) Kitching, R. L., Bergelson, J. M., Lowman, M .D., McIntyre, S. and Carruthers, G. (1993). The biodiversity of arthropods from Australian rainforest canopies: General introduction, methods, sites and ordinal results. Australian Journal of Ecology 18, 181–191. Lindquist, E. E. (1979). 12. Acari. Introduction. Memoirs of the Entomological Society of Canada 108, 252–256. May, R. M. (1978). The dynamics and diversity of insect faunas. In ‘Diversity of Insect Faunas.’ (Eds L. A. Mound, N. Waloff.) pp. 188–204. (Blackwell Scientific Publications: Oxford.) May, R. M. (1988). How many species are there on earth? Science 241, 1441–1449. OConnor, B. M. (1990). The North American Acari: Current status and future projections. In ‘Systematics of the North American Insects and Arachnids: Status and Needs.’ (Eds M. Kosztarab and C. W. Schaefer.) pp. 21–29. (Virginia Agricultural Experiment Station Information Series 90–1: Blacksburg.) Seeman, O. (2001). Myriad Mesostigmata associated with log-inhabiting arthropods. In ‘Acarology: Proceedings of the 10th Annual Congress’ (Eds R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff.) pp. 272–276. (CSIRO Publishing: Melbourne.)

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David Evans Walter Walter D. E. (1998). Hoploseius australianus, sp. nov. (Acari: Mesostigmata: Ascidae), a unique element in the Australian acarofauna. The Australian Entomologist 25, 69–74. Walter, D. E., and Behan-Pelletier, V. (1999). Mites in forest canopies: Filling the size distribution shortfall? Annual Review of Entomology 44, 1–19. Walter, D. E., and O’Dowd, D. J. (1995). Beneath biodiversity: Factors influencing the diversity and abundance of canopy mites. Selbyana 16, 12–20.

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Walter, D. E., O’Dowd, D. J., and Barnes, V. (1994). The forgotten arthropods: Foliar mites in the forest canopy. Memoirs of the Queensland Museum 36, 221–226. Walter, D. E., and Proctor, H. C. (1998). Predatory mites in tropical Australia: Local species richness and complementarity. Biotropica 30, 72–81. Walter, D. E., Seeman, O., Rodgers, D., and Kitching, R. L. (1998). Mites in the mist: how unique is a rainforest canopy knockdown fauna? Australian Journal of Ecology 23, 501–508.

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

CLOSELY RELATED SPECIES OF PARASITENGONAE (ACARI: PROSTIGMATA) INHABITING THE SAME AREAS: FEATURES FACILITATING COEXISTENCE

Institut für Zoologie, Freie Universität Berlin, Königin-Luise-Strasse 1-3, D-14195 Berlin, Germany email: [email protected]

....................................................................................................

Andreas Wohltmann

.................................................................................................................................................................................................................................................................

Abstract From samples taken at different localities in northern Germany during the years 1989–1997 it became evident that parasitengone mites belonging to the same genus often occur sympatrically. Thirty-seven species were found, belonging to 25 genera, of which 26 species were examined with regard to the validity of species status, their life history and their environmental demands. In all of the closely related co-occurring species, most characters (e.g. nutrition of postlarval instars) are only slightly differentiated or identical whereas interspecific differences were found concerning the parasitic phase of the larvae (e.g. host range, annual appearance of larvae). This is an indication of the strong selection pressure correlated with larval parasitism occurring today and which had occurred during the evolutionary history of the main parasitengone subgroups. The data show that those taxa of Parasitengonae which have retained the ancestral life-style and type of parasitic association, differentiation in larval parasitism has been the key process facilitating co-occurrence of closely related species in the same biotope.

INTRODUCTION The species niche according to Hutchinson is a multidimensional hypervolume which includes the total of environmental interactions and interdependencies of a given species. It is widely accepted that the niches of different species may be more or less overlapping, but cannot be identical in all niche parameters (Begon et al. 1996). This is because identical niches would result in interspecific competition for identical resources, which consequently would lead to the extinction of one of the species or to character displacement. Closely related species often display a high degree of niche identity owing to their shared evolutionary heritage. If such species have the same microhabitat and occur at the same localities, they ought to be differentiated with respect to the main limiting resource. Therefore, one appropriate way of recognising this very limiting resource and detecting the main selection pressure, is to consider closely related species inhabiting the same area. Moreover, repetitions of such comparisons in

higher taxonomic groups allow for an estimate of the constancy of selection pressures throughout the course of their evolution. Parasitengonae constitute one of the most diverse taxa of the Prostigmata, inhabiting a broad range of biotopes including limnic waters and desert areas. Major subgroups of the Parasitengonae are the aquatic Hydrachnidia and the terrestrial Trombidia. The latter includes the Trombidioidea, Calyptostomatoidea and Erythraeoidea. In general, Parasitengone mites are characterised by their complex life-cycle which includes a parasitic larva, a quiescent (calyptostatic) proto- and tritonymph and an active predatory deutonymph and adult. Most reports on the species assemblages of Parasitengonae at particular localities refer to water mites inhabiting limnic waters (e.g. Piecynski 1976; Böttger and Völkl 1987; Davids et al. 1994; Böttger and Martin 1995). Few data are available concerning the terrestrial groups (Franke 1940; Willmann 1951; Gabrys 1996), and

121

122

Figure 1

0

50

100

150

200

250

300

350

No of larvae

M

r

A

p

9

r

M

a

y

6

J

3 1 u

n

J

5

l

Month

u

10

A

u

g

S

2

4

e

7

p

O

c

t

11

N

o

v

Phenology of parasitengone larvae in the field. Accumulated data of regular collections, made three times a month (1991–1994 at location 1-3; 1993–1994 at location 4; 1993 at location 5; 1996–1997 at location 6–8; 1993–1995 at location 10). No differences were found in the temporal appearance of larvae in subsequent years and at different localities. Number at row of columns: 1 = Leptus trimaculatus, 2 = L. ignotus, 3 = L. beroni, 4 = Erythraeus rivalis, 5 = E. sp. A, 6 = E. phalangioides, 7 = Abrolophus brevicollis, 8 = A. rudaensis, 9 = A. longicollis, 10 = Johnstoniana rapax, 11 = J. parva, 12 = J. errans, 13 = J. tuberculata (underlined = sympatric occurrence of species of a genus).

a

8

12

13

Andreas Wohltmann

CLOSELY RELATED SPECIES OF PARASITENGONAE (ACARI: PROSTIGMATA) INHABITING THE SAME AREAS

even less concerning the potential ecological interferences between species (Key 1990, 1994). In fact, most reports on terrestrial Parasitengonae might convey the mistaken impression that species usually occur allopatrically and are well separated in space. From samples taken at different localities in Northern Germany during the years 1989–1997 it became evident (1) that more than one species of Trombidia can be found at almost all localities observed, and (2) that even closely related species of Parasitengonae do often occur sympatrically. In the present work investigations focus on co-occurring terrestrial Parasitengonae with special emphasis on these questions: What kinds of life-cycles are displayed by closely related species and do environmental factors control the synchronisation of the life cycle within a particular species? What type of nutrition is used by the predatory postlarval instars, and what are the parasitic associations of the larvae? What are the habitat requirements of the species? Are there direct interactions, such as predation or competition, between parasitengone species? Which niche parameters are identical in closely related species inhabiting the same area, and in which parameters has divergence taken place? Which transformations in resource usage facilitated co-existence of closely related species? On the basis of the phylogenetic system, the results will be discussed with special emphasis on important selection factors and the constancy of selection conditions during the evolutionary history of Parasitengonae.

MATERIALS AND METHODS Parasitengonae were sampled during the years 1989–1997 at ten localities in northern Germany (Table 1) using sweep net, pit-fall traps and hand collecting. Each of the ten localities was repeatedly sampled at regular intervals for at least one year. Laboratory rearing was done in polystyrene boxes (25 × 25 × 20 mm) filled to a third with plaster-charcoal. Individuals were kept in an incubator at defined temperature and light conditions at saturated air humidities. All boxes were checked daily. Temperature control of diapausing instars was checked as follows: In one experiment specimens were chilled (100 or more days at 5°C) and subsequently exposed to 15° or 20°C, and in another specimens were exposed to constant 15° or 20°C (control). Host- and site specificity were tested in parallel experiments, each including at least 20 laboratory-reared larvae in polystyrene boxes in which potential hosts captured in the field were offered to the larvae. Experiments were regarded as valid when contact between mite larvae and potential host was observed more than once. Attachment and subsequent swelling of the larva was regarded as parasitism. Identification of specimens was done according to Oudemans (1912), Viets (1936), Thor and Willmann (1947), Robaux (1970), Haitlinger (1986, 1987), Fain (1991), Wendt and Eggers (1993), Wendt et al. (1994), Wohltmann et al. (1994) and Gabrys (1996). Voucher specimens are deposited in the author’s collection.

RESULTS AND DISCUSSION In total, 30 species of terrestrial Parasitengonae were collected (Table 1). Water mites were observed in temporary ponds in which six species were captured (Table 2). All localities observed were inhabited by two or more species. Irregular observations at further localities showed that only two types of biotopes were each

settled by a single parasitengone species: the rocky shores of the marine coasts of northern Germany inhabited by Abrolophus rubipes and the stone surfaces of buildings and walls inhabited by Balaustium murorum. Both of these species have lost parasitism and have predatory larvae. In this investigation, species are termed sympatric when they were found at the same locality and when they co-occurred in the same strata in a particular biotope, characterised by its specific assemblage of ground structure and vegetation patterns. This is of course only a rough approximation, since the true microhabitats of species may be more differentiated. In general, the Trombidioidea display a more or less subterranean life-style all year round. Their appearance on the soil surface is mostly restricted to (1) the larvae in their preparasitic phase and to (2) the adults during the period of spermatophore deposition. By contrast, the Erythraeoidea are surface dwellers or inhabit the crevices of stones but never burrow into the soil. All of the Trombidia found display semi- to univoltine life-cycles. In all species hitherto examined for the control of life-cycles, an obligatory diapause of a particular instar (Table 2) serves to synchronise the annual appearance of larvae and its hosts as well as the appearance of males and females during the mating period. Consequently, the phenology of each species shows only minor differences in successive years. This is most obvious for the larvae (Fig. 1), while the postlarval active instars in species displaying semivoltinism and/or iteroparity are often to be found the whole year round, albeit in varying abundance. The life cycle is strictly univoltine in Erythraeinae but often semivoltine in Calyptostoma and the Trombidioidea. Regarding the nutrition of postlarval instars, most erythraeoid species and a number of trombidioid taxa could be fed in laboratory with a range of insect eggs, larvae and pupae (Table 3). Investigations on the nutritional resources used in the field are difficult. However, the few observations confirmed the assumption that the more closely related species display no obvious specialisation in the diets of the postlarval predatory instars. Much more specialisation has occurred in the parasitic associations of the larvae (Table 3). Species displayed distinct differences in modes of host recognition and in host range. Direct interaction between parasitengone species was seldom observed; obvious cases are the parasitism of larvae on other Parasitengonae (obligatory in Johnstoniana parva, facultative in Leptus trimaculatus and Leptus ignotus) and predation of postlarval instars on other Parasitengonae. The latter was observed occasionally in Johnstoniana species and Allothrombium fuliginosum in the field. Under laboratory conditions without any additional food supply, starving specimens of most species preyed on weakened conspecifics. In general, species of Parasitengonae inhabiting the same area seem to be well separated from each other through (1) the inhabited biotope strata, (2) the annual appearance of instars or (3) the nutritional demands of instars. The following examples focus on sympatric species belonging to the same genus. It is difficult to determine which are most closely related species (i.e. sister species) because of the phylogenetic relationships of species belonging to one genus or even to one

123

Andreas Wohltmann Table 1

Locations

No.

Location

Description

1

Osterviertelsmoor near Bremerhaven, Northern Germany fresh meadow

originally extensive pasture, without human influence for 20 years; dominated by Agropyron repens, Stellaria graminea, Poa pratensis and Poa trivialis; at the margins Urtica dioica. Summer temperatures reach 32°C on the litter surface

2

Osterviertelsmoor near Bremerhaven, Northern Germany oak-birch forest

deciduous forest adjacent to fresh meadow, dominated by Populus tremola, Sambucus nigra and Sorbus aucuparia; in the herb layer by Urtica dioica, Rubus fructicosus and Galium aparine. Characterised by rapid temperature increase in spring; later temperature always below 25°C

3

Osterviertelsmoor near Bremerhaven, Northern Germany fen wood

temporary water in the centre of the oak – birch forest with dry phase from late spring to autumn. Vegetation dominated by Alnus glutinosa and Betula pubescens, in the herb layer by Carex canescens and Glyceria fluitans, in the centre Sphagnum phallax. Characterised by well buffered temperatures not exceeding 20°C and by saturated air humidities above ground level all of the time

4

Stoteler Wald near Bremen, Northern Germany fen wood

temporary pond in an oak – birch forest flooded by an adjacent creek form autumn to spring. Vegetation dominated by Alnus glutinosa, in the herb layer by Urtica dioica. Much dead wood covered by a thick moss layer constitute terrestrial islands during the inundation period. Characterised by low temperatures below 20°C and high humidity all of the time

5

Lake Wittensee, Northern Germany reed belt

temporary pond at the western margin of Lake Wittensee, separated from the lake by an small dike. The inundation period lasts from autumn to spring; the vegetation is dominated by Phragmites australis.

6

Lilo forest south-west Berlin Northern Germany oak-birch forest

forest bordering maize field, dominated by Populus tremola and Sorbus aucuparia; in the herb layer by Urtica dioica and Galium aparine.

7

Lilo forest south-west Berlin Northern Germany reed belt

adjacent to oak birch forest, dominated by Alnus glutinosa and Phragmites australis. Area usually not inundated in spring

8

Lilo forest south-west Berlin Northern Germany inundation area near creek

adjacent to reed belt, area flooded from autumn to spring, vegetation dominated by Phragmites australis

9

Mahler Park in Berlin Northern Germany park

small park near Campus of the Free University, mites were captured in the litter, which consists of 1–3 cm thick layer of rotting wood chips

10

Campus of University of Bremen Northern Germany ruderal area near creek

ruderal area on the campus with sparse ground vegetation, scarcely shaded by a few birch trees. Characterised by comparably high temperatures above ground (maximum 40°C) and strong variability in air humidities

subfamily are not adequately resolved. However, one may assume that species belonging to one genus are more closely related to each other than to other Parasitengonae and hence should display more similarity in their niche dimensions. Johnstoniana

Species were found exclusively in biotopes characterised by permanently hygric conditions and temperatures below 20°C. Postlarval instars of all Johnstoniana species inhabit the litter layer of such biotopes. The restriction to this biotope correlates with observations (1) on low desiccation resistance in eggs, protonymphs (Wohltmann 1998) and adults (Wendt 1994) and (2) on low haemolymph osmolalities of about 225 mOsm/ kg in the active instars (Wendt 1994). At all 5 hygric localities of this type more than one Johnstoniana species was found (Table 2). At one locality all four Johnstoniana species co-occurred (Table 2: 4). No differences in the specific microhabitats of these species were obvious. The annual appearance of larvae was from May – August in J. parva, while larvae of the other species were found in spring only (Fig. 2). Rearing in the laboratory (Wohltmann et al. 1999)

124

revealed that the life cycle of all species is univoltine to semivoltine and controlled by an obligate diapause of the egg, which results in simultaneous appearance of larvae at times of best host availability (Fig. 3). The active postlarval instars feed on a range of arthropod larvae and pupae, facultatively on other Trombidioidea or water mites resting in formerly submerged areas (e.g. Thyas barbigera), and even Johnstoniana species are preyed upon (Table 3). Apart from possible differences in preferred prey-size, no differences were observed among the postlarval predatory instars of Johnstoniana species. Regarding the larva, differences in the parasitic phase are obvious among all species. Parasitism on adult Tipulidae combined with preparasitic attendance, as in J. errans and J. tuberculata (Table 3), probably constitutes the original type of parasitic association (Wohltmann et al. 1999). The larvae recognise only the preadult instars of the host where they stay until the adult hosts eclose. During the eclosion process of the host, mite larvae transfer to the imago where they attach and begin feeding (Wohltmann 1996). This mode of host detection often leads to accumulation of mite larvae on a particular host (Table 3). Parasitism on other Parasitengonae (J. parva) or predation (J. rapax)

litter surface

litter surface

litter vegetation

litter layer

litter layer

litter layer

litter surface

litter surface

litter surface

litter surface

Abrolophus longicollis

Abrolophus brevicollis

Charletonia cardinalis

Leptus beroni

Leptus ignotus

Leptus trimaculatus

Erythraeus rivalis

Erythraeus phalangioides

Erythraeus sp. A

Erythrites sp.

litter

Calyptostoma velutinus B

litter layer

litter layer

litter layer

litter layer

litter layer

litter layer

litter layer, soil

soil

soil

soil

soil

soil

litter, soil

litter, soil

Johnstoniana tuberculata

Johnstoniana parva

Johnstoniana rapax

Johnstoniana errans

Diplothrombium longipalpe

Centrotrombidium schneideri

Valgothrombium major

Enemothrombium sp.

Georgiothrombium pulcherrimum

Microtrombidium fasciatum

Microtrombidium parvum

Platytrombidium sylvaticum

Camerotrombidium rasum

Campylothrombium boreale

Trombidioidea

litter

Calyptostoma velutinus A

Calyptostomatoidea

litter surface

Abrolophus rudaensis

Habitat

April – June

June – August

July ?

June – July

July – August

April – May

?

June – July

July

June

May – June

April – June

May – August

May – June

May – June

August – October

?

July – August

May – June

July – August

June – August

June – September

June – July

April – June

June – July

April – June

March – May

Abundance of larvae

whole year

whole year

whole year

whole year

whole year

whole year

whole year

whole year

June

September – April

whole year

May – August

whole year

whole year

whole year

whole year

May – June

August – June

June – August

August – June

August – April

August – July

September – April

May – August

July – May

June – October

April -August

Abundance of postlarval instars

uni – semi voltine

uni – semi voltine

uni – semi voltine

uni – semi voltine

uni – semi voltine

uni – semi voltine

?

?

?

?

uni – semi voltine

strictly univoltine

uni – semi voltine

uni – semi voltine

uni – semivoltine

uni – semi voltine

?

strictly univoltine

strictly univoltine

strictly univoltine

strictly univoltine

strictly univoltine

strictly univoltine

strictly univoltine

strictly univoltine

strictly univoltine

strictly univoltine

Voltinism

322

118

303

egg, nymph/adult

144 136

adult

-

14

egg, nymph/adult

nymph/adult

adult

8

361

egg, adult adult

-

23

2 ?

adult ?

adult ?

22

27 egg ?

612

80

59

269

144

304

101

142

5

229

24

4

187

65

657

35

(193)

(193)

egg, nymph/adult

364

53

236

27

35 -

182

14

72 33

11

126 5

330

232

10

353

246

787 251

43

38

No nymphs/adults

egg, nymph/adult

nymph/ adult

larva/ nymph/adult

?

adult

egg

deutonymph

adult

protonymph

deutonymph

egg

adult

egg

egg

Hibernating instars No larvae

2

1

5

7,8

9

2, 6

4

5, 8

5

4, 5

3, 4

4, 5

4, 5, 7, 8

3, 4, 5,7, 8,

2, 3, 4, 5, 7, 8

3

10

6, 7, 8

10

10

1

6, 7

1, 2, 3, 4, 5

1, 7

1

1

1

Locatlity

Phenology, voltinism and locations of terrestrial Parasitengonae captured in Northern Germany. Accumulated data derived from examinations carried out in 1989–1998. No significant differences concerning annual appearance of instars in subsequent years or at different localities were found. ? = no data available; Hibernating instars: derived from field observations, underlined = diapause tested in laboratory; No. larvae = total number of larvae captured; No. nymphs/ adults = total number of postlarval instars captured, in brackets = no differentiation between the Calyptostoma types possible in postlarval instars; Calyptostoma velutinus A/ B: status unclear. Locality: numbers refer to Table 1. For References see Table 3.

Erythraeoidea

Species

Table 2

CLOSELY RELATED SPECIES OF PARASITENGONAE (ACARI: PROSTIGMATA) INHABITING THE SAME AREAS

125

126

soil

soil, litter, vegetation May – July

Trombidium holosericeum

Allothrombium fuliginosum

temporary ponds

temporary ponds

temporary ponds

temporary ponds

temporary ponds

temporary ponds

Panisellus thienemanni

Euthyas truncata

Thyas barbigera

Thyopsis cancellata

Hydryphantes ruber

Tiphys ornatus

Hydrachnidia

soil

Trombidium brevimanum

June – July

July – September

July – August

June – August

June – September

April – May

June – September

June – August

May – July

litter

Podothrombium sp.

Abundance of larvae

Habitat

adults: April – May

whole year

?

whole year

whole year

?

whole year

whole year

whole year

whole year

Abundance of postlarval instars

univoltine

uni- semivoltine

?

uni- semivoltine

uni- semivoltine

uni- semivoltine

uni – semivoltine

uni – semi voltine

uni – semi voltine

uni – semi voltine

Voltinism

?

nymph/adult

?

nymph/adult

nymph/adult

?

nymph/adult

nymph/adult

nymph/adult

deutonymph/adult

5

25

59

27

29

79

20

937

21

69

Hibernating instars No larvae

63

301

6

129

65

1

361

933

63

213

No nymphs/adults

3, 4, 8

3, 8

3

3, 4, 5, 8

3, 8

4

9

1, 2, 5, 6, 9

9

1, 2, 3, 5, 7, 8

Locatlity

Phenology, voltinism and locations of terrestrial Parasitengonae captured in Northern Germany. Accumulated data derived from examinations carried out in 1989–1998. No significant differences concerning annual appearance of instars in subsequent years or at different localities were found. ? = no data available; Hibernating instars: derived from field observations, underlined = diapause tested in laboratory; No. larvae = total number of larvae captured; No. nymphs/ adults = total number of postlarval instars captured, in brackets = no differentiation between the Calyptostoma types possible in postlarval instars; Calyptostoma velutinus A/ B: status unclear. Locality: numbers refer to Table 1. For References see Table 3. (Continued)

Species

Table 2 Andreas Wohltmann

Feb

Figure 2

Jan

J. parva

J. tuberculata

J. rapax

J. errans

Apr

May

Jun

Aug

year 1.

Jul

Sep

Oct

Nov

Dec

Jan

Feb

larvae emerge May year 2.

larvae emerge May year 2.

WINTER

larvae emerge May year 2.

Oviposition

egg

adult

egg

egg

larvae emerge May year 2.

Mar

Apr

Oviposition

May

Jul

Aug

year 2.

Jun

larvae emerge May year 3.

larvae emerge May year 3.

larvae emerge July year 2.

Sep

Phenology and life cycle of Johnstoniana species. Based on field sampling (1991–1997) at different localities and on laboratory rearing. Winter indicated by grey shading.

Mar

tritonymph deutonymph protonymph larva

adult tritonymph deutonymph protonymph larva egg

adult

adult

tritonymph deutonymph protonymph larva

tritonymph deutonymph protonymph larva

Oct

Nov

Dec

CLOSELY RELATED SPECIES OF PARASITENGONAE (ACARI: PROSTIGMATA) INHABITING THE SAME AREAS

127

Andreas Wohltmann

is regarded as derived. Direct interference among Johnstoniana species was much more obvious than in other Parasitengonae. This includes (1) the parasitism of J. parva larvae on other Johnstoniana species, (2) the predation of J. rapax larvae on tipulid pupae already occupied by larvae of J errans waiting for the host’s eclosion, (3) the predation of J. rapax larvae on larval instars of other Johnstoniana species and (4) the predation of deutonymphs and adults of all species on other Johnstoniana species. With regard to development times, differences were found when comparing co-occurring populations of J. rapax and J. errans (Table 1: 4) to those captured at other localities (Table 1: 3, 5). In the case of sympatry, variability in development times of all instars was smaller in both species and shifted towards short development in J. rapax, whereas J. errans displayed an unusually long deutonymphal stage (Wohltmann et al. 1999). This character displacement may be a result of the actual direct interference. In conclusion, Johnstoniana species are well separated with respect to larval instars whereas postlarval instars share resources. Niche separation of larvae is not dependent on whether species occur sympatrically or not, but predominately concerns the particular range of hosts. Abrolophus

The three species of Abrolophus co-occurred in a fresh meadow. There was no obvious difference in their spatial distribution. Since the nutrition of postlarval instars is unknown, no hypotheses about differences concerning this resource were possible. However, differences were found in the annual distribution of their life stages as well as in larval nutrition. All meadow species were strictly univoltine and semelparous (Table 2). However, larvae of A. longicollis and A. rudaensis occurred in early spring while larvae of A. brevicollis were abundant in summer (Fig. 1). Field data and laboratory rearing showed that the annual appearance of larvae is controlled by an obligatory diapause of the eggs in A. longicollis and A. rudaensis. In A. brevicollis, the field data suggest that the pre-reproductive adult instar undergoes a comparable diapause; in this species eggs are not able to survive for longer than a week at low temperatures (5°C). Regarding parasitism, larvae of A. rudaensis and A. brevicollis are parasitic on Thysanoptera while A. longicollis larvae are not parasitic at all but predatory, with other mites and small arthropods serving as prey. As a result, these co-occurring Abrolophus species are well separated with respect to those niche dimensions used by the larval instar, either with respect to time (when using the same host resource) or to nutrition (when appearing at the same time). Erythraeus

Species of Erythraeus are active on the soil and litter surface. Of the three species observed two occurred at the same locality (Table 2: 10). There were no obvious differences in neither the spatial distribution nor the nutritional demands of the active instars of these two species (Table 3). The life cycle of all species was found to be strictly univoltine and semelparous. An obligatory winter diapause occurs in the egg of E. phalangioides, in the deutonymph of E. rivalis (Wendt 1997) and in the pre-reproductive adult of Erythraeus sp. A. Thus, the annual appearance of instars is constant within a species but differs between species. This is most

128

obvious with respect to the larvae (Fig. 1), whereby postlarval instars of the co-occurring species may overlap in their annual appearance. Other Parasitengonae

In other Trombidia, co-occurring species are usually well separated with respect to the larval stage as well. This is found among more closely related species like the Microtrombidiidae whose larvae display broad overlapping host specificity. In most microtrombidiids the larvae use brachyceran hosts (e.g. Lauxaniidae, Chloropidae, Drosophilidae) without any further host specificity being evident (Table 3; see also: Welbourn 1983). Microtrombidiids with similar host range were found well separated in space, the only exception being co-occurring Microtrombidiidae (Platytrombidium sylvaticum and Valgothrombium major, Table 2) having different host specificity. The same was found for the Hydrachnidia observed in a temporary fen. The Thyasidae and Hydryphantidae display broad overlap in the nutritional demands of postlarval instars (insect eggs, freshly dead larvae and pupae of Culicidae) as well as in their temporal and spatial abundance. As in Trombidia, distinct diversity exists in larval parasitism and none of the co-occurring hydryphantid and thyasid species was found on the same host species (Table 3). Even when comparing Trombidioidea to Erythraeoidea, or terrestrial to aquatic species (Table 2), overlapping in host resource between species is avoided by differences in host specificity, or by spatial or temporal separation. As a consequence, co-occurrence of different species on the same host individual is rare in Parasitengonae. Of a total of 1,151 parasitised hosts that were captured at the localities listed in Table 1 as well as at occasional observations at further places, in only 39 cases were host individuals parasitised by more than one parasitengone species. Five of these observations refer to exceptional cases of co-parasitism (Johnstoniana errans and Euthyas truncata parasitic on Tipula maxima maxima [Nematocera], Johnstoniana tuberculata and Johnstoniana rapax on Limonia phragmitidis [Nematocera], Trombidium holosericeum and Hydryphantes ruber on an Empididae [Brachycera], in the laboratory Valgothrombium major and Centrotrombidium schneideri on a Dasyhelea sp. [Ceratopogonidae]). The remaining 35 cases concern co-parasitism of Johnstoniana tuberculata and Calyptostoma velutinus B on Limonia phragmitidis (Nematocera); this constitutes approximately 10 percent of all captured host individuals parasitised by these species. In this particular case mite species display a strict site specificity on the host, in which J. tuberculata always attaches to the abdominal segments of the host but C. velutinus B larvae are to be found dorsally on Thorax I-II. This site specificity was found in all samples and was not dependent on the actual co-occurrence of both species on a particular host. Comparable site displacement (believed to limit potential competition among mite species) has been reported for parasitengone parasites of Australian grasshoppers (Key 1994).

CONCLUSIONS In all species observed little or no difference was found in the mode of feeding or type of prey of postlarval instars, when comparing

?

?

?

mites, larvae and pupae of Diptera and ants

larvae and pupae of Diptera and ants

larvae and pupae of Diptera and ants

larvae and pupae of Diptera and ants

larvae and pupae of Diptera and ants

larvae and pupae of Diptera and ants

larvae and pupae of Diptera and ants

?

larvae of Tipulidae

larvae of Tipulidae

other Parasitengonae, larvae and pupae of Diptera and ants

other Parasitengonae, larvae and pupae of Diptera and ants

Species

Abrolophus rudaensis

Abrolophus longicollis

Abrolophus brevicollis

Charletonia cardinalis

Leptus beroni

Leptus ignotus

Leptus trimaculatus

Erythraeus rivalis

Erythraeus phalangioides

Erythraeus sp. A

Erythrites sp.

Calyptostoma velutinus A

Calyptostoma velutinus B

Johnstoniana tuberculata

Johnstoniana parva

Parasitengonae: Trombidioidea

Nematocera: Limonia phragmitidis (abdomen)

Nematocera: Limonia phragmitidis, L. nubeculosa (thorax dorsally)

Nematocera: Limonia nubeculosa, L. macrostigma, Dicranomyia chorca (abdomen)

?

Homoptera

Homoptera

Homoptera

Acari: Prostigmata, Collembola, Hymenoptera Homoptera1, Nematocera1

Acari: Prostigmata, Opilionida, Collembola, Hemiptera, Hymenoptera, Coleoptera

Opilionida: Phalangiidae

76/ 6

206/ 22

96/ 10

25/ 5

-

16/ 3

13/ 3

Rack 1976 (Limonia spp. ; mite misidentified as J. errans) Wohltmann et al. 19943

Limonia pupae2 (NOT: adults of Limoniidae, pupae and adults of other Nematocera and Brachycera)

Wendt et al. 19943

Theis 1974 (Tipulidae?), Wohltmann et al. 19993

Limonia pupae2 (NOT: adult Nematocera, pupae and adults of Brachycera)

Trombidiinae, Microthrombidiidae, Johnstonianidae (NOT: Calyptostoma, Erythraeidae)

Theis 1974 (Tipulidae?), Wohltmann et al. 19993

Wendt19973

Wendt 19973

Wendt et al. 19923

-

(NOT: Aphidae)

Aphidae (NOT: Brachycera, Miridae, Cantharidae)

Aphidae

Aphidae

Anystis

6/ 2

24/ 5

-

Beron 1975 (Phalangiidae) Wohltmann 19943

Treat 1980 (Lepidoptera ?, Delphacidae)

Delphacidae (NOT: Brachycera, Culicidae, Aranae, Miridae) Phalangiidae (NOT: Brachycera, Miridae)

Haitlinger 1986, 1987 (Thysanoptera, Homoptera)

Haitlinger 1986

Haitlinger 1987 (Thysanoptera)

References

-

-

-

Host specificity and recognition (laboratory data)

33/ 3

42/ 16

55/ 8

35/ 1

Thysanoptera Homoptera1, Nematocera1 Homoptera: Cicadina

-

15/ 1

predatory on small arthropods

Thysanoptera

Host of larva (field data)

No hosts/ maximum parasite load

Nutritional demands of larvae and postlarval instars of terrestrial Parasitengonae. Nutrition of nymph and adult: nutritional demands of postlarval active instars investigated in the laboratory; Host of larva: field results, 1 = single case of host parasite association, in ( ) = site specificity; No. hosts = number of parasitised hosts captured at the localities 1-10; Host specificity: as tested in parallels in the laboratory, – = not tested, in ( ) = no parasitism observed, 2 = preparasitic attendance; References: in ( ) = hosts reported, ? = determination of mite uncertain 3 = data in table 3 partly published in reference.

Nutrition of deutonymph and adult

Table 3

CLOSELY RELATED SPECIES OF PARASITENGONAE (ACARI: PROSTIGMATA) INHABITING THE SAME AREAS

129

130

larvae and pupae of Diptera, calyptostatic instars of Parasitengonae

larvae of Chironomidae and Ceratopogonidae

larvae of Chironomidae and Ceratopogonidae: Dasyhelea spec. Ceratopogonidae (venter of thorax)

?

eggs of Tipulidae

larvae and pupae of Diptera

eggs of Nematocera

eggs of Staphylinidae

eggs of Staphylinidae

Aphidae, larvae and pupae of Diptera and ants

?

Diplothrombium longipalpe

Centrotrombidium schneideri

Valgothrombium major

Georgiothrombium pulcherrimum

Microtrombidium fasciatum

Microtrombidium parvum

Platytrombidium sylvaticum

Camerotrombidium rasum

Campylothrombium boreale

Podothrombium sp.

Trombidium brevimanum

Aranae

Aphidae Brachycera1

Brachycera: Lauxaniidae, Empididae, Nematocera1, Hymenoptera1

Brachycera: Anthomyzidae, Agromyzidae, Chloropidae, Drosophilidae, Lauxaniidae

Brachycera: Drosophilidae

Brachycera: Agromyzidae Nematocera1, Oribatida1

Nematocera: Dicranomyia sp.1 (venter of thorax)

Nematocera: Tipula spp. (venter and lateral sites of thorax)

other Parasitengonae, larvae and pupae of Diptera and ants

Johnstoniana errans

predatory on larvae and pupae of Diptera, other Johnstonianid larvae parasitic on Limonia phragmitidis1

Host of larva (field data)

other Parasitengonae, larvae and pupae of Diptera and ants

Nutrition of deutonymph and adult References

Brachycera: Drosophila sp., Chloropidae (NOT: Culicidae, Limoniidae, Aphidae, Ichneumoniidae)

6/3 1

12/ 4

7/2

31/4

-

-

Brachycera: Drosophila sp., Lauxaniidae (NOT: Cantharidae, Miridae)

Brachycera: Drosophila sp., Lauxaniidae (NOT: Cantharidae, Miridae)

Brachycera: Drosophila sp. (NOT: Culicidae, Aphidae, Ichneumoniidae)

-

34/ 2

Brachycera: Drosophila sp.

7/6

12/3

-

Wohltmann, 19993

Welbourn 1983 (Homoptera)

Wohltmann 19973

Wohltmann 19973

Gabrys 1996

Robaux 1971 (Brachycera: Muscidae, Anthomyzidae, Drosophilidae)

Wohltmann 19973

Wohltmann and Wendt 19963

pupae of Dasyhelea sp. 2 (NOT: adult Dasyhelea sp., chironomid larvae and pupae)

5/3

Wohltmann and Wendt 19963

pupae of Dasyhelea sp. 2 (NOT: adult Dasyhelea sp., pupae and adults of Chironomidae, Limoniidae, Drosophila sp.)

26/13 1

Rack 1976 (Limnophila, Molophilus, Erioptera)

Wohltmann 19963

-

pupae of Tipula spp. 2 (NOT: adult Tipula spp. , pupae and adults of Limoniidae and other Diptera)

(NO PARASITISM ON: larvae, pupae, Wendt and Eggers 1993 adult Tipulidae and other Diptera) Eggers 19943

Host specificity and recognition (laboratory data)

1/22

17/69

(1/1)

-

No hosts/ maximum parasite load

Nutritional demands of larvae and postlarval instars of terrestrial Parasitengonae. Nutrition of nymph and adult: nutritional demands of postlarval active instars investigated in the laboratory; Host of larva: field results, 1 = single case of host parasite association, in ( ) = site specificity; No. hosts = number of parasitised hosts captured at the localities 1-10; Host specificity: as tested in parallels in the laboratory, – = not tested, in ( ) = no parasitism observed, 2 = preparasitic attendance; References: in ( ) = hosts reported, ? = determination of mite uncertain 3 = data in table 3 partly published in reference. (Continued)

Johnstoniana rapax

Species

Table 3 Andreas Wohltmann

?

Acari, Aphidae, larve and pupae of Diptera and ants

?

eggs of Tipulidae, freshly dead Culex larvae

eggs of Culicidae, freshly dead Culex larvae

eggs of , freshly dead Culex larvae

?

Cladocera

Species

Trombidium holosericeum

Allothrombium fuliginosum

Panisellus thienemanni

Euthyas truncata

Thyas barbigera

Hydryphantes ruber

Thyopsis cancellata

Tiphys ornatus

4/ 27

1/ 3

Chironomidae1

10/ 5

14/ 4

21/ 8

35/ 6

4/ 1

223/ 40

Nematocera: Ptychopteridae (venter of thorax)

Brachycera: Chloropidae

Nematocera: Culex spp. (venter of thorax)

Nematocera: Tipulidae (venter of thorax)

Collembola: Tomocerinae (dorsally between head and thorax)

Homoptera: Aphidae

Heteroptera, Homoptera, Hymenoptera, Coleoptera, Brachycera, Nematocera1, Lepidoptera1

Host of larva (field data)

No hosts/ maximum parasite load

-

-

Chloropidae (NOT: Culicidae)

Culex (NOT: Brachycera)

Limonia, Tipula (NOT: Culex, pupae of Limonia or Tipula)

-

Aphidae (NOT: Brachycera)

Brachycera, Cantharidae, Miridae, ant larvae (NOT: Aranae)

Host specificity and recognition (laboratory data)

Smith and Oliver 1986 (Chironomidae: Orthocladinae; preparasitic attendance)

Münchberg 1936 (Tipulidae)

Böttger 1966

Mullen 1977 (Culicidae) Wohltmann et al. 19993

Smith and Oliver 1986 (Culicidae, Tipulidae) Wohltmann et al. 19993

Boehle 1996 (Arthropleona), Wohltmann et al. 19993

Robaux 1971 (Aphidae)

Robaux 1971

References

Nutritional demands of larvae and postlarval instars of terrestrial Parasitengonae. Nutrition of nymph and adult: nutritional demands of postlarval active instars investigated in the laboratory; Host of larva: field results, 1 = single case of host parasite association, in ( ) = site specificity; No. hosts = number of parasitised hosts captured at the localities 1-10; Host specificity: as tested in parallels in the laboratory, – = not tested, in ( ) = no parasitism observed, 2 = preparasitic attendance; References: in ( ) = hosts reported, ? = determination of mite uncertain 3 = data in table 3 partly published in reference. (Continued)

Nutrition of deutonymph and adult

Table 3

CLOSELY RELATED SPECIES OF PARASITENGONAE (ACARI: PROSTIGMATA) INHABITING THE SAME AREAS

131

Andreas Wohltmann

800 Number of Limonia imagoes

600

No. of parasitizing Johnstoniana tuberculata larvae

400

200

0 01.May Figure 3

30.Jun

30.Jul

Phenology of larvae of Johnstoniana tuberculata and of adults of its host Limonia phragmitides. Accumulated data (1991–1997) of field sampling three times a month at different localities. No differences were found in subsequent years or different localities.

closely related species. In contrast, all co-occurring species in this study differed with respect to the parasitic association of the larvae. In most of the closely related sympatric species differences in the annual appearance of larvae were found; others differed with respect to host specificity. This phenomenon is not restricted to closely related Parasitengonae but was found in sympatric Parasitengonae in general. The host specificity and the site specificity on the host is fixed in a species and does not depend on whether related species co-occur or not. The results are consistent with a number of earlier observations on terrestrial Parasitengonae (see citations in Table 3). The ultimate causes for the observed diversity in parasitic associations of sympatric Parasitengonae may be traced back to either (1) coevolution of host and parasites or (2) the limited availability of hosts and competition among mite species. Coevolution between hosts and parasites primarily results from host responses to parasitism and subsequent adaptations of the parasite to circumvent these defence mechanisms. In an evolutionary context this is likely to lead to a spiral of adaptations and counter-adaptations which will result in high host specificity of the parasites. Host-borne defence mechanisms are known from water mites, e.g. Sigara falleni (Corixidae) being immune to parasitism by Eylais discreta and Hydrachna cruenta (Davids 1973; Davids et al. 1977), or occasional melanin encapsulation of Arrenurus stylostomes by their zygopteran hosts (Åbro 1982). No such immune responses are known from the hosts of terrestrial Parasitengonae, but it seems likely that comparable reactions take place there. As a consequence of an evolutionary arms race between host and parasite one should expect (1) high host specificity and (2) parallelism in speciation events. Both expectations

132

31.May

are not supported by the data on terrestrial Parasitengonae (Table 3). Thus, differentiation in host associations as a result of coevolution of hosts and parasites seems rather unlikely and has probably played only a minor role in the evolution of Parasitengonae. Both intra- and interspecific competition on hosts may result in resource displacement (in the first case combined with sympatric speciation). In case of intraspecific competition we should expect that (1) the availability of hosts is limited; (2) the carrying capacity of hosts is limited; (3) the larval mortality is high. In case of potential interspecific competition we should expect that (4) sympatric species do not use same host resources but that different species in allopatric situations do so; (5) in case of using the same hosts different site-specificity may indicate competition avoidance. These possibilities may be examined in turn. (1) When comparing the abundance of suitable hosts to the availability of other resources used by Parasitengonae, suitable hosts are often abundant for only short periods in the year. The synchronised appearance and temporally limited abundance of questing larvae reflects this situation, whereas the postlarval instars are to be found the whole year round in iteroparous Parasitengonae. (2) Observations on terrestrial Parasitengonae showed that parasitised hosts captured in the field died earlier than unparasitised ones (personal observation); thus indicating that hosts are damaged by parasitism. (3) The larval mortality of some terrestrial species as calculated from laboratory and field data (Wohltmann 1999) is much higher than in the postlarval instars. However, most larval mortality occurs in the preparasitic phase and is probably more a result of predation by other arthropods or simply of the failure to detect a suitable host, rather than a result of intraspecific competition. (4) The data from terrestrial

CLOSELY RELATED SPECIES OF PARASITENGONAE (ACARI: PROSTIGMATA) INHABITING THE SAME AREAS

Parasitengonae show that there is little or no overlap in host resources in sympatric species. The small number of different parasitengone species on single host individuals supports this conclusion. In species occurring allopatrically the same host resource is used at the same period of the year (Table 2), e.g. as in the Microtrombidiidae parasitising Brachycera (Table 3). (5) The few cases of co-parasitism among terrestrial Parasitengonae are characterised by different site specificity on the host. The larvae of Johnstoniana tuberculata attach to the dorsal or lateral parts of the abdomen of Limonia phragmitidis while the spring larvae of Calyptostoma velutinus (type B) occurring on the same host at the same time are always attached at the dorsal region of thorax I-II. By contrast autumn larvae of C. velutinus (type A) prefer the dorsal site of the abdomen on their tipulid hosts. Thus I conclude that there are indications for intraspecific competition in terrestrial Parasitengonae, which need confirmation through more sophisticated experiments. Although there is no direct evidence for interspecific competition in terrestrial Parasitengonae, the small overlap in host resources found in sympatric species as well as the clear site displacement in the case of regularly shared hosts suggests ancestral competition. Actual competition as the original cause is less likely since host and site specificity is genetically fixed in a species and not dependent on whether closely related species co-occur or not. Modification of parasitic associations ‘by chance’ is again a less likely explanation because of the similarity of results in all Parasitengonae which display the ancestral type of life-style. Larval parasitism obviously constitutes the most restrictive phase with regard to population growth in the Trombidia. Thus, differentiation of parasitic associations allows coexistence of several species in sympatric conditions, whereas other resources may still be shared among species. This situation characterises all major taxa of Trombidia, but changed in all species in which larvae gave up parasitism and became predatory (e.g. all Balaustium spp. ) and in the chiggers (Trombiculidae) which underwent a dramatic change of host resource (vertebrates). Species having predatory larvae are always separated in space and do not occur sympatrically (e.g. Abrolophus spp. inhabiting the rocky shores of the North Sea and the Atlantic; Witte personal communication), probably because the main limiting resource for these species does not allow for sympatry. In the water mites, intraspecific competition has been found in a number of species, e.g. in larvae for host resources (Sperchon, Davies 1959; Hydryphantes, Lanciani 1979; Hydrachna and Eylais, Reilly and McCarthy 1991), and in adults of Unionicola species vying for space in their mussel hosts (Downes 1991). It has also been shown that parasitism of water mite larvae has significant influence on the longevity and reproductive success of hosts, and that this influence is positively correlated with parasite load (Lanciani 1983; Smith 1988, and references therein). Site-displacement in sympatric species using the same host has been interpreted as a result of competition in Eylais spp. and Hydrachna spp (Lanciani 1970; Reilly and McCarthy 1991, 1993). Species of both genera are characterised by prolonged host association and extraordinary larval growth during parasitism. Regarding interspecific competition and competition displacement, the situation in late derived Hydrachnidia is less well defined. For some Arrenurus species (Mitchell 1964) the situtation

is consistent with that described for most of the Trombidia, while other species, which use the same host resources at the same time when sympatric, often occur together on single host individuals without displaying site-displacement (Kouwets and Davids 1984; Smith 1988 and personal communication). Possibly the latter species are less exposed to selection on larval parasitism, possibly as a result of (1) reduced larval growth on the host and (2) increased numbers of available hosts; certainly this phenomenon deserves continued research.

ACKNOWLEDGEMENTS I wish to express my thanks to B. P. Smith, H. Witte, G. Davids, R. B. Halliday and an unknown reviewer for critical comments and valuable advice on earlier drafts of the manuscript.

REFERENCES: Åbro, A. (1982). The effects of parasitic water mite larvae (Arrenurus spp.) on zygopteran imagoes (Odonata). Journal of Invertebrate Pathology 39, 373–381. Begon, M., Mortimer, M. and Thompson, D. J. (1996). ‘Population Ecology.’ (Blackwell: Oxford.) Beron, P. (1975). Erythraeidae (Acariformes) larvaires de Bulgarie. Acta Zoologica Bulgarica 1, 45–75. Boehle, W. R. (1996). Contributions to the morphology and biology of larval Panisellus thienemanni (Viets, 1920) (Acari: Parasitengonae: Hydrachnidia). Acarologia 37, 121–125. Böttger, K. (1966). Einige biologisch-ökologische Beobachtungen zu Euthyas truncata (Neum. 1975) und Hydryphantes ruber ruber (Geer 1778) (Hydrachnellae, Acari). Zoologischer Anzeiger 177, 263–271. Böttger, K. and Martin, P. (1995). Faunistisch-ökologische Untersuchungen an den Wassermilben (Hydrachnidia, Acari) dreier kleiner Fließgewässer des Norddeutschen Tieflandes, unter besonderer Berücksichtigung der rheobionten Arten. Limnologica 25, 61–72. Böttger, K. and Völkl, R. (1987) Faunistisch-Ökologische Beobachtungen an den Wassermilben (Hydrachnellae, Acari) einiger Kleingewässer, nebst biologischen Angaben zu einzelnen Arten. Acarologia 28, 161–170. Davids, C. (1973). The water mite Hydrachna conjecta Koenike, 1895 (Acari: Hydrachnellae), bionomics and relation to species of Corixidae. Netherlands Journal of Zoology 23, 363–429. Davids, C., Nielsen, G. J. and Gehring, P. (1977). Site selection and growth of the larvae of Eylais discreta Koenike, 1897 (Acari: Hydrachnellae). Bijdragen tot de Dierkunde 64, 180–184. Davids, C., Ten Winkel, E. H., and De Groot, C. J. (1994). Temporal and spatial patterns of water mites in Lake Maarsseveen I. Netherlands Journal of Aquatic Ecology 28, 11–17. Davies, D. M. (1959). The parasitism of black flies (Diptera: Simuliidae) by larval water mites mainly of the genus Sperchon. Canadian Journal of Zoology 37, 353–369. Downes, B. J. (1991) Competition between mobile species using patchy resources: an example from a freshwater, symbioltic assemblage. Oecologia 85, 472–482. Eggers, A. (1994). Observations on parasitism and development of Johnstoniana spp. (Prostigmata: Parasitengonae: Johnstonianidae). In ‘The Acari: Physiological and Ecological Aspects of Acari-Host Relationships’ (Eds D. Kropczynska, J. Boczek and A. Tomcyk.), pp. 487–496. (Oficyna DABOR: Warzawa.) Fain, A. (1991). Two new larvae of the genus Leptus Latreille, 1776 (Acari: Erythraeidae) from Belgium. International Journal of Acarology 17, 107–111.

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Andreas Wohltmann Franke, A. (1940). Parasitengona (Trombidiformes, Acari) aus dem Gimmlitzquellmoor bei Hermsdorf (Erzgebirge). Zoologischer Anzeiger 129, 153–158. Gabrys, G. (1996). Microtrombidiidae (Acari: Actinedida) of Poland. Annals of the Upper Silesian Museum 6–7, 145–242. Haitlinger, R. (1986). The genus Hauptmannia Oudemans, 1910 (Acari, Prostigmata, Erythraeidae) in Poland. Polski Pismo Entomologiczne 56, 181–191. Haitlinger, R. (1987). Further information on distribution of species of the genus Hauptmannia Oudemans 1910 (Acari: Prostigmata: Erythraeidae) in Poland. Przeglad Zoologiczny 31, 159–164. Key, K. H. L. (1990). Host relations and distribution of species of Caeculisoma (Acarina: Erythraeidae) parasitising grasshoppers in Australia, with supplementary information for the genus Trombella (Trombellidae). Australian Journal of Zoology 38, 11–18. Key, K. H. L. (1994). Host relations and distribution of the Australian species of Eutrombidium (Acarina: Microtrombidiidae), a parasite of grasshoppers. Australian Journal of Zoology 42, 363–370. Kouwets, F. A. C., and Davids, C. (1984). The occurrence of chironomid imagines in an area near Utrecht (the Netherlands), and their relations to water mite larvae. Archiv für Hydrobiologie 99, 296–317. Lanciani, C. A. (1970). Resource partioning in species of the water mite genus Eylais. Ecology 51, 338–342. Lanciani, C. A. (1979). Intraspecific competition in the parasitic water mite, Hydryphantes tenuiabilis. The American Naturalist 96, 210–214. Lanciani, C. A. (1983). Overview of the effects of water mite parasitism on aquatic insects. In: ‘Biological Control of Pests by Mites.’ (Eds M. A. Hoy, G. L. Cunningham and L. Knutson.) pp. 86–90. (University of California: Berkeley.) Mitchell, R. (1964). A study of sympatry in the water mite genus Arrenurus (Family Arrenuridae). Ecology 45, 546–558. Mullen, G. R. (1977). Acarine parasites of mosquitos – IV. Taxonomy, life history and behaviour of Thyas barbigera and Thyasides sphagnorum (Hydrachnellae: Thyasidae). Journal of Medical Entomology 13, 475–485. Münchberg, P. (1936). Zur Kenntnis des Larvenparasitismus der Thyasinae (Hydracarina), zugleich ein Beitrag über Schmarotzer der Limnobiinae (Diptera). Internationale Revue der gesamten Hydrobiologie 33, 313–326. Oudemans, A.C. (1912). Die bis jetzt bekannten Larven von Thrombidiidae und Erythraeidae. Zoologische Jahrbuecher Abt. 1 Suppl. 14 (1), 1–230. Piecynski, E. (1976). Ecology of Water Mites (Hydracarina) in Lakes. Polish Ecological Studies 2, 5–54. Rack, G. (1976). Milben (Acarina) von europäischen Limoniinen /Diptera; Nematocera). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 73, 63–85. Reilly, P., and McCarthy, T. K. (1991). Watermite parasitism of Corixidae: infection parameters, larval mite growth, competitive interaction and host response. Oikos 60, 137–148. Reilly, P., and McCarthy, T. K. (1993). Attachment site selection of Hydrachna and Eylais (Acari: Hydrachnellae) water mite larvae infecting Corixidae (Hemiptera: Heteroptera). Journal of Natural History 27, 599–607. Robaux, P. (1970). Etude des larves de Thrombidiidae III – La larve de Johnstoniana errans (Johnston) 1852. Redescription de l’adulte et de la nymphe. Acarologia 12, 339–356. Robaux, P. (1971). Recherche sur le développement et la biologie des acariens Thrombidiidae. These de doctorat d’état ès-sciences naturelles. Faculté des Sciences de Paris. Smith, B. P. (1988). Host – parasite interaction and impact of larval water mites on insects. Annual Revue of Entomology 33, 487–507.

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Smith, I. M., and Oliver, D. R. (1986). Review of parasitic associations of larval water mites (Acari: Parasitengona: Hydrachnidia) with insect hosts. Canadian Entomologist 108, 1427–1442. Theis, G. (1974). Monographische Bearbeitung der Milbenfamilie Calyptostomidae (Trombidiformes). Ph.D. thesis, University of Graz, Austria. Thor, S., and Willmann, C. (1947). Acarina. Trombidiidae. Das Tierreich 71b, 187–544. Treat, A. E. (1980). Nymphal Sphaerolophus reared from larval Charletonia (Acarina; Erythraeidae). International Journal of Acarology 6, 205–214. Viets, K. (1936). Wassermilben oder Hydracarina (Hydrachnellae und Halacaridae). In ‘Die Tierwelt Deutschlands und der umgrenzenden Meeresteile (31/32)’ (Ed F. Dahl.) pp 1–574. (G. Fischer Verlag: Stuttgart.) Welbourn, W. C. (1983). Potential use of trombidioid and erythraeoid mites as biological control agents of insect pests. In: ‘Biological Control of pests by mites.’ (Eds M.A. Hoy, G.L. Cunningham and L. Knutson.) pp. 103–140 (University of California: (Berkeley.) Wendt, F.-E. (1994). Studies of the ecophysiology of four species of Johnstoniana George 1909 (Prostigmata: Parasitengonae: Johnstonianidae) with special regard to osmotic regulation. A phylogentical approach. In ‘The Acari, Physiological and Ecological Aspects of Acari-Host Relationships.’ (Eds D. Kropczynska, J. Boczek and A. Tomczyk.) pp. 97–107. (Oficyna DABOR: Warszawa.) Wendt, F.-E. (1997). On the ecophysiology of four species of Erythraeinae (Prostigmata: Parasitengonae) with special regard to osmotic regulation. In ‘Acarology IX, Proceedings’ (Eds R. Mitchell, D. J. Horn, G. R. Needham and W. C. Welbourn.) pp. 697–701. (Ohio Biological Survey: Columbus.) Wendt, F.-E., and Eggers, A. (1993). Johnstoniana rapax n. sp., a new species of the Johnstonianidae from Europe including a description of all active instars (Acari: Parasitengonae: Trombidia). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 91, 113–126. Wendt, F.-E., Olomski, R., Leimann, J. and Wohltmann, A. (1992). Parasitism, life cycle and phenology of Leptus trimaculatus (Hermann, 1804) (Acari: Parasitengonae: Erythraeidae) including a description of the larva. Acarologia 33, 55–68. Wendt, F.-E., Wohltmann, A. Eggers, A., and Otto, J.C. (1994). Studies on parasitism, development and phenology of Johnstoniana parva n. sp. (Acari: Parasitengonae: Johnstonianidae) including a description of all active instars. Acarologia 35, 49–63. Willmann, C. (1951). Untersuchungen über die terrestrische Milbenfauna im pannonischen Klimagebiet Österreichs. Österreichische Akademie der Wissenschaften, Mathematisch-naturwisenschaftliche Klasse, Sitzungsberichte Abt. I 160, 91–176. Wohltmann, A. (1994). On the life cycle of two Leptus species with remarks on the diversity of life cycle strategies within the genus Leptus Latreille (Prostigmata: Parasitengonae: Erythraeoidea). In ‘The Acari: Physiological and Ecological Aspects of Acari-Host Relationships.’ (Eds D. Kropczynska, J. Boczek, and A. Tomcyk.) pp. 447–454. (Oficyna DABOR: Warzawa.) Wohltmann, A. (1996). On the life-cycle and parasitism of Johnstoniana errans (Johnston) 1852 (Acari: Prostigmata: Parasitengonae). Acarologia 37, 201–209. Wohltmann, A. (1997). Parasitism and life cycle strategies in Microthrombidiidae (Prostigmata: Parasitengonae) from Central Europe. In ‘Acarology IX: Proceedings’ (Eds R. Mitchell, D. J. Horn, G. R. Needham and W. C. Welbourn.) pp. 101–104. (Ohio Biological Survey: Columbus.) Wohltmann, A. (1998). Water vapour uptake and drought resistance in immobile instars of Parasitengona (Acari: Prostigmata). Canadian Journal of Zoology 76, 1741–1754.

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Wohltmann, A. (1999). Life history evolution in Parasitengonae (Acari: Prostigmata): Constraints on number and size of offspring. In ‘Evolution and Ecology of Acari’ (Eds J. Bruin, L. P. S. van der Geest and M. Sabelis.) pp. 137–148 (Kluwer Academic Publishers: Dordrecht.) Wohltmann, A. (1999). On the biology of Trombidium brevimanum (BERLESE 1910) (Acari: Prostigmata: Parasitengonae: Trombidiinae) with a redescription of all active instars. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 96, 157–168 Wohltmann, A., Wendt, F.-E., Eggers, A., and Otto, J. C. (1994). Observations on parasitism, development and phenology of Johnstoniana

tuberculata Schweizer 1951 (Acari: Parasitengonae: Johnstonianidae) including a redescription of all active instars. Acarologia 35, 153–166. Wohltmann, A. and Wendt, F.-E. (1996). Observations on the biology of two hygrobiotic trombidioid mites (Acari: Prostigmata: Parasitengonae) with special regard to host finding and parasitism tactics. Acarologia 37, 31–44. Wohltmann, A., Wendt, F.-E., Witte, H., and Eggers, A. (1999). The evolutionary change in the life history patterns in hygrobiontic Parasitengonae (Acari: Prostigmata). In ‘Acarology IX: Symposia.’ (Eds G. R. Needham, R. Mitchell, D. J. Horn and W. C. Welbourn.) pp. 165–174 (Ohio Biological Survey: Columbus.)

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ACAROLOGY

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

AQUATIC MITES AS BIOINDICATORS, WITH AN AUSTRALIAN EXAMPLE

....................................................................................................

J. E. Growns Cooperative Research Centre for Freshwater Ecology, Department of Biological Sciences, Monash University, c/Murray Darling Freshwater Research Centre, PO Box 921, Albury, NSW, Australia 2640.

.................................................................................................................................................................................................................................................................

Abstract Aquatic mites are rarely included in biomonitoring studies or as indicators in themselves, despite several studies showing that they are sensitive to different types of pollution. The sensitivity of aquatic mites to urban pollution near Sydney, Australia was investigated to determine their potential as bioindicators. Mites were collected from six moderately polluted and six unpolluted rivers using kick samples in riffles and sweep samples in edges. The numbers of species and abundances of aquatic mites were far higher at the unpolluted than the polluted sites for both habitats. The numbers of species and abundances of aquatic mites were also significantly higher in edge samples than riffle samples for unpolluted sites. There was little overlap between the species collected from riffles and edges, demonstrating that each habitat had a distinct fauna. Analysis of Similarity showed that the polluted and unpolluted sites could be discriminated using the mite assemblage composition for both habitats. However, the results were not quite as significant as when family data for all macroinvertebrates were used. The results of this study suggest that aquatic mites could be very useful bioindicators, particularly for lowland rivers where riffle habitats are rare and the other macroinvertebrates collected from edge habitats are generally tolerant taxa.

INTRODUCTION Most aquatic mites are macroinvertebrates, which are typically defined as invertebrates that are > 0.5 mm long when mature. Freshwater macroinvertebrates are widely used for biomonitoring, particularly of lotic systems, throughout the world (Rosenberg and Resh 1993). However, aquatic mites have been little used as indicators of pollution or disturbance of aquatic systems and are usually not identified beyond ‘aquatic mite’ in most monitoring studies (Hilsenhoff 1988; Stark 1993; Teles 1994; Wright et al. 1994; DeShon 1995; Cao et al. 1997). This is despite the fact that several field studies in Europe and North America have indicated that aquatic mites are sensitive to different types of pollution (Wagener and LaPerriere 1985; Biesiadka and Kowalik 1991; Cicolani and Di Sabatino 1991; Gerecke and Schwoerbel 1991; Smit and van der Hammen 1992). In Australia, the

136

National River Health program states that greater discrimination may be achieved by identifying mites to family level, but that doing so is time-consuming (Anon. 1994). In most states, this has resulted in mites being identified only to Hydracarina. Characteristics of macroinvertebrates that make them suitable as biomonitors include their being ubiquitous and diverse, abundant and easily collected, relatively sedentary, having life cycles of moderate length (weeks to years), showing variation among taxa in sensitivity to pollutants, and being easily identified (modified from Metcalfe-Smith 1994). Aquatic mites meet most of these criteria. They are almost always collected in samples of macroinvertebrates and, in Australia, their diversity is comparable with most of the other major groups of freshwater macroinvertebrates (Harvey 1998). They are easily collected in the same way as other aquatic macroinvertebrates, are relatively sedentary and have life

AQUATIC MITES AS BIOINDICATORS

Table 1

List of sampling sites and characteristics.

Reference sites

Stream order

Altitude (m)

Polluted sites

Stream order

Altitude (m)

Bola Creek

4

40

Berowra Creek

4

170

Colo River

6

100

Brookside Creek

1

100

Erskine Creek

5

20

Georges River

5

10

Kowmung River

5

200

Lane Cove River

4

40

Little River

4

170

South Creek

4

10

Wallandoola Creek

3

150

Winmalee Creek

1

200

cycles of months to years. The reasons they have not been used as biomonitors are therefore probably threefold. Firstly, they are usually not as abundant as other groups, although Proctor and Pritchard (1989) note that they have been recorded occurring in high densities in both lakes and rivers. Secondly, there have been relatively few studies showing that they are sensitive to different types of pollution. Finally, they are perceived as being difficult to identify because they often need to be slide mounted for species level identification and keys may be difficult to obtain or use. However, with expert teaching, the ability to identify to generic level using whole specimens can be achieved rapidly. This study was part of a wider project to determine the best rapid assessment technique to enable discrimination between polluted and unpolluted sites using macroinvertebrate assemblages. Other macroinvertebrates were identified only to family level but the mites were identified to species wherever possible. The objective of this paper was to determine whether the polluted and unpolluted sites could be discriminated using the mites alone. A review of the available information on aquatic mite responses to pollution is also included.

METHODS Study sites

Twelve freshwater rivers and streams within a 100 km radius of Sydney, New South Wales, Australia, ranging in size from 1st to 6th order (Table 1) were sampled. All streams were at elevations of 200 m or less above sea level, so that comparisons between sites would not be confounded by altitudinal effects (Growns et al. 1995). Six streams in outer suburban Sydney and the lower Blue Mountains were polluted to varying degrees by either disposal of secondary or tertiary municipal sewage effluent, or stormwater runoff from extensive urban development in their catchments, or both. The remaining regional reference streams, which are peripheral to the broader Sydney region, have catchments that are predominantly or entirely natural bushland and lack substantial agricultural or industrial development. They are distributed widely in an arc from the north (Colo River) to the south (Bola Creek) of the city. Sampling

Sampling was conducted in November 1993, and is described in detail in Growns et al. (1997). Briefly, three riffle and three edge samples were collected using a dip-net (250 mm mesh) at each site, and were picked live in the field. Edge samples were taken over the range of habitats present at a site, including vegetated and unvegetated areas. Three different picking methods were used, as

the aim of the main study was to determine the most appropriate field picking method. Consequently, data were pooled for the three samples for this paper. Mites were identified to species level wherever possible. Data analysis

The number of mite taxa (Nspp) and the number of individuals (Nind) were recorded for each habitat at each site. Box and whisker plots (Wilkinson et al. 1992) were used to compare values between pollution levels and habitats. The length of each box shows the range within which the central 50% of the values fall, with the box hinges (borders) at the first and third quantiles. The whiskers show the range of values that fall within the inner fences (but do not necessarily extend all the way to the inner fences). Values between the inner and outer fences are plotted with asterisks. Values outside the outer fence are plotted with empty circles. Lower inner fence = lower hinge (1.5 (median lower hinge)) Upper inner fence = upper hinge + (1.5 (upper hinge median)) Lower outer fence = lower hinge (3 (median lower hinge)) Upper outer fence = upper hinge + (3 (upper hinge median)). Mann-Whitney U tests were used to compare abundances and numbers of species between pollution levels for each habitat. ANOSIM (Analysis of Similarity; Clarke, 1993) in the Primer software package (available from Plymouth Marine Laboratory, U.K.) was used to see if the mite assemblages could be used to discriminate between the polluted and unpolluted sites for each habitat. ANOSIMs were performed on both standardised and presence/absence data. Bray-Curtis dissimilarity measures were calculated to form the similarity matrix for input to ANOSIM.

RESULTS A total of 504 mites from 58 taxa were collected (Appendix). Mites were recorded from all sites except one, the polluted South Creek. Mann-Whitney U tests showed that unpolluted sites had significantly greater numbers of mites recorded than polluted sites for both riffle (U = 36.0, p < 0.01) and edge (U = 3.5, p < 0.01) habitats (Figure 1a). Unpolluted sites also recorded greater numbers of taxa than polluted sites (edges, U = 36.0, p < 0.01; riffles, U = 33.5, p < 0.05; Figure 1b). At unpolluted sites, edge samples collected significantly greater numbers of mites (U = 34.0, p = 0.01) and more taxa (U = 33.5, p < 0.05) than riffle samples. The numbers of taxa recorded from each habitat and polluted or unpolluted sites are shown in Table 2; the number of taxa for each

137

J. E. Growns

No. of individuals

(a)

200 unpolluted polluted

150 100 50

No. of species

(b)

25 20 15 10 5

riffles

edges Figure 1

Table 2

Box and whisker plots for (a) numbers of individuals and (b) numbers of taxa of aquatic mites, in edge and riffle habitats from polluted and unpolluted sites.

Numbers of aquatic mite taxa recorded from riffle and edge habitats and polluted and unpolluted sites. Numbers in brackets indicate the numbers of taxa recorded only from that combination of habitat and degree of pollution. Unpolluted

Polluted

Total

Riffles

20(14)

5(1)

22(16)

Edges

38(32)

6(2)

42(40)

Total

53(52)

9(5)

58

combination of habitat and degree of pollution is also shown. There was little overlap between the species collected from edge and riffle samples, indicating that the different habitats had distinct faunas. Five taxa were recorded only from polluted sites and three taxa were recorded from both polluted and unpolluted sites (Table 3). From the genera that were collected in at least two samples, twelve genera from 8 families were recorded only from edges, whereas five genera from three families were recorded only from riffles (Table 3). The numbers of individuals collected for most species was low but six species had at least 20 individuals recorded: Hydrodroma SWB9; Aspidiobates scutatus; Limnesia maceripalpis; Limnesia parasolida; Momoniella parva; and Frontipoda gredada. Hydrodroma was collected only from edges but appeared to be fairly tolerant of

138

pollution as it was collected from the polluted Georges River as well as three unpolluted sites. Aspidiobates scutatus and L. maceripalpis were locally abundant but each was only recorded from two unpolluted sites. Limnesia parasolida was the most abundant mite recorded in this study, with 73 individuals collected. It was found at three unpolluted sites, as was F. gredada. Momoniella parva was the most ubiquitous species and was collected at five of the six unpolluted sites. Recifella females were also collected from edge samples at five of the six unpolluted sites and Monatractides australis was collected from riffles at four of the six unpolluted sites. ANOSIM showed that polluted and unpolluted sites had significantly different mite assemblages for both riffle and edge habitats and using either standardised abundances or presence/absence data (Table 4).

DISCUSSION This study has shown that the polluted and unpolluted sites could be distinguished using the mite fauna alone. The numbers of mites collected, the number of taxa collected and the assemblage composition could all distinguish between the two groups of sites. ANOSIM was also used by Growns et al. (1997) to test if the macroinvertebrate family-level assemblage composition varied between these groups of sites. The mite comparisons gave slightly lower R-values (measure of the difference between groups) to the

AQUATIC MITES AS BIOINDICATORS

Table 3

Genera of aquatic mites that were only collected from certain groups of samples. Only genera that were collected in at least 2 samples are shown.

Family or higher taxon

Genus

Edges

Family or higher taxon

Aturidae

Albia

Hydrodromidae

Hydrodroma

Hydryphantidae

Cyclohydryphantes

Hygrobatidae

Hygrobatidae

Kallimobates

Pseudohydryphantes

Limnesiidae

Tubophorella

Caenobates

Torrenticolidae

Monatractides

Coaustraliobates

Polluted sites

Dropursa

Mesostigmata

Physolimnesia australis

Oribatida

Momoniidae

Momoniella

Limnesiidae

Oxidae

Frontipoda

Unionicolidae

Procorticacarus Gondwanabates

Limnesiidae

Table 4

Genus or species

Riffles

Oxus

Unionicolidae

Koenikea

Polluted and unpolluted sites

ANOSIM results comparing aquatic mite data from polluted and unpolluted sites. * = p < 0.05 Presence/absence

Standardised abundances

Riffles

0.36*

0.36*

Edges

0.66*

0.57*

families of macroinvertebrates for both edge samples (presence/absence 0.42, standardised 0.55, from Growns et al. 1997) and riffles (presence/absence 0.50, standardised 0.46, from Growns et al. 1997). The significance values were also less for the tests using mites compared with those for macroinvertebrates for both habitats (edges p < 0.01 for both types of data, riffles p < 0.01 presence/absence, p < 0.05 standardised). Many more individuals and species were collected from edge samples than riffles and for this reason, aquatic mites might be better indicators for edge habitats in this region. This would be very useful for lowland rivers where riffles rarely occur and effective biomonitoring techniques have yet to be developed. There was little overlap between the species collected from edges and riffles, which indicates that riffle habitats do have different mite assemblages, rather than just fewer mites of the same types as edges. There was also evidence of habitat preferences at the genus level. However, species within some genera showed different preferences. For example, most species of Limnesia were collected only from unpolluted edges. However, L. corpulenta was only collected from a polluted site and L. parasolida was collected from both riffle and edge samples. Several other studies have shown that the diversity of aquatic mite assemblages decreases with organic and urban pollution. Gerecke and Schwoerbel (1991) collected aquatic mites in the late 1950s and in 1984 at 31 sites in the Upper Danube region. They found that the numbers of species of aquatic mites were greater at sites

Limnesia corpulenta Physolimnesia australis Unionicola

Hydrodromidae

Hydrodroma SWB 9

Hygrobatidae

Procorticacarus hirsutus

Oxidae

Flabellifrontipoda

with better water quality. At sites where water quality had improved between sampling dates, the species richness of aquatic mites had increased, whereas where water quality had declined, so had the numbers of species of aquatic mites. They identified seven species that were relatively tolerant to poor water quality, including Hygrobates fluviatilis. They also found that the numbers of spring-dwelling mite species had drastically declined due to habitat loss and pollution, whereas numbers of species which prefer habitats with slower flow had increased. Cicolani and Di Sabatino (1991) compared the diversity of aquatic mites with a biotic index based on the entire macroinvertebrate assemblage for two streams affected by olive growing and sewerage effluent in Italy. They found that the diversity of water mites decreased with increased pollution, both of which varied seasonally. They also showed that the diversity of water mites correlated strongly with the biotic index. Hygrobates fluviatilis was again identified as the most tolerant species. Aquatic mites have also been found to be useful indicators of lake trophic status. Biesiadka and Kowalik (1991) found that sublittoral and profundal mites could be used as indicators of trophic status for lakes in Poland. The mites in the littoral zone were generally tolerant of enriched conditions and were therefore not very useful indicators in themselves. However, as trophic status worsened, the contribution of littoral mites to the total mite assemblage increased. Smit and van der Hammen (1992) suggested that aquatic mites would be useful indicators for coastal dune lakes in the Netherlands and northern France. Half of the aquatic mite species in the Netherlands were recorded from these dunes during their study. Water abstraction from these lakes has led to inflow of eutrophic groundwater and this deterioration in water quality is correlated with decreased numbers of mite species.

139

J. E. Growns

Aquatic mites have also been found to be sensitive to other types of pollution. Wagener and LaPerriere (1985) found that they were the most affected group of organisms in streams affected by mining for precious metals. However, they could not be sure whether the effect was due to loss of habitat because of infilling of crevices by sediment or to heavy metal contamination. Dieter et al. (1996) suggested that the number of mite species in wetlands might have been decreased by the use of phorate, an organophosphate pesticide. Brodin and Gransberg (1993) suggested that mite assemblages in a Scottish lake had been affected by anthropogenic acidification. Another useful resource is provided by Steenbergen (1993), which details the distribution and abundance of 119 species of water mites and their associations with environmental variables. For example, Hydrodroma despiciens occurs in north Holland in waters with the highest nutrient levels recorded (> 2 mg/L total phosphorus; > 1.1 mg/L nitrate), however, it prefers waters with lower levels. These data support my observation that Hydrodroma occurred at both polluted and unpolluted sites. There have been some laboratory toxicological studies on aquatic mites, looking at their sensitivity to: iron and pH levels (Rousch et al. 1997); 3,4-dichloroaniline (Schmitz and Nagel 1995); cypermethrin, a synthetic pyrethroid (Stephenson 1982); heavy metals (Braginskij and Shcherban 1978); phenol (Alekseyev 1973) and arsenic oxide (Kamshilov and Flerov 1976). In each case the mite concerned was found to be sensitive to the pollutant and usually was among the more sensitive of the organisms tested. The available evidence therefore suggests that aquatic mites are sensitive to many different types of pollution and that different species show different levels of sensitivity. They therefore show much promise as bioindicators. Simply the numbers of individual mites, or the number of taxa collected, would probably be useful indicators when comparing impacted sites with similar but unimpacted sites. They may be particularly useful for edge habitats, as the mite assemblages are more diverse and abundant here than in riffles. Effective biomonitoring techniques for lowland rivers are urgently needed in Australia. The present techniques do not work very well because riffles rarely occur and the macroinvertebrate assemblages from the edges of these rivers are composed of mostly tolerant taxa. For most aquatic mites, identification to generic level is possible without slide mounting for experienced staff. Identification to generic level of the mites collected from edge habitats in lowland rivers for the Australian National River Health program might therefore prove a useful and cost-effective biomonitoring technique.

ACKNOWLEDGEMENTS I would like to thank Mark Harvey for teaching and encouraging me to identify aquatic mites and Ivor Growns, who provided statistical advice and made useful comments on the draft manuscript.

REFERENCES Alekseyev, V.A. (1973). Toxicological characteristics and symptom complex of acute phenol intoxication of aquatic insects and arachnids.

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Trudy, Instituta Biologii Vnutrennikh Vod Akademii Nauk SSSR 24, 72–89. Anonymous (1994). ‘National River Processes and Management Program Monitoring River Health Initiative. River Bioassessment Manual Version 1.0.’ (Department of the Environment, Sport and Territories/Land and Water Resources Research and Development Corporation/Commonwealth Environment Protection Agency: Canberra.) Biesiadka, E., and Kowalik, W. (1991). Water mites (Hydracarina) as indicators of trophy and pollution in lakes. In ‘Modern Acarology’. (Eds F. Dusbábek and V. Bukva.) pp. 475–481. (Academia, Prague and SPB Academic Publishing bv: The Hague.) Braginskij, L. P., and Shcherban, Eh. P. (1978). Acute toxicity of heavy metals to aquatic invertebrates under different temperature conditions. Hydrobiological Journal 14, 78–82. Brodin, Y-W., and Gransberg, M. (1993). Responses of insects, especially Chironomidae (Diptera), and mites to 130 years of acidification in a Scottish Lake. Hydrobiologia 250, 201–212. Cao, Y., Bark, A. W. and Williams, W.P. (1997). Analysing benthic macroinvertebrate community changes along a pollution gradient: a framework for the development of biotic indices. Water Research 31, 884–892. Cicolani, B. and Di Sabatino, A. (1991). Sensitivity of water mites to water pollution. In ‘Modern Acarology’. (Eds F. Dusbábek and V. Bukva.) pp. 465–474. (Academia, Prague and SPB Academic Publishing bv: The Hague.) Clarke, K.R. (1993). Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology 18, 117–143. DeShon, J. E. (1995). Development and application of the Invertebrate Community Index (ICI). In ‘Biological Assessment and Criteria. Tools for Water Resources Planning and Decision Making’. (Eds W. S. Davis and T. P. Simon.) pp. 217–243. (Lewis Publishers: London.) Dieter, C. D., Duffy, W. G. and Flake, L. D. (1996). The effect of phorate on wetland macroinvertebrates. Environmental Toxicology 15, 308–312. Gerecke, R. and Schwoerbel, J. (1991). Water quality and water mites (Acari, Actenidida) in the upper Danube region, 1959–1984. In ‘Modern Acarology’. (Eds F. Dusbábek and V. Bukva.) pp. 483–491. (Academia, Prague and SPB Academic Publishing bv: The Hague.) Growns, J. E., Chessman, B. C., McEvoy, P. K. and Wright, I. A. (1995). Rapid assessment of rivers using macroinvertebrates: case studies in the Nepean River and Blue Mountains, NSW. Australian Journal of Ecology 20, 130–141. Growns, J. E., Chessman, B. C., Jackson, J. E. and Ross, D. G. (1997). Rapid assessment of Australian rivers using macroinvertebrates: cost and efficiency of 6 methods of sample processing. Journal of the North American Benthological Society 16, 682–693. Harvey, M. S. (1998). ‘The Australian Water Mites: A Guide to Families and Genera.’ (CSIRO Publishing: Melbourne.) Hilsenhoff, W. L. (1988). Rapid field assessment of organic pollution with a family-level biotic index. Journal of the North American Benthological Society 7, 65–68. Kamshilov, M. M. and Flerov, B. A. (1976). Experimental research on phenol intoxication of aquatic organisms and destruction of phenol in model communities. In ‘Proceedings 1 st and 2nd USA-USSR Symposia on Effects of Pollutants upon Aquatic Ecosystems, Duluth, MN’. (Eds D. I. Mount, W. R. Swain and N. K. Ivanikiw.) pp. 181–192. (U.S. NTIS PB-287–219.) Metcalfe-Smith, J. L. (1994). Biological Water-Quality Assessment of Rivers: Use of Macroinvertebrate Communities. In ‘The Rivers Handbook. Hydrological and Ecological Principles’. (Eds P. Calow and G. E. Petts.) pp. 144–170. (Blackwell Scientific Publications: Oxford.)

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Proctor, H. and Pritchard, G. (1989). Neglected predators: water mites (Acari: Parasitengona: Hydrachnellae) in freshwater communities. Journal of the North American Benthological Society 8, 100–111. Rosenberg, D. M. and Resh, V. H. (Eds) (1993). ‘Freshwater Biomonitoring and Benthic Macroinvertebrates.’ (Chapman and Hall: London.) Rousch, J. M., Simmons, T. W., Kerans, B. L. and Smith, B. P. (1997). Relative acute effects of low pH and high iron on the hatching and survival of the water mite (Arrenurus manubriator) and the aquatic insect (Chironomus riparius). Environmental Toxicology and Chemistry 16, 2144–2150. Schmitz, A., and Nagel, R. (1995). Influence of 3,4-dichloroaniline (3,4DCA) on benthic invertebrates in indoor experimental streams. Ecotoxicology and Environmental Safety 30, 63–71. Smit, H. and van der Hammen, H. (1992). Water mites as indicators of natural aquatic ecosystems of the coastal dunes of the Netherlands and northwestern France. Hydrobiologia 231, 51–64. Stark, J. D. (1993). Performance of the Macroinvertebrate Community Index: effects of sampling method, sample replication, water depth, current velocity, and substratum on index values. New Zealand Journal of Marine and Freshwater Research 27, 463–478.

Steenbergen, H. A. (1993). ‘Macrofauna-atlas of North Holland: Distribution maps and responses to environmental factors of aquatic invertebrates.’ (Cip-gegevens Kononklijke Bibliotheek: Den Haag.) Stephenson, R. R. (1982). Aquatic toxicology of cypermethrin 1. Acute toxicity to some freshwater fish and invertebrates in laboratory tests. Aquatic Toxicology 2, 175–185. Teles, L. F. O. (1994). A new methodology for biological water quality assessment. Verhandlungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 25, 1942–1944. Wagener, S. M. and LaPerriere, J. D. (1985). Effects of placer mining on the invertebrate communities of interior Alaska streams. Freshwater Invertebrate Biology 4, 208–214. Wilkinson, L., Hill, M., Miceli, S., Birkenbeuel, G. And Vang, E. (1992). ‘SYSTAT for Windows: Graphics, Version 5 Edition.’ (SYSTAT, Inc.: Evantson, IL.) Wright, J. F., Furse, M. T. and Armitage, P. D. (1994). Use of macroinvertebrate communities to detect environmental stress in running waters. In ‘Water Quality and Stress Indicators in Marine and Freshwater Ecosystems: Linking Levels of Organisation (Individuals, Populations, Communities)’. (Ed D.W. Sutcliffe.) pp. 15–34. (Freshwater Biological Association: U.K.)

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J. E. Growns Appendix

Aquatic mite taxa collected from each habitat at polluted and unpolluted sites. E = edge, R = riffle. SWB numbers refer to undescribed species held in the Sydney Water Board voucher collection.

Species

Unpolluted

Polluted

Mesostigmata Mesostigmata sp.

R

Oribatida SWB15

E

R

Athienemaniidae Notomundamella SWB1

R

Arrenuridae E

Aturidae

Limnesia corpulenta E

Limnesia maceripalpis

E

Limnesia otruma

E

Limnesia parasolida

E

Limnesia szalayi

E

Limnesia timmsi

E

Tubophorella australis

Albia rectifrons

E

Limnocharidae

Axonopsella sp.

E

Limnochares australica

Hydrodromidae

E R

E

Austrolimnochares womersleyi E

E

Gretacarus australicus

Cyclohydryphantes trabeculiferus

E

Pseudohydryphantes occabus

E

R

Mideopsidae

Hydryphantidae

E

R

Momoniidae Momoniella parva

Hygrobatidae

E

Oxidae

Aspidiobates geometricus

E

Aspidiobates scutatus

E

R

Flabellifrontipoda sp.

E

R

Flabellifrontipoda pectinata

E

R

Aspidiobates SWB 58

R

Frontipoda gredada

E

Australiobates mutatus

R

Frontipoda neotasmanica

E

Australiobates ombatus

R

Frontipoda setipalpis

E

Frontipoda sp. nr. tasmanica SWB76

E

Frontipoda SWB 51

E

E

Australiobates SWB74

R

Caenobates acheronius

E

Frontipoda zunova

E

Coaustraliobates SWB1

E

Oxus orientalis

E

Coaustraliobates longipalpis

E

Oxus meridianus

E

Oxus troma

E

Procorticacarus sp.

R

Procorticacarus angulicoxalis

R

Procorticacarus hirsutus

R

Procorticacarus togalus

R

Dropursa boultoni

R

Physolimnesia australis E

Australiobates ventriscutatus

E

E

R

Torrenticolidae R

Monatractides australica

R

Unionicolidae Koenikea crinita

E

Gondwanabates SWB 63

R

Koenikea lemba

E

Kallimobates australicus

R

Koenikea sorpresa

E

Kallimobates vietsi

R

Recifella australica

E

Rhynchaustrobates SWB 60

R

Recifella vonjama

E

R

Unionicola sp. Number of species

142

Polluted

E

Limnesia ekama

Albia australica

Hydrodroma SWB9

Unpolluted

Limnesiidae

Oribatida

Arrenurus sp.

Species

E 38

21

6

5

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

STUDY OF THE DIVERSITY OF PTYCTIMA (ACARI: ORIBATIDA) AND QUEST FOR CENTRES OF ITS ORIGIN: THE FAUNA OF THE ORIENTAL AND AUSTRALIAN REGIONS

Department of Animal Taxonomy and Ecology, Adam Mickiewicz University, Szamarzewskiego 91A, 60–569 Pozna, Poland

....................................................................................................

Wojciech Niedba¬a

.................................................................................................................................................................................................................................................................

Abstract The faunas of ptyctimous mites of different subregions of the Oriental and Australian regions have been described and analysed. Similarity between the faunas of these and the neighbouring regions is statistically insignificant, the only common species being the widely distributed ones. No species has been found to occur only in neighbouring regions. Arguments are given to support the thesis that the Orient is the centre of origin and speciation of ptyctimous mites. The hypothesis that all genera originated before the breakup of Pangea, and that in some regions certain species underwent strong speciation and adaptive radiation, has been supported.

INTRODUCTION The moss mites of the group Ptyctima (Acari, Oribatida) have the ability to fold the aspidosoma under the opisthosoma to protect their appendages. They belong to two separate cohorts of primitive moss mites. The superfamilies Protoplophoroidea, ptychoid only in the adult stage and Mesoplophoroidea, ptyctimous in all ontogenetic stages, belong to Enarthronota, whereas the superfamilies Euphthiracaroidea and Phthiracaroidea (both known as Euptyctima), ptychoid only in the adult stage, belong to Mixonomata. So, ptychoidy is a convergent feature. The Euptyctima are macrophytophages and feed on dead organic matter of plant origin; the majority of them are xylophages. Living in litter and dead leaves they create irregular galleries and cavities in decayed wood (immature stages in particular), and take part in mechanical fragmentation of organic matter. This paper is a contribution to a comprehensive series on Ptyctima of the world. Previous studies include a review of Phthiracaroidea to about 1988 (Niedba¬a 1992), ptyctimous mites of Pacific islands (Niedba¬a 1998a), Central America (Niedba¬a and Schatz 1996) and Euphthiracaroidea of the Ethiopian region (Niedba¬a 1998b). The objective of this paper is to summarise

knowledge on the distribution of Ptyctima species in the Oriental and Australian regions, estimate comparative faunal diversity, and to attempt to identify the centres of origin of those faunas. Information on the Ptyctima from the Oriental and Australian regions is provided in a few papers mainly concerning species descriptions. For the Oriental region these works are those of Mahunka, Niedba¬a, and a few individual papers by Aoki, Berlese, Hu, Jacot, Hammer, Oudemans, Ramsay, Sellnick, Sheals, Stary and Wang. For the Australian region these works are those of Balogh J., Balogh P., Lee, Luxton, Mahunka, Niedba¬a, Ramsay, Spain and Wallwork. Usually, the first difficulty in biogeographical studies is delimitation of the regions. They are determined after an analysis of the fauna and are usually different for different animal groups. As far as the Oriental region is concerned, the problem is not only the southern border with the Australian region, but also the northern delimitation with the Palaearctic. Generally this latter border can be delimited by the desert area between India, Pakistan and Afghanistan, or along the Indus river, on the west, and by the ridges of the Hindukush and Himalaya mountains and the limiting edges of the southern China mountains or the Yangtzikiang

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Wojciech Niedbala

river to its mouth, on the north. There are many specific regions, especially along the south coast of Asia, which are the areas of the occurrence of many oriental species. For instance, Japan appears as a meeting point for Palaearctic and Oriental faunas; 13% of the genera found there are of Gondwanan origin (Hammer and Wallwork 1979). These regions have been treated separately under the name of ‘border zone of the Oriental region’ and the specific character of their fauna and its relationships to those of the adjacent regions have been determined. The region of the western and northern outskirts of the Orient includes Pakistan, northern India (Himalah Pradesh, Kashmir), Nepal, Bhutan, Korea, Japan, and even the areas at the Pacific coast of Russia, such as the Kuril Islands and Sakhalin. In these areas lying at the border of Oriental and Palaearctic regions, the fauna is of mixed character and it is hard to tell which species are the Oriental and which Palaearctic elements. It seems however, that the moss mites occurring along the eastern and southern outskirts of the Palaearctic are closer to the fauna of the Orient than to that of the Palaearctic.

MATERIALS AND METHODS The material on which the presented analysis has been made includes species determined by the author, from collections of different museums and institutions. The largest part of the material studied are new species and those which were found in new localities. Particular specimens selected from samples were subjected to microscopic morphological analysis, and identified or, when new, thoroughly described. Another part of the material studied comes from the earlier works of the author. The analysis was also based on literature data, on species described by other authors for which I have not studied material. Publications without detailed descriptions, or elements documenting finding of a given species were not incuded. For example, Sanyal and Bhaduri (1986) mention finding two species in India described by Hammer (1961) from Peru: Rhysotritia ventosus and R. peruensis. It is highly improbable that these two species occur in the Oriental region. The Ptyctima material studied comes from different habitats of the Oriental and Australian regions. For the purpose of clarity, the regions were divided into the following subregions. Oriental region: 1. India including Sri Lanka and Maldive Islands (81 samples), 2. China (4 samples), 3. Indo-Chinese Peninsula with Thailand, Vietnam and the part of Malaysia (100 samples), 4. Philippines (84 samples), 5. Sumatra (12 samples), 6. Borneo with part of Malaysia, Timor, Sabah and Sarawak (62 samples), 7. Sulawesi (11 samples), 8. Java and Bali (19 samples). Australian region: 1. Papua New Guinea (37 samples), 2. Queensland (26 samples), 3. Western Australia (4 samples), 4. New South Wales (28 samples), 5. Tasmania (135 samples), 6. New Caledonia (15 samples), 7. New Zealand (248 samples). As a distance coefficient between the fauna of the subregions, the following statistic was calculated (Sokal and Rohlf 1995): 2

a 2 χ = ------------------------(a + b + c)

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where: a is the number of species common to both communities, b and c – the number of species found only in the first and in the second faunas, respectively. The distance measured by the above equation has a χ2 distribution with one degree of freedom. The minimum possible distance is 0 – for completely dissimilar faunas without common species, and the maximum, equals the total number of species in the faunas of both regions – for faunas with identical species composition. The above statistic was used to test the null hypothesis that the distribution of the number of species common for both faunas and the number of uncommon species fit the expected distribution for completely dissimilar communities. The acceptance of the null hypothesis (p>0.05) means that the distribution of numbers of common and uncommon species does not differ from that of completely dissimilar communities.

RESULTS AND DISCUSSION 1. Assessment of the ptyctimous fauna of the Oriental region.

In the course of the study, 119 species of Ptyctima were found in the Oriental region: the superfamily Phthiracaroidea – 53, Euphthiracaroidea – 47, Mesoplophoroidea – 17 and Protoplophoroidea – 2; 27 species were new to science: Phthiracaroidea – 16, Euphthiracaroidea – 8 and Mesoplophoroidea – 3. The widespread species (dispersalists) were few: 4 semicosmopolitan (3.4%) and 11 pantropical (9.2%), belonging mostly to Phthiracaroidea. Only one species Mesoplophora (Mesoplophora) invisitata Niedba¬a was also found in the Ethiopian region. Among the three probably introduced species: Atropacarus (Atropacarus) striculus (C. L. Koch) was of Holarctic origin, Microtritia minima (Berlese) – of Palaearctic origin and Phthiracarus membranifer Parry – of European origin. A large number 101 species (84.9%), were of Oriental origin, and the relative contribution of this zoogeographical element in particular superfamilies was similar. Nearly 2/3 of the species (79) have low mobility and are not found outside the Oriental region. A significant percentage (51.2%) of the Ptyctima species of the Oriental region are endemic and this percent is a bit higher among Phthiracaroidea (60.4%) than among Euphthiracaroidea (44.7%). Endemic species are scattered and occur in different Oriental subregions, the majority in Vietnam. Apart from the above mentioned, three species (P. membranifer, A. (A.) striculus and M. minima) were probably accidentally introduced from the Palaearctic. None of the species from the faunas of the neighbouring regions penetrates the Orient. Euphthiracaroidea of the Oriental region include by 14 genera, with 2 subgenera, a number higher than in any other zoogeographical region of the world (Table 1). Most abundantly represented are two phylogenetically distant genera: the primitive Oribotritia (7 species) and phylogenetically much younger Rhysotritia (9 species). Also, the phylogenetically distant genera of Phthiracaroidea from this region are represented by a relatively high number of species. Each of the genera Mesoplophora and Apoplophora belonging to Mesoplophoroidea is represented by 8 species (Table 1). Interestingly, a particularly strong adaptive radiation of the genus Apoplophora, unique to this Region, is evident. More species were found in the three northern subregions (in India, the Indo-China Peninsula and Borneo) than on the southern and eastern islands.

ORIENTAL AND AUSTRALIAN PTYCTIMA

2. Assessment of the ptyctimous fauna of border zone of the Oriental region adjacent to Palaearctic.

At the border of the Palaearctic and Oriental regions, 98 species were found including: Euphthiracaroidea – 49, Phthiracaroidea – 45 and Mesoplophoroidea – 4; among which were 9 species new to science (Phthiracaroidea – 1 and Euphthiracaroidea – 8). Widespread species make a small contribution, however, with that of Phthiracaroidea higher than that of Euphthiracaroidea. The contribution of southern species to this fauna (pantropical and Oriental ones) is only slightly higher (19.4%) (that of Oriental Euphthiracaroidea species a few times greater than that of Phthiracaroidea) than that of Holarctic and Palaearctic species (16.3%). Although it is a transitory zone characterised by a mixed fauna of the two bordering regions, the number of endemic species is surprisingly high, being almost half (43.9%) of all the species found, and for Euphthiracaroidea more than half. The greatest number of endemic species was found in Japan, northern India and Nepal. The number of genera of Euphthiracaroidea in the bordering part of Palaearctic and Oriental regions is much lower than in the main part of the Oriental region. As in the Oriental region, the genera of Euphthiracaroidea are represented by a similar number of species from the phylogenetically different lineages: the primitive Oribotritia and Mesotritia on the one hand, and phylogenetically distant Euphthiracarus and Rhysotritia on the other (Table 1). The number of genera of Phthiracaroidea in the two regions is the same, however; more than 70% of the species belong to primitive genera, and almost half of the species belongs to the genus Phthiracarus (Table 1). 3. Assessment of the Australian region fauna.

The number of the known species of Ptyctima in the Australian region is 143, with greater representation of Phthiracaroidea (114) than Euphthiracaroidea (26), and only 3 Mesoplophoroidea presented. Almost half of the species found were collected from the continent (71) (Phthiracaroidea – 56 and Euphthiracaroidea – 14), while the rest were recorded from nearby large islands. Thirty seven species were new to science including 28 Phthiracaroidea and 7 Euphthiracaroidea. Among Euphthiracaroidea and Phthiracaroidea the number of widespread species is similar, however, of a relatively small number of Euphthiracaroidea the pantropical species make up one third of the fauna. Two species seem to have been introduced from the Palaearctic: Euphthiracarus monodactylus Willmann and Austrophthiracarus latior (Niedba¬a). There are only 6 species of Oriental origin. As much as 84% of species are Australian, including almost 65% endemics. Apart from these, the greatest number of widespread species is on the continent. Endemism is most pronounced among the Phthiracaroidea (almost 77%) on the continent, New Zealand and Tasmania. Endemism in Euphthiracaroidea is relatively low (23%) and strongest in New Zealand. In the Australian region the Euphthiracaroid genera are much less abundant than in the Oriental region, however, as in the other regions phylogenetically distant genera are represented by a similar proportion of species.

The Phthiracaroidea are represented by a large number of genera and subgenera, larger than in any other zoogeographical region of the world. Moreover, the most abundant in species are two relatively phylogenetically young genera: Austrophthiracarus and Notophthiracarus. The latter seems highly plastic as the process of its speciation is particularly pronounced. Almost half of the species of the fauna of the region belongs to these genera (Table 1). 4. A comparison of the ptyctimous fauna of the regions.

The ptyctimous mites of all the regions and subregions investigated are so individual in character that any similarity among them is statistically insignificant (χ2 test). Moreover, their common species are widespread (semicosmopolitan and pantropical), so that they cannot be treated as a measure of similarity between the faunas of the regions. (a) a comparison of the Ptyctima faunas of the Orient with that of border zones From among 119 ptyctimous species found in the Oriental region and 98 species found in the bordering zone, only 18 are in common, and the majority of them (10) belong to Euphthiracaroidea. Almost half of these are widespread: 5 are semicosmopolitan (Archoplophora rostralis (Willmann), Atropocarus (Hoplophorella) cucullatus (Ewing), Plonaphacarus kugohi (Aoki), Rhysotritia ardua (C. L. Koch)) and 3 are pantropical (Atropacarus (Hoplophorella) vitrinus (Berlese), Microtritia tropica Markel, R. comteae Mahunka. Eight species are of Oriental origin (Apoplophora pantotrema (Berlese), A. saraburiensis Aoki, Indotritia javensis (Sellnick), I. propinqua Niedba¬a, M. similis Niedba¬a, Notophthiracarus robertsi (Sheals), Oribotritia submolesta Niedba¬a, R. aokii (Niedba¬a), and only 2 come from the north: Holarctic A. (A.) strictulus and Palaearctic M. minima. The above numbers indicate a stronger penetration of oriental species into the northern and eastern bordering zones of the region. (b) a comparison of Ptyctima of the Oriental and Australian regions The Oriental (119 species) and Australian regions (143 species) share only widespread species: among them only one is semicosmopolitan (A. (H.) cucullatus) and 10 pantropical (Sobacarus corneri Ramsay and Sheals, Indotritia krakatauensis (Sellnick), Austrotritia lebronneci (Jacot), P. kugohi, R. comteae, R. lucida Niedba¬a, R. spiculifera Mahunka, M. tropica, A. (H.) vitrinus, A. (H.) floridus. Only 4 oriental species have reached the Australian region (A. pantotrema, Austrotritia robusta (Niedba¬a), Phthiracarus obscurus Niedba¬a, Phthiracarus paucus Niedba¬a). No species shared exclusively by these two zoogeographical regions have been identified. (c) a comparison of Ptyctima from the Oriental and the Ethiopian regions. In the Oriental region there are many more species from Euphthiracaroidea and Mesoplophoroidea, whereas in the Ethiopian Region there are more representatives of Phthiracaroidea. Among 119 species found in the Oriental region and 145 species from the Ethiopian region (Niedba¬a 1998 and unpublished data) there are only 3–4 common semicosmopolitan species (from among Euph-

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Wojciech Niedbala Table 1

The number of species of ptyctimous genera (Protoplophoroidea, Mesoplophoroidea, Euphthiracaroidea and Phthiracaroidea) in selected geographical regions.

Genera Protoplophoroidea Prototritia Σ Mesoplophoroidea Archoplophora Dudichoplophora Mesoplophora Mesoplophora Parplophora Apoplophora Σ Euphthiracaroidea Oribotritia Mesotritia Maerkelotritia Protoribotritia Indotritia Indotritia Afrotritia Sobacarus Terratritia Austrotritia Euphthiracarus Euphthiracarus Pocsia Rhysotritia Bukitritia Sumatrotritia Microtritia Synichotritia Sabahtritia Temburongia Σ Phthiracaroidea Phthiracarus Plonaphacarus Hoplophthiracarus Steganacarus Steganacarus Rhacaplacarus Tropacarus Austrophthiracarus Arphthicarus Protophthiracarus Phrathicarus Notophthiracarus Atropacarus Hoplophorella Atropacarus Σ Grand total

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Oriental

S and E border of Palaearctic

Australian

Ethiopian

1 1 1 3

2 2

Pacific Islands

2 2 1

3 5 8 17

1 1

1 2 5

4

1 2 3

7 1

11 6 1 1

6

5 2

2

3

5

4

6 1

1

1 2 5

1

1

5

4

7

1

10

1 1

3

6

9 5

6

2

4

2

2

49

26

31

15

10 8 6

19 2 9

5 8 6

20 9 3

8 3 2

1 2

10 9

3 5

1 1 4 3

29 4

2 8 5

1

13

1

1 51

15

8

7 1 53

3 2 45

5 2 114

29 110

7 2 31

119

98

143

145

49

4 1 10 1 2 2 3 4 1 47

ORIENTAL AND AUSTRALIAN PTYCTIMA

thiracaroidea and Phthiracaroidea): R. ardua, Phthiracarus anonymus Grandjean, A. (H.) cucullatus, (Phthiracarus lentulus (C. L. Koch) considered as a Palaearctic species introduced to the Orient and Ethiopian regions, however, it may be cosmopolitan) and 9 pantropical species: P. kugohi, R. comteae, R. spiculifera, M. tropica, Phthiracarus pygmaeus Balogh, A. (H.) vitrinus, Atropacarus (Hoplophorella) singularis (Sellnick), A. (H.) stilifer (Hammer)). No other species occurs exclusively in these two regions. There are no common species of Mesoplophoroidea. The faunistic distinctness of these two regions is clear. (d) a comparison of Ptyctima from the Australian and Ethiopian regions. From among 143 species from the Australian region and 145 species from the Ethiopian there is only one semicosmopolitan: A. (H.) cucullatus (Ewing) and 7 pantropical common ones: (I. krakatauensis (Sellnick), P. kugohi (Aoki), R. comteae Niedba¬a, R. spiculifera Mahunka, M. tropica Markel, A. (H.) vitrinus (Berlese) and A. (H.) singularis (Sellnick)). No species occurs exclusively in these two regions and there are no common species of the Mesoplophoroidea, which testifies to the separateness of the faunas of these regions. (e) a comparison of ptyctimous fauna of the Pacific islands, Oriental and Australian regions. Among 49 species found on the Pacific Islands (Niedba¬a 1998a) as many as 20 are known from the Orient, but only 6 of them are of oriental origin (Mesoplophora (Parplophora) leviseta Hammer, A. lebronneci, A. saraburiensis, R. refracta Niedba¬a, Phthiracarus crispus Hammer and P. paucus). The other 14 are widespread semicosmopolitan (R. ardua and A. (H.) cucullatus) and pantropical species (A. pantotrema, S. corneri, I. krakatauensis, R. comteae, R. lucida, M. tropica, P. pygmaeus, P. kugohi, A. (H.) vitrinus, A. (H.) floridus, A. (H.) singularis, A. (H.) stilifer). From among the species found in the Australian region 19 occur as well on the Pacific islands. Only three Australian species have been introduced to the Pacific islands, one from New Guinea (Atropacarus (Atropacarus) griseus Niedba¬a) and two from Queensland (Phthiracarus forsslundi Niedba¬a, Plonaphacarus grandjeani Niedba¬a). No species originating from New Caledonia, New Zealand, Tasmania or southern Australia has spread to the Pacific islands. The faunas of Australia and Pacific islands have 15 widespread species in common including one semicosmopolitan species: (A. (H.) cucullatus) and 12 pantropical ones: (S. corneri, I. krakatauensis, A. lebronneci, R. comteae, R. lucida, R. refracta, M. tropica, P. kugohi, Hoplophthiracarus proximus Niedba¬a, A. (H.) vitrinus, A. (H.) floridus, A. (H.) singularis) and two species of Oriental origin (A. pantotrema and P. paucus). Thus, the ptyctimous fauna of the Pacific islands is under greater influence of the Oriental fauna than of the Australian fauna. 5. The centre of speciation and the origin of Ptyctima.

Analysis of the above data leads to a hypothesis that the Oriental region is the centre of origin of Ptyctima. The arguments supporting this thesis are: 1.

The presence of the primitive Protoplophoroidea.

2.

Greater diversity of the ptyctimous mites in this region, in particular greater diversity of genera of Euphthiracaroidea and species of Euphthiracaroidea and Mesoplophoroidea.

3.

Equalised and harmonious number of species of the Phthiracaroidea genera in the Orient, against the disharmonious fauna of the Australian region, in which only two genera Notophthiracarus and Austrophthiracarus undergo strong adaptive radiation and are represented by a large number of species.

4.

Harmonious fauna of Euphthiracaroidea represented by a great number of genera (14) when compared to that of the Australian region (7 genera).

5.

A large number of mobile species especially among Euphthiracaroidea in the Orient, which spread to Australia, SE Palaearctic and to the Pacific islands. The penetration of Oriental species into the Australian region is stronger than in the opposite direction. The influence of the Oriental fauna on that of the Pacific islands is greater than of the Australian fauna.

6.

The ptyctimous species of the neighbouring regions, despite distinctness, reveals greater similarity to that of the Orient than to any other region.

7.

From among the species common to the Oriental fauna and that of the border zone of the Palaearctic, over half are species of Oriental origin and only 2 of Holarctic and Palaearctic origin.

8.

The Orient is the centre of speciation of many other invertebrates.

Among the Oriental species of Ptyctima only about 20% are mobile and penetrate neighbouring geographical regions; they include more representatives of Euphthiracaroidea (31%) than Phthiracaroidea (9%). The Oriental species penetrating the Australian region and Pacific islands are: S. corneri, A. lebronneci, R. lucida, R. spiculifera, R. comteae, P. paucus; the one penetrating New Caledonia and other Pacific Islands is R. refracta; those penetrating New Guinea are: A. robusta, Mesoplophora (Parplophora) polita Niedba¬a; the one penetrating north Australia − A. pantotrema; the one penetrating the Pacific Islands − P. crispus. The only species common with the Ethiopian region is M. (M.) invisitata. The south and east borders of the Palaearctic region are penetrated by O. submolesta, M. similis, I. javensis, I. propinqua, A. saraburiensis, H. concinuus, N. robertsi and Apoplophora heterotricha Mahunka. The above evidence supports the hypothesis of Niedba¬a (1991), that all Phthiracaroidea genera originate from before the break-up of Pangea, and that in some regions certain genera adaptively radiated e.g Notophthiracarus and Austrophthiracarus in the Australian region. This thesis is also probable as far as Euphthiracaroidea is concerned: majority of genera of different phylogenetic age occurred before breaking up of continents. Strong adaptative radiation of ptyctimous mites in the Oriental region contributed to an increase in specific diversity. This distinctive differentiation

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of species considered with special respect to intraspecific taxa hiatus enables us to define new generic level taxa. 6. Endemism

The ptyctimous mites of the neighbouring: Oriental, Palaearctic, Ethiopian and Australian regions are distinct, relative to other groups of invertebrates. This distinctness is measured by a high proportion of endemic species in each of those regions. Shared components of their faunas (which are very low) involve only widespread (cosmopolitan and pantropical) species. It is usually assumed that profound endemism depends on a high degree of isolation of the territory on which it occurs and high degree of differentiation of environmental conditions within it. All zoogeographical regions analysed meet these conditions. Drift of the continents which shaped Australia and southeast Asia, and the islands in particular, had ended one hundred million years ago. All these regions show a considerable diversity of environments. Strongly pronounced endemism testifies to the evolutionary activity and intensity of speciation processes in the particular regions. In general, these species are neoendemites (progressive endemites), young taxa, not easily distinguished systematically. Examples of such species are: A. setus (Niedba¬a) and A. parasentus Niedba¬a, O. aokii Mahunka and O. paraaokii Niedba¬a in Vietnam, or O. asiatica Hammer, O. nepalensis Niedba¬a and O. subsolana Niedba¬a in Nepal. Some of them have very local distributions.

ACKNOWLEDGEMENTS I wish to express my thanks to the researchers who helped me obtain the type specimens and comparative material. I am particularly grateful to the Drs: J. Balogh, University of Budapest (especially for the access to the R. R. Forster collection from New Zealand), A. S. Baker, Department of Entomology, British

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Museum (Natural History), London, H. Enghoff, Zoologisk Museum, Copenhagen, R. B. Halliday, CSIRO, Division of Entomology, Canberra, P. J. van Helsdingen, Rijksmuseum voor Natuurlijke Historie, Leiden, G. F. Hevel, Smithsonian Institution, National Museum of Natural History, Washington, P. T. Lehtinen, Zoological Museum of Turku, R. A. Norton, State University of New York (especially for the access to the N. A. Walker’s collection of Euphthiracaroidea from New Zealand), H. Ono, Department of Zoology, National Science Museum, Tokyo. I thank Dr Valerie Behan-Pelletier (Ottawa) for her critical reading of the manuscript.

REFERENCES Hammer, M. (1961). Investigations on the oribatid fauna of the Andes Mountains. II. Peru. Biologiske Skrifter 13, 1–157. Hammer, M., and Wallwork, J.A. (1979). A review of the world distribution of Oribatid mites (Acari; Cryptostigmata) in relation to continental drift. Biologiske Skrifter 22, 1–31. Niedba¬a, W. (1991). Preliminary hypothesis on the biogeography of the Phthiracaroidea (Acari, Oribatida). In ‘Modern Acarology.’ (Eds. F. Dusbabek and V. Bukva.) p. 219–231. (Academia: Prague and SPB Academic: The Hague.) Niedba¬a, W. (1992). ‘Phthiracaroidea (Acari, Oribatida). Systematic Studies.’ (PWN: Warzawa, and Elsevier: Amsterdam.) Niedba¬a, W. (1998a). Ptyctimous mites (Acari, Oribatida) of Pacific islands. Genus 9, 431–558. Niedba¬a, W. (1998b). Euphthiracaroidea (Acari, Oribatida) of ethiopian region. Journal of African Zoology 112, 15–75. Niedba¬a, W., and Schatz, H. (1996). Euptyctimous mites from the Galapagos Islands, Cocos Island, and Central America. Genus 7, 239–317. Sanyal, A. K., and Bhaduri, A. K. (1986). Check list of Oribatid mites (Acari) of India. Records of the Zoological Survey of India 83, 1–67. Sokal, R. R., and Rohlf, F. J. (1995). ‘Biometry. The Principles and Practice of Statistics in Biological Research. (W. H. Freeman and Company: New York.)

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

GENETIC MARKERS AND MITE POPULATION BIOLOGY

CBGP, Institut National de la Recherche Agronomique, Campus International de Baillarguet, CS 30 016, 34988 Montferrier sur Lez, cedex, France. [email protected]

....................................................................................................

Maria Navajas

.................................................................................................................................................................................................................................................................

Abstract Population biologists now have at their disposal new molecular tools with which to explore some questions that were difficult to address just 10 years ago. Among possible applications of these methods are the detection of sibling species and races, examination of genetic systems, tracing of the source of introductions, estimation of the level of migration, and gene flow between populations. These methods rely on the detection of genetic variation at individual genetic markers and the application of the methods of population genetics. Mitochondrial and nuclear variation in tetranychid mites are used to illustrate how different markers can provide different types of information about evolutionary biology, and to show the advantages of using a combination of different markers.

INTRODUCTION Variation, or biodiversity as it now tends to be called, may occur at the individual, intraspecific, specific or ecosystem level. Variation at the molecular level has been described and quantified only relatively recently, although it has long been recognised that individuals in a population vary phenotypically. This paper concentrates on the use of molecular markers and the utility of measuring molecular variation for population level studies. The study of biodiversity in acarology is faced with two major problems with regard to population studies. One is that of establishing a reliable taxonomy and being able to recognise different species unambiguously. The second is that of describing at the infraspecific level the amount and pattern of differentiation, because this helps (1) to understand the origin of species introductions or other historical phenomena and (2) to determine the possibility of local adaptation of populations. Apart from these fields of applied research, mites can also form fascinating material for more academic research in population biology and evolution

because of the diversity of their life history traits and reproductive systems. Molecular markers have provided researchers with reliable and objective tools for addressing questions on population biology. These new tools are not an end in themselves but represent a technical tool that enables the addressing of points whose approach has been difficult up to now.

MOLECULAR TOOLS IN POPULATION BIOLOGY The genetic study of natural populations is dependent on the availability of polymorphic markers. The introduction of enzyme electrophoresis revolutionised population genetics. More recent techniques have involved the exploitation of polymorphic DNA sequences for population analysis. The invention of the PCR (Saiki et al., 1988) made possible the application of DNA-based techniques to the study of very small animals, such as most species of mite. PCR is now the first step in all DNA analysis.

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Maria Navajas

Several molecular techniques are available, and the choice and utility of any molecular marker in population biology and evolutionary studies depends critically on the type of question addressed. Since patterns of genetic variation within and between species vary considerably from locus to locus (see for example Li and Graur 1991), the power of a molecular marker to address a particular question depends on the hierarchical level of organisation of the ‘unit’ of interest (e.g. individuals, populations, species; see Hillis and Mortiz 1990). Distinction is made between two categories of genetic marker, depending on whether the work concerns a particular locus or several loci at the same time. The first category includes isozymes, microsatellites, RFLP (restriction fragment length polymorphism) and sequencing. The second contains RAPD (random amplified polymorphic DNA). Enzyme electrophoresis

Different alleles of the same gene can often be distinguished by measuring the migration of proteins through an electric field in a gel matrix (Pasteur et al., 1988). Information about gene flow, allele frequencies and other parameters that are crucial in population biology are obtained through this approach by combining information from several loci. Microsatellites

Microsatellites consist of the tandem repetition of a short pattern of one or several nucleotides. Strong variability in the number of repeats at a given locus is generally observed. This provides a large number of alleles per microsatellite locus. Their utility in population studies has been reviewed by Jarne and Lagoda (1996). RFLP and sequencing

These classic molecular biology techniques are beginning to be used in the study of mites. The information to be used consists of the variation in the restriction enzyme profile of a DNA region or the variability of its sequence. Different regions of the genome can be analysed according to the question examined (see Hillis et al. 1996 for a review).

APPLICATION OF MOLECULAR TECHNIQUES TO POPULATION PROBLEMS

It is not possible to provide a detailed list of the many applications in which molecular tools have played a major role. Whole books have been devoted to them (Avise 1994; Berry et al., 1991), so only a few examples will be discussed here. Qin (1997) used five polymorphic allozyme loci to trace the origin of a major pasture pest Halotydeus destructur (Tucker) from its putative source in South Africa to Australia. Weeks et al. (1995) used allozymes to appraise the clonal diversity in populations of the thelytokous blue oat mite Penthaleus major Dugès. The role of environmental heterogeneity was proposed to explain spatial and temporal maintenance of clonal diversity. Examples of the use of DNA-based techniques are the detection of sibling species (Gotoh et al. 1998), and the identification of the origin of pest introductions (Navajas et al. 1994). I make here a number of observations concerning the use of genetic data on the results obtained in my laboratory. They show how different markers can give a contrasting picture of the

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evolutionary history of species and show the advantages of the combined use of information provided by different markers.

CONTRASTED PATTERNS OF EVOLUTION OF MITOCHONDRIAL AND RIBOSOMAL DNA Two of the most popular markers for inferring phylogenetic relationships between organisms are mitochondrial DNA (mtDNA) and ribosomal DNA (rDNA). Simon et al. (1994) and Brower and DeSalle (1994) reviewed the application of these methods in arthropods. The comparison of these two markers is interesting because their modes of evolution are very different. Mitochondrial DNA evolves clonally through maternal transmission. The patterns of evolution of animal mtDNA and its performance as a marker of intraspecific variation are well understood (Avise 1994). Ribosomal DNA is present in multiple copies in the genome. Its use for inferring phylogenetic relationships is rendered possible because of the process of concerted evolution (Dover 1982), ensuring intraspecific diversity to be generally small in comparison with interspecific divergence. To illustrate the influence of the mode of evolution of mitochondrial and ribosomal DNA on their polymorphism patterns, I subjected the same set of samples to the analysis of variation of nucleotide sequences for two markers. The first was a fragment of the mitochondrial cytochrome oxidase I (COI) gene and the second was the internal transcribed spacer 2 (ITS2) of ribosomal DNA. These markers are described by Navajas et al. (1997). Nucleotide sequences of these two markers were obtained for a worldwide set of samples of the species Tetranychus urticae Koch. The results obtained from the two markers were different. Whereas one unique sequence of ITS2 was detected in all the samples, the COI sequences displayed a certain degree of polymorphism, reflecting historical colonisation patterns of the species. It is important to note that one can thus characterise T. urticae by its ITS2 sequence. This homogeneity is an example of the effectiveness of the mechanism of concerted evolution to which the ribosomal sequences are subjected. Let us now compare the results obtained for the same two markers in Tetranychus turkestani (Ugarov and Nikolskii), a species that is phylogenetically very close to T. urticae. The T. turkestani ITS2 sequences are once again homogeneous, but clearly different from that of T. urticae. However, in constrast, COI sequences do not discriminate the two species. The mitochondrial sequences are not subjected to homogenisation, and closely related species, such as T. urticae and T. turkestani, might share ancestral mitochondrial polymorphism that remains in the populations even after the interruption of gene flow that occurred during the speciation phenomenon. In conclusion, ribosomal ITS2 seems to be a very good marker for species diagnosis. While mitochondrial COI supplies information concerning the geographical structuring and colonisation patterns of the species, it may not be suitable for species diagnostics in comparisons of closely related species.

REFERENCES Avise, J. C. (1994). ‘Molecular Markers, Natural History and Evolution.’ (Chapman and Hall: New York.)

GENETIC MARKERS AND MITE POPULATION BIOLOGY

Berry, R. J., Crawford, T. J., and Hewitt, G. M. (1991). ‘Genes in Ecology.’ (Blackwell: Oxford.) Brower, A. and DeSalle, R. (1994). Practical and theoretical considerations for choice of a DNA sequence region in insect molecular systematics, with a short review of published studies using nuclear gene regions. Annals of the Entomological Society of America 87 , 702–716. Dover, G. (1982). Molecular drive: a cohesive mode of species evolution. Nature 299, 111–117. Gotoh, T., Gutierrez, J. and Navajas, M. (1998). Molecular comparison of the sibling species Tetranychus pueraricola Ehara & Gotoh and T. urticae Koch (Acari: Tetranychidae). Entomological Science 1, 55–57. Hillis, D. M., and Moritz, C. (1990). An overview of applications of molecular systematics. In ‘Molecular Systematics.’ (Eds D. M. Hillis and C. Moritz.) pp. 502–515. (Sinauer Associates: Sunderland, Massachussets.) Hillis, D. M., Mable, B. K., Larson, A., Davis, S. K., and Zimmer, E. A. (1996). Nucleic Acids IV: sequencing and cloning. In ‘Molecular Systematics.’ (Eds D. M. Hillis, C. Moritz and B. K. Mable.) pp. 321–381. (Sinauer Associates: Sunderland, Massachussets.) Jarne, P., and Lagoda, P. (1996). Microsatellites, from molecules to populations and back. Trends in Ecology and Evolution 11, 424–429. Li, W. H. and Graur, D. (1991). ‘Fundamentals of Molecular Evolution.’ (Sinauer Associates: Sunderland, Massachussets.) Navajas, M., Gutierrez, J., Bonato, O., Bolland, H. R., and MapangouDivassa, S. (1994). Intraspecific diversity of the cassava green mite Mononychellus progresivus (Acari: Tetranychidae) using comparisons

of mitochondrial and nuclear ribosomal DNA sequences and crossbreeding. Experimental and Applied Acarology 18, 351–360. Navajas, M., Gutierrez J., and Gotoh, T. (1997). Convergence of molecular and morphological data reveals phylogenetic information in Tetranychus species and allows the restoration of the genus Amphitetranychus (Acari: Tetranychidae). Bulletin of Entomological Research 87 , 283–288. Pasteur, N., Pasteur, G., Catalan, J., and Bonhome, F. (1988). ‘Practical Isozyme Genetics.’ (Ellis Horwood: Chichester.) Qin, T. K. 1997. Population genetics of redlegged earth mites Halotydeus destructor and H. anthropus (Acarina: Penthaleidae) from Australia and/or South Africa. Bulletin of Entomological Research 87, 289–298. Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis K. B., and Erlich, H. A. (1988). Primer-directed enzymatic amplification of DNA with a thermostable DNA Polymerase. Science 239, 487–491 Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu H, and Flook, P. (1994). Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701 Weeks, A. R., Fripp, Y. J. and Hoffmann, A. A. 1995. Genetic structure of Halotydeus destructor and Penthaleus major populations in Victoria (Acari: Penthaleidae). Experimental and Applied Acarology 19, 633–646.

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ACAROLOGY: PROCEEDINGS OF THE 10TH INTERNATIONAL CONGRESS

EVOLUTIONARY ECOLOGY OF ACARINE REPRODUCTION

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

COERCION AND DECEIT: WATER MITES (ACARI: HYDRACARINA) AND THE STUDY OF INTERSEXUAL CONFLICT

1. Australian School of Environmental Studies, Griffith University, Queensland 4111, Australia 2. Department of Biology, Queen’s University, Ontario K7L 1N6, Canada

....................................................................................................

Heather Proctor1 and Karen Wilkinson2

.................................................................................................................................................................................................................................................................

Abstract In many taxa, courtship is neither a harmonious union of the sexes nor a masculine contest to impress females. Instead, females strive to retain control of fertilisation while males attempt to bypass female choice through deception or coercion. Here we discuss the mating biology of two clades of water mites (Parasitengona: Hydracarina), one exhibiting deceit (Unionicolidae) and the other coercion (Arrenuridae). Previous behavioural and cladistic studies of North American unionicolid species suggested that courtship could be an example of a ‘sensory trap’ in which male courtship takes advantage of pre-existing female sensitivities. We tested the robustness of the sensory trap hypothesis by adding several Australian species from previously unrepresented genera (Encentridophorus, Recifella) and subgenera (Neumania (Lemienia) sp.) plus one additional North American species of Neumania to the behavioural-cladistic analysis. The results neither support nor reject the sensory trap hypothesis, but rather maintain the ambiguity of the original conclusion. In some species of Arrenurus (Arrenuridae), possession of an intromittant device (the petiole) appears designed to bypass a female’s control over mate choice. We tested whether Arrenurus males with petioles (a) spent less time courting or (b) had simpler repertoires of courtship behaviour than males without petioles. There was no evidence of shorter courtship time in modified males; however, the least complex courtship occurred in a petiolate species and the most complex in an apetiolate one. More sensitive measures of courtship effort and complexity are required to thoroughly test this hypothesis.

INTRODUCTION Why do males tend to be gaudy and pugnacious while females are dull and demure? Darwin (1871) felt that elaborate characters in males resulted from selection for structures and behaviours that helped an individual to secure more or better mates. He termed this ‘sexual selection’, and divided it into two categories: intraand intersexual selection. Darwin’s contemporaries were quite willing to accept that battle between males for access to females could select for more powerful weapons (intrasexual selection); however, they found it difficult to credit female animals with the sense of aesthetics necessary to select for more attractive males (intersexual selection) (Andersson 1994; Shelley and Whittier

1997). It was almost a century before biologists began to re-investigate the theory of sexual selection through female choice. Trivers (1972) showed that sexual differences in behaviour are likely to be the result of differences in gamete size. Female gametes are large and rare relative to those of males. When a resource is rare, there is competition for it; thus males pursue and females choose. Sometimes the situation is reversed, if males become the limited sex due to environmental contitions (e.g. Gwynne and Simmons 1990) or parental investment (e.g. Clutton-Brock and Vincent 1991). However, this idea does not explain why certain male characters are modified as sexual ornaments and not others. Until recently, two hypotheses have vied for supremacy as

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Heather Proctor et al.

explanations for the evolution of elaborate male traits and female preferences for them. The good genes model suggests that a female should choose a male with traits that indicate his possession of high quality genes that can be passed to her offspring. This has been tied to parasite resistance (Hamilton and Zuk 1982) and to morphological symmetry as externalisation of good genes (e.g. Møller 1992). However, with a few exceptions, the crucial evidence that more elaborate males do sire better offspring is lacking. The rival hypothesis, runaway sexual selection, does not predict that male courtship traits should be associated with high genetic quality. Rather, it asserts that the genes for arbitrary male characters may by chance be genetically linked to female preferences for those characters. If the female preference for elaboration is openended, this may result in the evolution of ever greater gaudiness until the process is curtailed by natural selection. Runaway selection has received a great deal of attention from theoretical modelers (Andersson 1994). Empirically, however, there has been little attempt to test the runaway model. This is likely because runaway makes no testable predictions about what male traits should be modified, or of the direction (larger vs. smaller, duller vs. gaudier) in which the trait should evolve. In the late 1980s and early 1990s, a new hypothesis joined the fray. In the sensory exploitation scenario, females have a pre-existing bias or sensitivity ( = preference) to sensory cues of a particular type (Basolo 1990; Proctor 1992a; Ryan and Rand 1993; Shaw 1995). These cues need not be sexual, but rather may operate in a different realm of the female’s life (e.g. foraging, care of offspring). If a mutation allows a male to produce signals that stimulate the female in that region of sensitivity, and if the female’s response increases the male’s probability of mating, then the mutation for the novel male trait will spread. Good genes are irrelevant as long as the mutation doesn’t render males less viable, and rather than the male trait running away with the female preference, it catches up to her bias. A similar hypothesis has been termed ‘sensory drive’ by Endler (1992), who includes characteristics of an organism’s environment as well as its internal biases as selective forces for signals. The latest hypothesis to arrive is the sexual conflict theory. Adherents of the ‘conflict’ school feel that there is a battle between males and females for control over fertilisation. The courtship dances and elaborate genitalia of males are interpreted not as offerings to please choosy females, but as armaments to coerce or deceive females into giving up their eggs (e.g. Arnqvist and Rowe 1995; Alexander et al. 1998). Females in turn raise their thresholds of sensitivity to such male subterfuge, resulting in cycles of deception, disbelief, and stronger deception. This process has also been termed ‘chase-away’ sexual selection (Holland and Rice 1998). This sexual arms race is thought to be a driving force in the evolution of diversity (Parker and Partridge 1998), just as the battles between hosts and parasites and plants and pollinators are considered engines of diversification (Brooks and McLennan 1991; Mitter et al. 1991; Pellmyr 1992). The sensory exploitation and arms-race hypotheses are not mutually exclusive; in fact, Holland and Rice (1998) consider sensory exploitation to be the starting point of the cycle of escalating deception.

156

TESTING INTERSEXUAL-CONFLICT HYPOTHESES Intersexual-conflict hypotheses make several predictions. First, that females are often induced into mating when it is not in their best interests. There is good evidence for this in drosophilid flies. Female Drosophila melanogaster that mate repeatedly die earlier than singly mating females (Fowler and Partridge 1989). Rice (1996) showed that when female lineages are kept from coevolving with male lineages, the lifespans of such females are even more reduced by the act of mating than are those of coevolved females. This implies that males and females are in a constant battle in which toxic chemicals in male ejaculates usurp control over fertilisation and oviposition (Eberhard 1998). Another prediction of the conflict hypothesis is that morphological and behavioural tactics of each sex will change over time, as modes of attack by males are rendered ineffective by evolutionary changes in female defences. This pattern may be recoverable through phylogenetic analysis (Holland and Rice 1998). One might predict that male courtship would accumulate embellishments over evolutionary time while female coyness would increase. Thus, male genitalia may become more complex in derived species, and female sperm receptacles may evolve more tortuous paths. Conversely, the ‘discovery’ of a superior tactic may allow males to dispense with earlier, more costly structures or behaviours; this predicts that expensive types of courtship should be abandoned after the evolution of a powerful coercive device. Because the sensory exploitation hypothesis is inherently historical (i.e. it requires that one event occurs before the other), one type of test involves a phylogenetic approach – does the original female sensitivity precede the appearance of the male’s trait when these characters are mapped onto a cladogram? This approach has been taken for a wide range of taxa and courtship characters (tungara frog calls, Ryan et al. 1990; swordtail fish tails, Basolo 1990; mite leg-trembling, Proctor 1992a; spider dances, McClintock and Uetz 1996). The intersexual conflict hypothesis also has historical predictions, but as yet there have been no phylogenetic tests for patterns of escalating coercive characters in males. The other approach to testing these hypotheses is ethological. For the sensory exploitation scenario, one might predict that courtship cues produced by the male also occur in another, non-sexual context, where they would elicit similar female behaviour. Instances in which males mimic non-sexual cues to deceive females have been termed ‘sensory traps’ by Christy (1995). Although sensory traps have been casually hypothesised to occur in several taxa (e.g. Drosophila courtship song, fragrances produced by male bees; West-Eberhard 1984), the idea has been thoroughly tested in only two. Christy (1995) demonstrated that male fiddler crabs decorate their burrows to make them appear safe havens for frightened females. Proctor (1991) showed that male Neumania water mites mimic the vibrations of copepod prey during courtship. In response to this stimulation, the female orients to and clutches the male. This allows the sightless male to determine whether the chemical presence he is courting is a female or merely the pheromonal residues of one. Together with those of tungara frogs and swordtail fish, Proctor’s (1991, 1992a) studies of Neumania are almost invariably cited in

COERCION AND DECEIT: WATER MITES (ACARI: HYDRACARINA) AND THE STUDY OF INTERSEXUAL CONFLICT

Figure 1

Lateral views of the idiosomas of a typical female Arrenurus and of males of A. (Megaluracarus) manubriator, A. (Truncaturus) rufopyriformis, A. (Arrenurus) sp. nr. reflexus, and A. (Arrenurus) planus.

reviews of sensory exploitation (e.g. Christy 1995). Unlike the other two studies, Proctor’s have not been attacked as flawed (see Shaw 1995); however, some problems remain with the Neumania story. Of greatest concern is the fact that the tests were performed on a small number of taxa from the family Unionicolidae (3 of 15 genera; 8 of ca. 480 species). Moreover, the phylogenetic test was ambiguous about the order in which male and female characters evolved. One scenario involved female preference (net-stance) evolving before the male courtship character, but the other equally parsimonious scenario showed the male and female characters evolving simultaneously on the same branch of the cladogram. Although this is not evidence against sensory exploitation, it is not tremendously supportive. With the examination of more species, the story of the evolution of courtship behaviour in the Unionicolidae may be very different. In this paper, we extend the ethocladistic analysis of Proctor (1992a) by including a number of new genera and species of unionicolids from North America and Australia. For the sexual coercion aspect of the intersexual-conflict hypothesis, one would predict that males that have become highly modified to ‘force’ females to accept their sperm may forgo previous adaptations designed to convince females to accept them as mates. Choe (1998) notes that male Zoraptera that are able to maintain prolonged coupling with females through a genitalic ‘lock’ show no precopulatory courtship, while those without such coercive structures engage in extensive courtship, including offering a tasty secretion from their cephalic glands. In water mites, there are many examples of closely related species that seem to vary in the ability of males to coerce females into accepting their sperm. For example, the genus Arrenurus (Arrenuridae) comprises over 800 species divided into a number of subgenera based primarily on modifications of the male opisthosoma (termed the ‘cauda’). The typical mating position in this genus is for the female to be mounted on top of the male with her venter glued to his dorsum via secretions from caudal glands (Proctor 1992b). In the more early derivative subgenera (e.g. Truncaturus), the male’s hind body typically shows no modification other than being more elongate than the female’s (see Fig. 1, rufopyriformis). A

more extreme modification is found in the subgenus Megaluracarus, in which the cauda may be greatly elongated (Fig. 1, manubriator). More derived subgenera (e.g. Arrenurus, Fig. 1, nr. reflexus and planus) have a median protuberance – the petiole – that appears to be employed as an intromittant organ during sperm transfer. Males from subgenera characterised by lacking a petiole (e.g. Truncaturus, Megaluracarus) transfer sperm by first depositing spermatophores on a substrate, then lowering the female down so that the sperm packet is adjacent to her genital opening. Females of these species seem to have the option of accepting a male’s sperm or of keeping their genital flaps closed. This contrasts with females of the subgenus Arrenurus, in which the males forcibly insert their spermladen petioles into the female’s genital opening. In this paper we describe ethological studies on four species of Arrenurus, two with petiolate and two with apetiolate males, to examine whether males modified to bypass female choice over sperm uptake have less lengthy or complex courtships, or have females that appear more reluctant to mate.

MATERIALS AND METHODS A. Evolution of courtship trembling in the Unionicolidae

Data collection One of us (HP) observed the mating and predatory behaviour of several species of Unionicolidae to further test Proctor’s (1992a) sensory trap hypothesis for courtship trembling. Observations were made casually over the period from 1992 to 1996. These species were: Neumania (Neumania) latifemoris Conroy (from Edmonton, Alberta, Canada); Neumania (Lemienia) sp. nr. gila K. O. Viets (from a pond near Kakadu National Park, Northern Territory, Australia); and Encentridophorus sarasini Walter (numerous sites in southeast Queensland, Australia). With the exception of courtship trembling and predatory net-stance, behavioural and morphological characters of these species and of another species whose mating behaviour was not observed, Recifella triradiata Cook (from Booloumba Creek, Queensland, Australia), were added to the character state matrix of Proctor (1992a) (Table 1, Appendix 1). Two new morphological characters were added to Proctor’s (1992a) matrix: character 29, highly

157

158

1

0

0

0

0

0

0

0

0

0

0

0

1

1

1

1

1

0

Hydrodroma americana

Atractides nodipalpis

Huitfeldtia rectipes

Koenikea haldemani

Koenikea spinipes

Recifella triradiata

Neumania distincta

Neumania papillator

Neumania ‘ovata’

Neumania latifemoris

Neumania sp. nr. gila

Unionicola ‘red body’

Unionicola ‘red eye’

Unionicola ‘brown eye’

Unionicola ‘crassipes’

Unioncola ‘gracilipalpis’

Encentridophorus sarasini

0

1

1

1

1

1

0

0

0

0

0

0

0

0

0

0

0

2

1

1

1

1

1

1

0

1

1

1

1

1

1

1

1

0

0

3

0

0

0

0

0

0

0

1

1

1

1

0

0

0

0

0

0

4

0

1

1

1

1

1

1

0

1

1

1

0

1

1

0

0

0

5

0

0

0

0

0

0

1

0

1

1

1

0

0

0

0

0

0

6

1

1

1

1

1

1

1

1

1

1

1

1

1

1

0

0

0

7

0

0

0

0

0

0

1

1

1

1

1

0

0

0

0

0

0

8

0

1

1

1

1

1

0

0

0

0

0

0

0

0

0

0

0

9

0

0

0

0

0

0

?

?

1

1

0

?

?

?

0

0

0

10

Character state matrix for characters described in Appendix 1.

Species

Table 1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

0

0

0

11

0

0

0

0

0

0

1

1

1

1

1

0

0

0

0

0

0

12

0

1

1

1

1

1

0

0

0

0

0

0

0

0

0

0

0

13

0

1

1

1

1

1

1

1

1

1

1

1

0

0

0

0

0

14

0

1

1

1

1

1

0

0

0

0

0

0

0

0

0

0

0

15

0

0

0

0

0

0

1

1

1

1

1

0

0

0

0

0

0

16

0

0

0

0

0

0

0

0

0

0

0

1

1

1

0

0

0

17

1

1

1

1

1

1

0

1

1

1

1

0

0

0

0

0

0

18

0

1

1

1

1

1

0

0

0

0

0

0

0

0

0

0

0

19

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

0

0

20

0

1

1

1

1

1

1

1

1

1

1

0

0

0

0

0

0

21

0

0

0

0

0

0

0

0

0

0

0

0

1

1

0

0

0

22

0

1

1

1

1

1

?

0

0

0

0

?

?

0

?

0

0

23

?

?

1

0

0

0

0

1

0

0

0

0

0

?

? 0

1

1

1

1

1

1

0

?

? 1

0

?

? 1

0

0

25

0

0

24

1

1

1

1

1

1

?

1

1

1

0

?

?

1

?

0

0

26

0

0

0

0

0

0

0

1

1

1

0

?

?

0

?

0

0

27

1

0

0

0

0

0

1

0

0

0

0

?

?

1

?

0

0

28

0

0

0

0

0

0

1

1

1

1

0

1

1

1

0

0

0

29

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

0

0

30

Heather Proctor et al.

COERCION AND DECEIT: WATER MITES (ACARI: HYDRACARINA) AND THE STUDY OF INTERSEXUAL CONFLICT

pectinate seta at distal end of tibia of LIII (at least in females); and

Figure 2

Dorsal view of male and female Encentridophorus sarasini (Unionicolidae) prior to the female mounting the male (see text for details).

character 30, location of eye capsules. Also, the species originally called Neumania nr. muttkowski Marshall in Proctor (1992a) appears to be closer to N. ovata Marshall. Data analysis The matrix was entered into the HENNIG86 program (version 1.5, distributed by J. S. Farris, New York) with Hydrodroma despiciens as the designated outgroup. All characters were given equal weight, and the implicit enumeration (ie*) algorithm was used to identify all trees that were of equal, shortest length. Courtship trembling and net-stance were mapped onto the resulting tree(s) to determine the order in which these characters evolved. B. Comparative study of sperm transfer behaviour of Arrenurus species

Mite collection and maintenance One of us (KW) compared the mating behaviour of four species of North American Arrenurus to test the hypothesis that species with males modified for intromittant transfer of sperm should have less complex courtship, spend less time courting, and have females that showed a greater reluctance to mate. Males of two of the species lacked intromittant petioles while those of the other two had them (Fig. 1).

Data for Arrenurus manubriator Marshall were obtained from Proctor and Smith (1994) and Proctor (unpub). The other species were collected from the Queen’s University Biological Station near Chaffey’s Locks, Ontario, Canada. (hereafter QUBS) or were provided by Dr Bruce Smith (Ithaca College, NY), and were maintained and observed at QUBS. Arrenurus planus Marshall were collected in the deutonymphal stage from ponds near QUBS. Each deutonymph was placed in its own vial with ostracods for food. The vials were kept in situ until the mites transformed into adults. Adult A. planus were maintained individually in tissue culture wells filled with water and were fed ostracods from a colony located at QUBS. Both Arrenurus rufopyriformis Habeeb and Arrenurus sp. nr. reflexus Marshall were collected from sites at and near QUBS and cultured by Bruce Smith . We obtained them just after they emerged as adults. Mating observations: videotaping A tissue culture well was half filled with water and the well bottom was scratched with tweezers to create a textured substrate. The culture well was then placed under a Panasonic black and white security camera fitted with a Micro-Nikkor 105mm 1.28 macro lens. The camera was connected to a monitor and Panasonic video recorder, and a small desk lamp was used as a moveable light source. The trial began when a conspecific male was introduced

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Heather Proctor et al.

to a well containing a female. Whenever possible, virgin adults were used, but some males were used twice. The entire mating

Figure 3

Lateral view of male and female E. sarasini; the female is mounted on top of the male (see text for details).

Mating observations: behavioural events While reviewing the videotapes, KW recorded the sequence of behavioural events, described the behaviours, and noted the duration of each behaviour using the recorder’s built-in timer. After all tapes had been reviewed, an ethogram (a chronological description of behavioural steps) was made for each species. The exception was A. manubriator; for this species, we modified an ethogram from Proctor and Smith (1994). Using the four ethograms, we compared types, complexities, and durations of behaviours between and within species and subgenera.

RESULTS A. Unionicolid phylogeny

Mating and predatory behaviour Complete mating sequences were obtained for Encentridophorus sarasini and Neumania latifemoris, while only partial observations were made for Neumania sp. nr. gila. Feeding was observed for all species. Encentridophorus sarasini showed a complex and interesting array of behaviours during sperm transfer. When placed in a well together with a female, the male moved in halting, clock-work jerks across the substrate. His legs IV were held vertically and the tarsi were twitched. Then, in a very rapid movement, he deposited

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behaviour of each pair was videotaped. Ten trials were run for each of A. planus, A. nr. reflexus and A. rufopyriformis.

a webbed-together group of spermatophores on the tarsi of his own legs III (Fig. 2). The sperm mass was centrally located, supported by strands attached to the tarsi. He held the spermatophores behind himself, and oriented his posterior idiosoma towards any passing sources of vibrations. The female showed no signs of orientation to the slight twitching of the male’s leg IV tarsi, nor did she clutch at them. If she was interested in mating, she groomed her venter vigorously, and then attempted to climb onto the male’s dorsum. As well as having modified legs III and IV, male E. sarasini have a saddle-shaped dorsum. The female’s venter fits snugly in this concavity (Fig. 3). Once on the male’s back the female was held in place by the male’s legs III. He kept his hind body lifted high off the substrate, and occasionally performed slow ‘press-ups’ by gently flexing legs I. The female stroked her legs IV over her dorsum and around to the male’s legs IV, presumably pressing the spermatophores into her genital opening. Predatory behaviour in E. sarasini did not involve netstance; rather, the mites simply grabbed whatever prey they bumped into in the course of swimming or crawling. They fed on cladocerans and occasionally on small dipteran larvae. Sperm transfer behaviour in Neumania latifemoris was very similar to that of Neumania papillator, including trembling, orientation of females to trembling males, deposition of a complex net of spermatophores on the substrate, and fanning with legs IV. The

COERCION AND DECEIT: WATER MITES (ACARI: HYDRACARINA) AND THE STUDY OF INTERSEXUAL CONFLICT

major difference was in the duration of fanning; while N. papillator fans for approximately 60 seconds, N. latifemoris did so for much shorter bouts of less than 20 seconds, and seemingly less

vigorously. Perhaps the modification of the femora of male N. latifemoris (they are noticeably broader than those of the female) is

ie* length 43, CI 69, RI 86, 8 trees¤ 3 positional subtrees Hydrodroma americana Atractides nodipalpis Huitfeldtia rectipes Recifella triradiata Koenikea spinipes Koenikea haldemani E. sarasini R. triradiata K. spinipes K. haldemani

A

N. nr. gila

Encentridophorus sarasini Unionicola gracilipalpis Unionicola crassipes Unionicola ‘redeye’¤ Unionicola ‘browneye’¤ Unionicola ‘redbody’¤

N. distincta

B

N. latifemoris N. ‘ovata’¤ N. papillator

C Figure 4

N. latifemoris N. ‘ovata’¤

Neumania distincta Neumania nr. gila Neumania latifemoris Neumania ‘ovata’¤ Neumania papillator

N. papillator

Schematic cladograms of the results of the HENNIG86 implicit enumeration algorithm, showing the three positional subtrees (A, B, and C) responsible for the eight cladograms.

an adaptation for greater efficiency of fanning. Predatory behaviour was the same as in N. papillator, with net-stance, orientation, and clutching of copepod prey. Nearly complete mating observations were made on only one pair of Neumania sp. nr. gila. Like males in other species of the subgenus Lemienia, male N. sp. nr. gila have modified tibiae on legs IV (see Viets 1975, Fig. 20). They are broader than the female’s and are equipped with spines near the junction with the tarsus. When placed in a well with a female, the male trembled legs I and II while rotating slowly on legs III and IV (‘spinning in place’). The female was not observed orienting to or clutching the male, but she seemed to take up a more cramped net-stance, with her legs curved inwards rather than spread widely. The male turned to face away from the female in her cramped net-stance and backed up until his posterior was almost directly beneath her raised legs I. He then deposited a mass of what was presumably spermatophore material on the tips of his own legs III, and grasped the female’s legs I with his modified legs IV. Then, holding on to the substrate with only his legs I, he gave strong, whole-body shakes by jerking his raised legs II. At this point we separated the couple in an attempt to observe ejaculate structure but did not succeed.

Thus we are not sure how sperm is transferred from the male’s legs III to the female’s genital opening. Predatory behaviour in N. sp. nr. gila is like that of other Neumania, with net-stance, orientation, and clutching at copepod prey. Cladograms Eight equally parsimonious trees were produced from the matrix of 17 species and 30 characters. The trees were 43 steps in length and had a CI of 69. Hydrodroma, Atractides and Huitfeldtia were always outgroups to a clade containing the unionicolid genera. Variation in the unionicolid trees occurred in three places (Fig. 4). One pair of positional subtrees (A vs main cladogram) varied in whether E. sarasini was grouped with Koenikea and Recifella, or at the base of a clade containing the sister genera Neumania and Unionicola. As Encentridophorus, Koenikea, and Recifella have not been observed to engage in net-stance or courtship trembling, this subtree is not relevant to the hypothesis. The second pair of subtrees (B vs main cladogram) differs in whether Neumania distincta is at the base of the Neumania clade or if that position is occupied by Neumania sp. nr. gila. As these species differ in the presence of net-stance and trembling, this variation is relevant to testing the

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hypothesis. The third pair of subtrees (C vs main cladogram) shows variation in the placement of three Neumania (Neumania) spp. ; as these taxa all display both net-stance and trembling, this variation is not of interest. Figure 5 shows the cladogram with the varation in the subtree of interest (B) displayed. The top two

Figure 5

Results of mapping net-stance (N) and trembling (T) on the cladogram. The top and bottom trees reflect the topological variation expressed in positional subtree B (see Fig. 4). Trees with Scenario I (net-stance and trembling evolve simultaneously) are presented on the left, and those with Scenario II (trembling evolves repeatedly after net-stance) are on the right.

same time as trembling, with trembling being lost in N. distincta, is as parsimonious (three changes) as the scenario of trembling evolving twice after net-stance. When they are mapped on the bottom pair of cladograms, the first scenario (of trembling being lost in N. distincta) is more parsimonious (two changes) than that of trembling evolving after net-stance (four changes). Thus Scenario I (simultaneous origin of net-stance and trembling) is more parsimonious in four of the eight trees, while Scenario II (of repeated origins of trembling after net-stance) is not more parsimonious in any of them. No tree supported the hypothesis that trembling evolved prior to net-stance. B. Arrenurus mating behaviour

Sixteen videotapes, each containing approximately six hours of mating trials, resulted in more than 100 hours of tape to analyse. The verbal descriptions below refer parenthetically to which of

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cladograms have N. distincta at the base of the Neumania clade, and the bottom two have N. sp. nr. gila in that position. When net-stance (N) and courtship trembling (T) are mapped onto the top pair of cladograms, the scenario of net-stance evolving at the

the sexes engaged in each behaviour. The verbal ethogram for Arrenurus manubriator is modified from Proctor and Smith (1994), in which most behaviours are illustrated. For the other species, both verbal ethograms and illustrations of selected behaviours are presented. Ethograms Arrenurus manubriator (n = 7 pairings) 1. Walking (both): Male and female walked around the well bottom with fourth legs held up over their backs, or moved them in a rotary motion (flailing). 2.

Ready position (male): Male crooked his fourth legs at the fourth distal segment and held them flat over his back when the female came into contact with or ran by the

COERCION AND DECEIT: WATER MITES (ACARI: HYDRACARINA) AND THE STUDY OF INTERSEXUAL CONFLICT

willingly climbed on to the male’s cauda; however, videotape evidence shows that the male uses his hind legs to capture the female (H. Proctor, pers. obs.).

male. Often he directed his cauda towards the female. The number of failed attempts was not noted. 3.

Mounting and gluing (male): Male grabbed female’s leg using fourth leg spurs then manoeuvred her onto his back. Female was then glued in mating position on male’s back. Proctor and Smith (1994) assumed that the female

Figure 6

4.

High vertical jerking (male): Male sharply jerked cauda upwards approximately once per second. Female stopped flailing her legs after jerking.

a–h. Mating behaviour of Arrenurus rufopyriformis (see text for details).

5.

Striking/stroking (male): After female stopped moving, male used fourth legs to strike or stroke the sides of the female.

6.

Low vertical shaking (male): While striking/stroking and with his cauda held parallel to the substratum, male shook

his cauda up and down more or less continuously, often walking over bottom of well. 7.

Slow lateral waving (male): Interspersed with periods of low vertical shaking, the male made slow lateral movements with his cauda close to the substrate.

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8.

9.

Spermatophore deposition (male): This only occurred if the pair were on a vertical surface (i.e. well wall). Male was motionless, then leaned backwards, pressed venter against substratum, rocked from side to side for several seconds, lifted slightly to reveal spermatophore stalk, then lifted again to reveal the sperm mass.

10. Tick-tock shuttling (male): Male was still for a few minutes after completing translocation, but then engaged again in

Spermatophore translocation (male): Male leaned forward to bring juncture of male cauda and female’s venter above

Figure 7

a-g. Mating behaviour of Arrenurus sp. nr. reflexus (see text for details).

low vertical shaking, striking/stroking, lateral waving and eventually tick-tock shuttling. In this behaviour, the male maintained his body parallel to substratum but lunged sharply side to side in almost clockwork fashion. 11. Violent shaking (male). The male lifted his cauda at approximately 45° to the substrate and vigorously swung his cauda in a 180° arc at a rate of approximately three to

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the spermatophore. He then lowered the female onto the spermatophore while moving his cauda from side to side and up and down. Deposition and translocation were repeated 8–21 times.

four times per second. Striking/stroking occurred simultaneously and was also vigorous. Typically, the female began to flail. 12. Separation (both): . This was achieved either during violent shaking or when female grabbed the substrate and twisted herself laterally, thus breaking the glue bond.

COERCION AND DECEIT: WATER MITES (ACARI: HYDRACARINA) AND THE STUDY OF INTERSEXUAL CONFLICT

Arrenurus rufopyriformis (n = 10 pairings, 1 male used twice) 1. Walking (both): After introduction to well, both male and female walked around with their fourth legs raised high over their backs, or moved them in a rotary motion (flailing). 2.

Ready position (male): Male crooked his fourth legs at the fourth distal segment and held them flat over his back when the female came into contact with or ran by the male. He presented his cauda to the female, and often attempted to push his back end under her (Fig. 6a). It took

Figure 8

4.4 ± 1.6 attempts (reactions or grabs) to successfully grab the female. 3.

Mounting and gluing (male): Male grabbed one of female’s legs using spurs on his fourth legs, then manoeuvred her onto his back. Female was glued in mating position on male’s back (Fig. 6b, c).

4.

Jerking and stroking (male): Male jerked cauda up repeatedly, but at a slower rate than A. manubriator. The female often stopped flailing her legs after jerking (Fig. 6d).

a-c. Mating behaviour of Arrenurus planus (see text for details).

5.

Stroking (male): Interspersed with jerking, the male stroked his fourth legs along sides of female’s body from rear to front (thus drawing her legs forward) (Fig. 6e).

11. Alternate rapid stroking (male): Male performed rapid stroking with one leg as in step 10, and then with the other leg (no jerks in between). This was repeated.

6.

Spermatophore deposition (male): Male paused motionless, then leaned forward (presumed to be drawing out a spermatophore) (Fig. 6f).

12. Stroking and jerking (male): Male returned to jerking and stroking (as in steps 4–5) with both legs, interspersed with periods of motionlessness. This was repeated.

7.

Spermatophore translocation (male): After each deposition, male rubbed his back end on substrate (presumed to be rubbing sperm onto female’s venter) (Fig. 6g).

13. Separation (both): Male brushed own body with fourth legs, or female grabbed substrate and twisted herself to face backwards – then used her legs to get off male.

8.

Repeated jerking and stroking and deposition (10–27 times) while walking around.

14. Grooming (both): Once separate, both brushed own body from front to back with fourth legs.

9.

Jerking with leaning (male): Male jerked cauda up repeatedly, with a slight sideways leaning.

10. Rapid stroking with jerking (male): Male made small, rapid stroking motions with one fourth leg repeatedly, then jerked his cauda up. This was repeated with alternate legs (Fig.6h).

Arrenurus sp. nr. reflexus (n = 10 pairings, 2 males observed twice) 1. Walking (both): As in A. rufopyriformis. 2.

Ready position (male): After first contact, male stopped and held legs slightly crooked over his back (Fig. 7a). He

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grabbed female with fourth leg spurs, and possibly used glue as well, as often after failed grabs there appeared to be a substance holding the tips of the male’s fourth legs together. The male took 5.25 ± 2.5 attempts to successfully grab the female. 3.

Mounting (male): Female was manoeuvred into mating position (glued on male’s back) (Fig. 7b).

4.

Walking, tapping and motionlessness (male): Male walked around, tapping female’s body with fourth legs,

Table 2

interspersed with periods of motionlessness (female may flail her legs). 5.

Spermatophore deposition (male). Male was motionless, then pulled up back end (assumed to be drawing out a spermatophore) (Fig. 7c).

6.

Spermatophore collection (male): After deposition, male leaned forward, rubbed back end of cauda on substrate (gathering sperm on petiole) (Fig. 7d).

7.

Side-jerking (male): Interspersed with deposition and collection, male jerked cauda side to side (Fig. 7e), and

Summary of mating behaviour in the four species of Arrenurus. Data are means ± S.E. Arrenurus planus does not deposit spermatophores, therefore its behaviour cannot be partitioned in the same manner as the other three species. A. manubriator* (N = 7)

A. rufopyriformis (N = 9)

A. nr. reflexus (N = 8)

A. planus (N = 7)

pre-deposition behaviour (%)

67.3 ± 4.6

9.6 ± 1.2

2.3 ± 0.26

N.A.

spermatophore deposition (%)

11.5 ± 2.31

15.2 ± 1.8

3.2 ± 0.34

N.A.

spermatophore number (N)

13.1 ± 1.89

10.8 ± 1.40

19.4 ± 1.954

N.A.

post-deposition behaviour (%)

21.2 ± 3.91

77.0 ± 2.5

94.3 ± 0.45

N.A.

pre-pairing duration (s)

N.C.@

224 ± 63.2

591 ± 288

300 ± 83.3

mean number of attempts

N.C.@

4.4 ± 1.6

5.3 ± 2.5

1.4 ± 0.29

total duration of mating (s)

7956 ± 1198

3398 ± 299

19540 ± 1179

5181 ± 1081

*

data from Proctor and Smith (1994) @ not calculated in Proctor and Smith (1994)

3.

Attachment (male): Male manoeuvred himself so as to be under the standing female, facing in the opposite direction as her, lying on his back. Male attached his fourth legs somewhere in the vicinity of the female’s hind coxae.

4.

Brushing (male): Male repeatedly brushed venter with third, second and first legs (Fig. 8c), presumably pushing sperm from his genital opening down towards his petiole, which appeared to be inserted into the female. Steps 4–5 occurred throughout the mating, and often at the same time.

5.

Brushing (female): Female used fourth legs to brush from her back to her underside, presumed to be pushing sperm into her genital opening (Fig. 8c).

6.

Walking (female): Female walked around – male was dragged around on his back and was often motionless. Walking was interspersed with periods of motionlessness.

12. Grooming (both): Both groomed own body, ran around.

7.

Separation (both): Pair separated when male let go with his fourth leg spurs.

There were many of periods of motionlessness throughout mating trials.

8.

Grooming (both): Once separate, both brushed own body with fourth legs.

tapped female with fourth legs. This was repeated (6–19 times). 8.

9.

Sperm translocation, side-jerking and tapping (male): Used fourth legs to push female back onto (presumably) spermladen petiole (Fig. 7f), jerked side to side, tapped female. Repeated. Motionlessness and side-jerking (male): Repeated. (female may flail).

10. Pullback (male): While keeping legs in place, male pulled his body back (as if attached to a string) (Fig. 7g) and then returned to original position and was motionless (sometimes slight rocking of body). Repeated. 11. Separation (both): Usually male pushed female off using his fourth legs.

Arrenurus planus (n = 10, 3 males used twice) 1. Walking (both): Both walked around the well bottom as in A. rufopyriformis. 2.

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Wrestling (male): When male came into contact he ‘wrestled’ with the female, climbing over and around her body, grabbing her with his legs (Fig. 8a). It took 1.4 ± 0.29 grab attempts to successfully continue on to the mating.

DISCUSSION A. Sensory traps and courtship in the Unionicolidae

The addition of observations for species from two genera not included in the analysis by Proctor (1992a), (Encentridophorus, Recifella), one new subgenus of Neumania (Lemienia), and a sexually dimorphic member of the subgenus Neumania (N. latifemoris) did little to alter the previous evolutionary interpretation of

COERCION AND DECEIT: WATER MITES (ACARI: HYDRACARINA) AND THE STUDY OF INTERSEXUAL CONFLICT

courtship trembling in the Unionicolidae. However, rather than a single most parsimonious tree, eight trees were produced from the modified character state matrix. None of the trees supported trembling evolving prior to net-stance, a scenario that would provide evidence against the sensory trap hypothesis. As in Proctor (1992a), there was support for both the possibility that trembling evolved several times after net-stance and that evolution of trembling and courtship occurred at the same time However, this analysis showed slightly more evidence for a concurrent origin than for repeated evolutions of courtship trembling (Fig. 5). As it was in the original analysis, Neumania (Tetraneumania) distincta is a crucial taxon in that it displays net-stance without trembling while all other Neumania so far observed engage in both behaviours. If it were excluded from the cladistic analysis, only the scenario of a simultaneous origin of net-stance and trembling at the base of the Neumania-Unionicola clade would be feasible. Further observations of this species and other members of the subgenus Tetraneumania may help to clarify its position within the Neumania+Unionicola clade, and hence the order of evolution of male and female characters. It would also be interesting to get complete mating observations for members of the subgenus Lemienia, as well as for other subgenera with modified males (e.g. Alloneumania). Other taxa worthy of further examination are Koenikea and Recifella, as the mating behaviour of only one species of Koenikea has been observed. B. Coercion in Arrenurus

Courtship duration and complexity There was no evidence that petiolate males spent less time in courtship than apetiolate males, based on the rough measure of total time males and females spent attached (Table 2). However, the most complex behavioural sequence was indeed shown by an apetiolate species (A. rufopyriformis) and the least complex by the petiolate species with the most direct form of sperm transfer (A. planus); however, the apetiolate A. manubriator and petiolate A. reflexus had a similar number of steps in their ethograms. Clearly, many more species must be observed to test the idea that complexity of sperm transfer behaviour is negatively related to degree of morphological coercion. Female willingness to mate Mating attempts were initiated by the males. We interpreted the number of attempts to mate by the male (ready position, directed his cauda towards the female, or grabbed the female) to be negatively correlated with female willingness to mate, for if the female were eager to mate there should be very few attempts before pairing occurred. Males of Arrenurus sp. nr. reflexus had the largest number of unsuccessful attempts before mating. Attempts for this species were split into two categories; male reactions (i.e. ready position and caudal direction) and male grabs; when added, the mean number of attempts (5.3 ± 2.5) was the highest of the three species whose mating attempts were monitored (i.e. excluding A. manubriator) (Table 2). Male A. planus had the most success in grabs leading to the mating position. However, even though these two species are in the same subgenus, the number of failed attempts are not easily compared. While A. sp. nr. reflexus uses its leg spurs to attempt to capture the female, A. planus uses all of its

legs and then climbs around on the female’s body for a period of time, thus making it difficult to determine separate attempts. However, the amount of time spent in pre-pairing activities (Table 2) can be more readily compared. We had expected that the petiolate species, A. sp. nr. reflexus and A. planus, would encounter higher female resistance because of the males’ potential ability to circumvent female choice, and would therefore have longer pre-pairing times. In non-petiolate species, even though the female is grabbed and placed on the male’s back, she has the ‘choice’ to open her genital flaps. The pre-pairing times support this hypothesis (Table 2); however, there was a great deal of variation within as well as between species. From our observations, it appeared that the female mites regardless of their species were unwilling to mate. Females struggled upon capture, and males had to overcome this resistance in order to manoeuvre their partners onto their backs. This appears to be similar to the matings of water strider Gerris odontogaster (Gerridae), where Arnqvist (1992) concluded that females showed a reluctance to enter copula because the act of mating was costly, not because their coyness allowed them to assess mate quality through male persistence. Jablonski and Vepsälainen (1995) predicted that in the presence of excess males, Gerris lacustris males should prolong mating and guarding, and females should show lower levels of resistance to prolonged mating in order to be protected from harassment by other males. Conversely, in the absence of other males, mate guarding should be lessened and female resistance should be higher. However, for water mites it is unclear whether mature individuals congregate in an area in order to find mates, and whether mites can sense the density of other mites around them. Arrenurus manubriator males do not change the amount of time attached to females when other males or females are nearby (H. Proctor, unpublished data). Ethological comparison of the four species The ethograms constructed for these four species indicate some behavioural similarities and differences within and among subgenera. Arrenurus (Megaluracarus) manubriator and A. (Truncaturus) rufopyriformis show similarities in the method of grabbing the female, depositing spermatophores, and separation. However, there are also behavioural differences, as is expected for species in different subgenera. For A. manubriator, pre-deposition courtship lasts for a longer proportion of the mating duration than postdeposition, while A. rufopyriformis makes a bigger investment in postdeposition behaviour (Table 2). In fact, the A. manubriator ratio of pre- to post-deposition courtship is also in contrast with the ratios of A. nr. reflexus and A. planus. This difference in emphasis may indicate that A. manubriator females need more persuasion to initially accept the male, while females of the other species need more post-deposition courtship to ensure that they use their partner’s sperm. Arrenurus sp. nr. reflexus and A. planus, while in the same subgenus (Arrenurus), were not very similar in mating behaviour or duration. The behavioural differences appear right at the start of mating; male A. planus do not use their fourth leg spurs to grab the female, but instead grab the female with all of their legs. These differences, many of which are probably due to the ventrally-

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directed orientation of the A. planus petiole, continue throughout the mating. A. nr. reflexus exhibits the more common mating position of the female glued onto the male’s back; the male then deposits spermatophores, collects sperm on the petiole, and then pushes the female back to insert the petiole into her genital opening. In contrast, A. planus does not deposit spermatophores at all. Instead, sperm is translocated by the leg action of both the male’s and female’s legs. The petiole appears to be inserted into the female, but is not used in the same manner as A. nr. reflexus. Sperm is not collected on its tip, as it is inserted into the female at the beginning of the mating. The petiole is probably used as a ramp to guide the placement of the sperm, or just to hold the female’s genital flaps open while sperm is pushed in. Another difference is the duration of the matings. For A. sp.nr. reflexus, the average duration was 19 540 ± 1179 seconds. In contrast, the mean duration of A. planus was only 5181 ± 1081 seconds. Periods of motionlessness occurred during the matings of all four species, though most frequently and for the longest periods in A. sp. nr. reflexus, resulting in this species having the longest mean mating duration. Long postcopulatory associations in animals are often assumed to be mate-guarding by males, i.e. he guards his paternity by preventing his female from mating with another male during her receptive period (Alcock 1994). But this passive phase may also be a form of courtship rather than mate guarding. Females that do not receive this courtship may exercise their choice by seeking additional males to mate with (Alcock 1994). This assumes that the sperm of the first male doesn’t have complete precedence. First-male precedence is widespread in the Acari, and is reflected in precopulatory guarding of virgin females (e.g. Tetranychidae, Cone 1985; Macrochelidae, Yasui 1988). Post-copulatory guarding and last-male precedence is much rarer; however, Radwan and Siva-Jothy (1996) have demonstrated that in Rhizoglyphus robini (Acaridae), a species in which individuals of both sexes may mate several times a day, a male increases his fertilisation of a clutch by prolonging his attachment to a female for up to six hours after copulation. Sperm-precedence patterns have not been determined for any water mite species. Without knowing how duration of post-copulatory association affects a male’s paternity, it is difficult to ascribe a rationale to the lengthy postcopulatory periods of Arrenurus sp. nr. reflexus, which spent more than 90% of all pairing time in this state.

REFERENCES Alcock, J. A. (1994). Postinsemination associations between males and females in insects: the mate-guarding hypothesis. Annual Review of Entomology 39, 1–21. Alexander, R. D., Marshall, D. C., and Cooley, J. R. (1998). Evolutionary perspectives on insect mating. In ‘The Evolution of Mating Systems in Insects and Arachnids’. (Eds J. C. Choe and B. J. Crespi.) pp. 4–31. (Cambridge University Press: Cambridge.) Andersson, M. (1994). ‘Sexual Selection.’ (Princeton University Press: Princeton.) Arnqvist, G. (1992). Pre-copulatory fighting in a water strider – intersexual conflict or mate assessment? Animal Behaviour 43, 559–567. Arnqvist, G., and Rowe, L. (1995). Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proceedings of the Royal Society of London, Series B 261, 123–127.

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Basolo, A. L. (1990). Female preference predates the evolution of the sword in swordtail fish. Science 250, 808–809. Brooks, D. R., and McLennan, D. A. (1991). ‘Phylogeny, Ecology, and Behavior.’ (University of Chicago Press: Chicago.) Choe, J. C. (1998). The evolution of mating systems in the Zoraptera: mating variations and sexual conflicts. In ‘The Evolution of Mating Systems in Insects and Arachnids’. (Eds J. C. Choe and B. J. Crespi.) pp. 130–145. (Cambridge University Press: Cambridge.) Christy, J. A. (1995). Mimicry, mate choice, and the sensory trap hypothesis. The American Naturalist 146, 171–181. Clutton-Brock, T. H., and Vincent, A. C. J. (1991). Sexual selection and the potential reproductive rates of males and females. Nature 351, 58–60. Cone, W. W. (1985). Mating and chemical communication. In ‘Spider Mites: Their Biology, Natural Enemies and Control.’ (Eds W. Helle and M. W. Sabelis) pp. 243–251 (Elsevier, Amsterdam.) Darwin, C. (1871). ‘The Descent of Man and Selection in Relation to Sex.’ (John Murray: London.) Eberhard, W. G. (1998). Sexual selection by cryptic female choice in insects and arachnids. In ‘The Evolution of Mating Systems in Insects and Arachnids’. (Eds J. C. Choe and B. J. Crespi.) pp. 32–57. (Cambridge University Press: Cambridge.) Endler, J. A. (1992). Signals, signal conditions, and the direction of evolution. The American Naturalist 139 (Supplement), S125–S153. Fowler, K., and Partridge, L. (1989). A cost of mating in female fruitflies. Nature 338, 760–761. Gwynne, D. T., and Simmons, L. W. (1990). Experimental reversal of courtship roles in an insect. Nature 346, 172–174. Hamilton, W. D., and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387. Holland, B., and Rice, W. R.. (1998). Perspective: chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52, 1–7. Jablonski, P., and Vepsälainen, K. (1995). Conflict between sexes in the water strider Gerris lacustris: a test of two hypotheses for male guarding behaviour. Behavioural Ecology 6, 388–392. Maynard Smith, J. (1987). Sexual selection – a classification of models. In ‘Sexual Selection: Testing the Alternatives’. (Eds J. W. Bradbury and M. B. Andersson.) pp. 9–20. (John Wiley & Sons: New York.) McClintock, W. J., and Uetz, G. W. (1996). Female choice and pre-existing bias: visual cues during courtship in two Schizocosa wolf spiders (Araneae: Lycosidae). Animal Behaviour 52, 167–181. Mitter, C., Farrell, B., and Futuyma, D. J. (1991). Phylogenetic studies of insect-plant interactions: insights into the genesis of diversity. Trends in Ecology and Evolution 6, 290–293. Møller, A. P. (1992). Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters. Journal of Evolutionary Biology 5, 691–699. Parker, G. A., and Partridge, L. (1998). Sexual conflict and speciation. Philosophical Transactions of the Royal Society of London, Series B 353, 261–274. Pellmyr, O. (1992). Evolution of insect pollination and angiosperm diversification. Trends in Ecology and Evolution 7, 46–49. Proctor, H. C. (1991). Courtship in the water mite Neumania papillator: males capitalize on female adaptations for predation. Animal Behaviour 42, 589–598. Proctor, H. C. (1992a). Sensory exploitation and the evolution of male mating behaviour: a cladistic test using water mites (Acari: Parasitengona). Animal Behaviour 44, 745–752. Proctor, H. C. (1992b). Mating and spermatophore morphology of water mites (Acari: Parasitengona). Zoological Journal of the Linnean Society 106, 341–384. Proctor, H. C., and Smith, B. P. (1994). Mating behaviour of the water mite Arrenurus manubriator (Acari: Arrenuridae). Journal of Zoology, London 232, 473–483.

COERCION AND DECEIT: WATER MITES (ACARI: HYDRACARINA) AND THE STUDY OF INTERSEXUAL CONFLICT

Radwan, J., and Siva-Jothy, M. T. (1996). The function of post-insemination mate association in the bulb mite, Rhizoglyphus robini. Animal Behaviour 52, 651–657. Rice, W. R. (1996). Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381, 232–234. Ryan, J. J., Fox, J. H., Wilczynski, J. H., and Rand, A. A. (1990). Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343, 66–67. Ryan, M.M., and Rand, A.S. (1993). Sexual selection and signal evolution: the ghosts of biases past. Philosophical Transactions of the Royal Society of London, Series B 340, 187–195. Shaw, K. (1995). Phylogenetic tests of the sensory exploitation model of sexual selection. Trends in Ecology and Evolution 10, 117–120.

Shelley, T. E., and Whittier, T. S. (1997). Lek behavior of insects. In ‘The Evolution of Mating Systems in Insects and Arachnids’. (Eds J. C. Choe and B. J. Crespi.) pp. 273–293. (Cambridge University Press: Cambridge.) Trivers, R. L. (1972). Parental investment and sexual selection. In ‘Sexual Selection and the Descent of Man.’ (Ed B. Campbell.) pp. 136–179. (Adline: Chicago.) Viets, K. O. (1975). Neue Wassermilben (Acari, Hydrachnellae) aus Australien. Zoologica Scripta 4, 93–100. West-Eberhard, M. (1984). Sexual selection, competitive communication and species-specific signals in insects. In ‘Insect Communication.’ (Ed T. Lewis.) pp. 283–324. (Academic Press: Toronto.) Yasui, Y. (1988). Sperm competition of Macrocheles muscaedomesticae (Scopoli) (Acarina: Mesostigmata: Macrochelidae), with special ref-

Appendix 1 List of characters and character states. Characters 1–28 are from Proctor (1992a); characters 29 and 30 have been added for this analysis. Character Number

Character Description

1.

Clutch morphology:

2.

Egg shape:

0 = round; 1 = oval

3.

Chelicera shape:

0 = with tooth; 1 = without tooth

4.

Flap over anal pore:

0 = absent; 1 = present

5.

Apodemes on tips of coxa III:

0 = absent; 1 = present

6.

Apodemes on medial sides of coxa III:

0 = absent; 1 = present

7.

Transverse muscle attachment scar on coxa III:

0 = absent; 1 = present

8.

Location of pore in anal plate relative to anal setae:

0 = not closer to top than to bottom setae; 1 = closer to top than to bottom setae

9.

Tarsal empodium:

0 = not bifurcate; 1 = bifurcate

10.

Number of pairs of genital acetabula:

Character States

Egg & larval characters 0 = membranous egg capsule; 1 = no capsule

Deutonymphal characters 0 = two pairs; 1 = more than two pairs

Adult characters 11.

Chelicerae fused medially:

0 = no; 1 = yes

12.

Apodemes of coxae I:

0 = not extending beyond coxae III; 1 = extending into coxae IV

13.

Female genital spines:

0 = absent; 1 = present

14.

Jointed, tubercled spines on legs I:

0 = absent; 1 = present

15.

Long tubercles on medial side of palp tibia:

0 = absent; 1 = present

16.

Thickened, blade-like setae on medial and lateral sides of palp genu:

0 = absent; 1 = present

17.

Integument of idiosoma:

0 = membranous; 1 = entirely sclerotised

18.

Shape of lower margin of coxa IV:

0 = smooth; 1 = with sharp hook

19.

Incorporation of gladularium and seta in inner margin of coxa IV:

0 = absent; 1 = present

20.

Peg-like seta located distoventrally or distolaterally on palp tibia:

0 = absent; 1 = present

21.

Enlarged glandularia flanking acetabular plates:

0 = absent; 1 = present

22.

Glandularium and seta within each acetablular plate:

0 = no; 1 = yes

23.

Spermatophore stalk structure:

0 = solid; 1 = chambered

24.

Webbing on stalk:

0 = absent; 1 = present

25.

Sperm capsule:

0 = absent; 1 = present

26.

Spermatophores bound together in integrated groups:

0 = no; 1 = yes

27.

Male fans over spermatophores:

0 = no; 1 = yes

28.

Spermatophore deposition site:

0 = substrate; 1 = male’s own legs

29.

Highly pectinate seta at distal end of tibia of LIII (at least in females):

0 = absent: 1 = present

30.

Location of eye capsules:

0 = external; 1 = internal

169

ACAROLOGY

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

....................................................................................................

erence to precopulatory mate guarding behavior. Journal of Ethology 6, 83–90.

.................................................................................................................................................................................................................................................................

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THELYTOKOUS

THELYTOKOUS REPRODUCTION IN THE FAMILY ACARIDAE (ASTIGMATA) Kimiko Okabe1 and Barry M. OConnor2

REPRODUCTION IN THE FAMILY

ACARIDAE (ASTIGMATA)

1

Kyushu Research Centre, Forestry and Forest Products Research Institute, 4-11-16 Kurokami, Kumamoto 860–0862, Japan 2 University of Michigan, Museum of Zoology, Ann Arbor, Michigan, 48109–1079, USA

Abstract

Parthenogenesis in the family Acaridae was examined through literature records and laboratory cultures of several species. Live specimens of parthenogenetic species of Schwiebea and Thyreophagus were collected in Japan, and Sancassania and Acotyledon formosani from Japan were documented as parthenogenetic. The type of parthenogenesis was thelytoky in all species. We hypothesise that parthenogenesis evolved in these genera independently. Experiments compared life-history traits for two pairs of sexual and asexual species of Schwiebea (similis-group and lebruni-group). Asexual species exhibited either higher fecundity or faster development than their sexual relatives, but not both. It was hypothesised that related sexual and asexual species can coexist because they segregate their habitats and niche in the field. The asexual species conform to theory in inhabiting aquatic situations. The asexual S. elongata was assumed to have speciated relatively recently because potential habitats often overlapped with those of its sexual relative, and the male was retained. On the other hand, the lebruni-type mites seemed to represent a longer separate history because they are morphologically more distinct and occupied different types of substrates.

INTRODUCTION Among astigmatid mites, parthenogenesis has been documented in only a few species in the families Histiostomatidae (Hughes and Jackson 1958), Winterschmidtiidae (Nesbitt 1946; Dosse and Schneider 1957; Gonzalez 1961), and Acaridae (Philipsen and Coppel 1977). Arrhenotoky has been demonstrated in the Histiostomatidae, while thelytoky occurs sporadically in all these families. Parthenogenesis has also been suspected in the Suidasiidae and in some other Acaridae because many species in these families have been collected only as females (Norton et al. 1993). In particular, the speciose family Acaridae contains many species known only from females, notably in the large genus Schwiebea. We have recently been investigating the systematics and ecology of acarid mites in Japan. Those species which have been demonstrated or suspected to be parthenogenetic are listed in Table 1, along with their habitats. Among these, the genus Schwiebea is best represented among parthenogenetic species. In our observations, all parthenogenetic Schwiebea species reproduced without mating. Although this suggests a thelytokous sexual mode, we observed small numbers of males in some populations. At this point, we regard the species as thelytokous because we were not able to demonstrate deuterotoky through documentation of male sexual function and sex-ratio in field populations. Norton et al. (1993) summarised current theory on the distribution of thelytoky in mites, indicating that thelytoky should not appear randomly in clades, but should be clustered in taxa that share biological attributes that predispose them to thelytoky. Norton and Palmer (1991) mentioned that egg size should be smaller, egg numbers smaller and developmental period longer in thelytokes than in related sexual species. Walter and Lindquest (1995) tested several of those hypotheses with field experiments and also from literature involving mesostigmatid mites. However, no experimental data on astigmatid mites has been published to test these hypotheses. In this paper we provide experimental tests of the hypothesis that sexual species should have higher fecundity than coexisting asexual relatives, for several species of Schwiebea mites collected in Japan. We compare habitats (collection sites), female body size, which may contribute to egg storage capacity, developmental

period, sex ratio, egg mortality (egg viability) and number of eggs produced per female, all of which may directly or indirectly affect each species’ fecundity.

MATERIALS AND METHODS We chose the genus Schwiebea for our experiments because we have demonstrated parthenogenesis in several species through laboratory rearing, and related sexual species were available for comparison. Schwiebea similis Manson originated from soil in an agricultural field in Okayama Prefecture. Schwiebea elongata (Banks) was collected from indoor swimming pool water in Ibaraki Prefecture, S. lebruni Fain from pine forest litter on Mt. Azuma, Fukushima Prefecture and an undescribed species similar to S. lebruni from marsh moss also on Mt. Azuma. For our comparisons, we grouped the four species in two pairs, each pair composed of morphologically similar, and likely phylogenetically related, sexual and asexual species. One pair included S. similis (Fig.1 A-a) (sexual) and S. elongata (Fig.1 A-b) (asexual), having an almost identical external morphology but differing slightly in spermathecal morphology. The other included the morphologically similar pair S. lebruni (Fig. 1 B-a, sexual) and the undescribed species near lebruni (called lebruni-like hereafter) (Fig.1 B-b, asexual). The size of the female idiosoma and the setal lengths were obtained from the average values of ten individuals in each species. Although very similar morphologically, we observed Schwiebea similis to be reproductively isolated from S. elongata. We regard the lebruni-like mite as a species different from S. lebruni based on distinctive morphological differences between the females: the idiosoma of S. lebruni is consistently larger, the propodosomal sclerite of S. lebruni has a cleft but the other does not, and seta l''G on genu I is filiform in lebruni but spine-like in the other species. We reared the mites in Petri dishes with the fungus Flammulina velutipes (Agaricales, Tricholomataceae, stock culture KRCM377) cultivated on PDA (potato dextrose agar, Nissui Co. Ltd.) for numerous generations before the experiments. To collect eggs for determining developmental period, about 30 females (with several males for sexual species) were isolated in a Petri dish with the fungus on PDA at 25°C, and eggs were collected every 12 h. Each egg was

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Kimiko Okabe et al.

transferred to a small glass ring containing the mycelium, following the individual rearing method of Okabe (1993). We assumed that all eggs were laid at the time we collected them and adjusted the developmental period. Glass rings with mites were maintained at 25°C and mite development was checked every 12 h under a stereomicroscope. Total developmental period was measured as the time between egg deposition and eclosion. Initially, 60 eggs of the similis-type pair and 40 eggs of the lebruni-type pair were isolated, but some were lost during the experiments. The sex of each reared adult was determined at the end of the developmental period experiment. For S. elongata, we eventually reared more than 50 eggs to obtain a sex ratio. The egg mortality of each species was also obtained from this experiment (S. similis and the lebruni-type mites) or from another similar experiment (S. elongata). We used the same individual rearing method (Okabe, 1993) at the same temperature to determine the number of eggs laid per female. Thelytokous females were reared individually in rings. For the sexual species, we supplied a male for each female. As a result, each female had the opportunity to mate with several males by the end of the experiment. The egg numbers were checked and eggs removed every day under a stereomicroscope. Each pair in sexual species or each female in asexual species was transferred to fresh mycelium when the environment deteriorated, approximately every 3 or 4 days. We also tested survivorship, which was calculated using the formula of the average egg numbers laid per female times the egg survival rate [(1 – the egg mortality) × 100] with a Kolmogorov-Smirnov Test.

RESULTS Parthenogenetic and sexual species listed in Table 1 did not always conform to the theory of where they should live. Several of these species are typical of astigmatid mites in inhabiting patchy habitats associated with insects. Coptotermes formosanus, the host of Acotyledon formosani, is a common subterranean termite in warm areas of Honshu, Shikoku and Kyushu in Japan. The Sancassania species reported here was collected as deutonymphs from the scarab beetle, Heptophylla picea and one of them established a population (K. Kurosa, personal communication). The larva of the beetle inhabits the soil, feeding on plant roots, and the adult feeds on leaves. The mite may naturally feed on dead larvae or adult beetles as do other related species of Sancassania (OConnor, personal observation). The Schwiebea species were more similar in their habitats to thelytokus oribatid mites in that they were collected from disturbed soils or aquatic or semiaquatic situations, although the natural habitat of S. elongata in Japan is unclear. In our experiments with Schwiebea, there was no clear relationship between the size of the female idiosoma and sexual mode (Fig. 1). The sexual S. similis was smaller than asexual S. elongata while the sexual S. lebruni was larger than the asexual lebruni-like mite. There was also no correlation between female body size and the egg numbers laid. Spermathecal morphology was slightly different within a group. Schwiebea similis had parachute-shaped cells in the spermatheca (Manson 1972) while S. elongata had more even cells apparent in the spermathecal wall. On the other hand, S. lebruni had a slightly thicker wall in the basal part of the spermatheca below the balloon-like sac at the end of the sper-

172

matheca (Fain 1977) than in the lebruni-like mite. Overall, there were more apparent morphological differences between the two lebruni-type species than were observed between the similis-type species. However, it was not clear that any of morphological characters affected sexual modes. Developmental periods were not very different within a group, although S. similis had a slightly longer developmental time than S. elongata (Table 2). Egg numbers tended to be smaller in the sexual species. There was no significant difference in egg viability between the mites within each group.

DISCUSSION In the Acaridae, species in several genera have been documented or hypothesised (Norton et al. 1993) to be parthenogenetic. In Japanese acarid species, parthenogenesis seemed to cluster in Schwiebea (Table 1). However, the amount of available information is small, and more information on many more taxa will be necessary before the hypothesis of phylogenetic clustering of thelytoky can be tested in this group. Some oribatid groups, such as Trhypochthoniidae (considered to be related to the Astigmata by Norton et al. 1993), exhibit only parthenogenetic reproduction (summarised in Norton et al. 1993). Although it is clear that the Acaridae is clearly not such a family, there are not enough data to estimate the extent of parthenogenesis in this large group. Many authors have hypothesised that parthenogenetic species might specialise in certain niches: fresh water rather than marine, aquatic rather than terrestrial, higher altitude and latitude, disturbed habitats rather than stable and smaller islands or archipelagos rather than continental (Bell 1982; Maynard Smith 1978; Norton et al. 1993). Some Japanese species in Table 1 conform to these suggestions but others do not. ‘Acotyledon’ formosani presumably inhabits the soil together with its termite hosts. The Sancassania mite in Table 1 was also suspected of inhabiting soil, the larval habitat of its phoretic host. Both of these species are probably closely associated with their host insects as food sources. There was little information available for the wasp host of the thelytokous Thyreophagus mite, which was confirmed to be parthenogenetic by rearing. The mite was suspected to be associated with the wasp, which nested in a bamboo shoot or with lepidopteran prey of the wasp. The other acarid species associated with insects in numbers were not always documented parthenogenetic. Additionally, it is not likely that the hosts of the three live an aquatic or high altitude or latitude habitats, but they likely inhabit disturbed areas. Though biological data were lacking in most species, these three species did not match the theory of niches for parthenogens. As for the three species of Schwiebea confirmed asexual by means of the rearing experiments, all conform to the theory. So far, all acarid mites collected in indoor swimming pools are asexual (Tagami and Okabe, unpublished). This suggests that the aquatic niche or a similar wet habitat is favored by these asexual species. Other Schwiebea species collected from aquatic or subaquatic habitats are suspected of being asexual, as males are rare or unknown. Schwiebea araujoae, morphologically similar to Schwiebea sp. 1 was collected from a swimming pool (Fain 1977) and also from soil (Ho 1993). Schwiebea aquatilis was collected from subterranean springs (Fain 1982), S. codognoensis from an aque-

THELYTOKOUS

A-a

REPRODUCTION IN THE FAMILY

ACARIDAE (ASTIGMATA)

A-b

100 m

B-a Figure 1

Table 1

B-b

Female dorsal idiosoma with spermatheca of four Schwiebea mites. A: the similis-group of mites. A-a is S. similis (sexual species) and A-b is S. elongata (asexual species). B: the lebruni-group of mites. B-a is S. lebruni (sexual) and B-b lebruni-like (asexual). The 100 µm scale is for all mites.

Collections of Japanese thelytokous acarid mites.

Species

Collection site

Stage collected

Source

termite nest (Coptotermes formosanus): Wakayama Pref.

feeding stages and deutonymphs

Phillipsen and Coppel (1977)

Sancassania sp.

scarabeid beetle body (Heptophylla picea): Saitama Pref.

deutonymphs

Kurosa (pers. comm.)

Schwiebea sp. 1

indoor swimming pools, agricultural field soil: Tokyo, Gunma Pref.

feeding stages

Tagami and Okabe (unpublished)

Schwiebea sp. 2

marsh at high altitude: Aomori Pref.

feeding stages

Okabe (unpublished)

‘Acotyledon’ formosani

A

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Kimiko Okabe et al. Table 1

Collections of Japanese thelytokous acarid mites.

Species

Collection site

Stage collected

Source

Schwiebea elongata

indoor swimming pools: Ibaraki Pref.; agricultural field soil: Kochi Pref.; under bark weevil’s galler (Sipalinus gigas): Oita Pref.

feeding stages

Tagami, Okabe and OConnor (unpublished)

Schwiebea ‘lebruni-like’

marsh moss at high altitude: Fukushima Pref.

feeding stages

in this paper

Thyreophagus sp.

wasp’s nest (unknown species): Kumamoto Pref.

feeding stages

Okabe and Makino (unpublished)

A

This species actually represents an unnamed genus, which is currently being described by the authors.

duct (Fain and Pagani 1989), S. estradai, morphologically close to Schwiebea sp. 2 from salmon gills in a hatchery (Fain and Ferrando 1990), and S. kurilensis from a marshy area (Bugrov 1995). There are, however, some species also described only from females which were not collected from aquatic conditions. Many Schwiebea species have been collected from soil (Woodring 1966; OConnor 1982, 1994), which may periodically become saturated, especially if the soil is clay rather than sand. Because most species of Schwiebea have not been examined for their sexual modes, we cannot conclude that they are thelytokous even when they are described only from females. The female body size may restrict the number of eggs the mite can mature at one time and result in a competitive disadvantage. In this sense, a sexual mite should have a larger body than an asexual relative to be advantageous in survival. In our experiments, there was no consistent relationship betweem sexual modes and female size (Fig. 1). The difference represented in the figure, however, did not affect the number of eggs laid per female (Table 1) for either group. The developmental period of S. similis was a little longer than that of S. elongata. Schwiebea elongata could outcompete S. similis if they were reared in the same Petri dish together. This does not explain how both sexual and asexual species can coexist in nature. However, all-female species of Lasioseius (Mesostigmata: Ascidae) Table 2

are not always reproductively inferior but are sometimes competitively superior to their sexual relatives (Walter and Lindquist 1995). We hypothesise that mites in our laboratory colonies exhibit the observed fecundity when food is not limited and the environment is free from natural enemies. Under such competitive conditions, an asexual species might be expected to extirpate a sexual species. In nature, however, both sexual and asexual mites exist and segregate their habitats to some extent. Schwiebea mites are fungivorous (OConnor 1982) and are presumably generalists based on our rearing experiments (Okabe and OConnor, unpublished). We presume that natural enemies, including diseases, and/or environmental changes such as climate, control this and other life-history parameters. In the field, the habitats of the similis-type mites overlapped (but were not actually shared) with the collection materials of soil in Japan (Table 1) because of their relative closeness. We suspect that at least in wet soil, S. elongata could be able to take over the niche of S. similis. On the other hand, the lebruni-type mites showed less overlap than the similistype since both were collected in distinct habitat types isolated from each other (marsh and forest litter), albeit in the same mountain region. One of the reasons for this apparent difference between these two groups of species could be that lebruni-type species speciated much earlier, as evidenced by the several morphological differences between them. Although our collection records of these mites were too few to be confident, the mites may

Developmental period and fecundity of each mite in the two species-groups. similis-type spp.

Developmental period A Female ratio (%) Egg numberA Egg mortalityB (%)

lebruni-type spp.

S. similis

S. elongata

S. lebruni

lebruni-like sp.

10.53 ± 1.41* (43)

9.59 ± 1.6 (50)

18.90 ± 1.88 (20)

19.37 ± 1.46 (30)

80

99.7

60

100

97.85 ± 81.6 (20)

137.6 ± 57.2 (20)

23.38 ± 12.7* (16)

41.4 ± 27.6 (16)

6

14

13

21

A

Developmental period and Average Egg No. laid per female expressed as mean ± SD, with the number of samples in parentheses. B The mortality was averaged from the unhatched egg numbers and all eggs laid per female (20 females were used). The developmental period and the average egg number were analyzed within a group by Kolmogorov-Smirnov Test, respectively. * indicates that the mean for a sexual species was significantly different from that for the asexual species within a group (p 40 µm; dorsal plate with a foveal row

186

pattern of 1-5-2-4-2-2-2 including the main characteristic of the presence of only one pair of bilobed, rounded or subtriangular anterolateral foveae (Figs. 1–4). Regarding the latter point, P. grandisoma shows small differences in the foveal row pattern, as a displacement of two foveae in the second row and a subdivided sixth row. Nevertheless it maintains the primary formula of 1-5 (2-3)-2-4-2-2/2-2 (Fig. 5). A diagonal curved ridge on the posterolateral area of coxa I of males is present throughout the lineage (Figs. 14–18). It is noteworthy that all bat associations of the acutisternus-clade reflect an evolutionary group, because these mites are parasites mainly of bats of the subfamilies Phyllostominae and Macrotinae, and only one species (P. ramirezi) is found in the tribe Stenodermatini (Fig. 37). This last mite species could be the link with the other Periglischrus clade. The acutisternus-clade species can be divided into four species groups and an additional independent species, based on their morphological similarities and evolutionary affinities with their bat hosts. These are discussed below. The acutisternus species group. This group includes five species: Periglischrus acutisternus, P. paracutisternus, P. dusbabeki, P. tonatii, and the new species Periglischrus sp. B. Females of all of these have a sclerotised median anterior projection at the anterior end of the sternal plate, which may be subtriangular or elongated in shape (Figs. 6–7), and the anterolateral corners of the sternogenital plate are weakly marked and with long sternogenital setae (Fig. 14). Each species of the acutisternus group is associated with a phyllostomine bat: Phyllostomus elongatus, Trachops cirrhosus, Mimon crenulatum, Tonatia silvicola, and Tonatia evotis, respectively. The gameroi species group. Three species belong to this group: Periglischrus gameroi, P. micronycteridis, and P. parvus. All have a similar outline of the sternal plate (Herrin and Tipton 1975), with its anterior margin having a subtriangular border without projection (Fig. 8), and the sternogenital plate somewhat pear-shaped with medium length setae (Fig. 15). The three species of the gameroi group were found mainly on the phyllostomine bats Lonchorhina aurita, Micronycteris megalotis, and M. nicefori, respectively. The torrealbai species group. This group is composed of Periglischrus torrealbai, P. paratorrealbai, and the new species Periglischrus sp. A. According to Herrin and Tipton (1975), all the species in this group have a similar broad pear-shaped sternal plate with a somewhat narrow or broadly rounded anterior border. While some ventral hysterosomal setae are grossly enlarged (Figs. 9–10), the proteronotal and poststigmal setae are very small in females (6–22) and males (13–26), and the sternogenital plate has rounded lateral borders (Fig. 16). The torrealbai species group was found associated with the phyllostomine bats Phyllostomus hastatus, Tonatia bidens, and Phylloderma stenops. The delfinadoae species group. Only Periglischrus delfinadoae and P. ramirezi belong to this group. These species have few morphological similarities, and the main reason for including them in the same group is that females of both species have a small sternal plate with a nearly rounded outline (Fig. 11). Also, the sternogenital plate has slightly rounded anterolateral borders (Fig. 17). However, each species is associated with a different bat group, with P. delfinadoae

NEW MORPHOLOGICAL

Figures 1–9

ANALYSIS OF THE BAT WING MITES OF THE GENUS

PERIGLISCHRUS

Morphological features of the acutisternus – clade of the bat associated mite genus Periglischrus. (1–5) Female dorsal plates. (1) P. tonatii. (2) P. gameroi (arrow: 1 anterolateral fovea). (3) Periglischrus sp. A. (4) P. delfinadoae. (5) P. grandisoma. (6–9) Sternal plates. (6) P. acutisternus. (7) P. dusbabeki. (8) P. gameroi. (9) P. torrealbai.

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Figures 10–18

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Morphological features of the acutisternus – clade of the bat associated mite genus Periglischrus. (10) Periglischrus sp. A, sternal plate, genital plate and some ventral opisthosomal setae. (11–12) Sternal plates. (11) P. delfinadoae. (12) P. grandisoma. (13) P. grandisoma, female coxae II-IV. (14–18) Male ventral idiosoma and sternogenital plates. (14) P. tonatii (arrow: 1 diagonal curved ridge on coxa I). (15) P. gameroi. (16) Periglischrus sp. A. (17) P. delfinadoae. (18) P. grandisoma.

NEW MORPHOLOGICAL

Figures 19–27

ANALYSIS OF THE BAT WING MITES OF THE GENUS

PERIGLISCHRUS

Morphological features of the caligus – clade of the bat associated mite genus Periglischrus. (19-24) Female dorsal plates. (19) P. caligus (arrows: 2 anterolateral foveae). (20) P. vargasi. (21) P. hopkinsi. (22) P. iheringi. (23) P. ojastii. (24) P. cubanus. (25–27) Sternal plates. (25) P. caligus. (26) P. vargasi. (27) P. herrerai.

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Figures 28–33

Morphological features of the caligus – clade of the bat associated mite genus Periglischrus. (28–29) Sternal plates. (28) P. iheringi. (29) P. cubanus. (30–33) Male ventral idiosoma and sternogenital plates. (30) P. caligus. (31) P. paracaligus. (32) P. herrerai. (33) P. iheringi.

Figures 34–36

Mesoperiglischrus natali. (34) Female dorsal prosoma and dorsal plate. (35) Sternal plate. (36) Male ventral idiosoma and sternogenital plate.

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NEW MORPHOLOGICAL

found on a macrotine bat, Macrotus waterhousii, and P. ramirezi on a Stenodermatini bat, Rhinophylla pumilio. The last species in the acutisternus-clade to be considered is Periglischrus grandisoma. Originally Herrin and Tipton (1975) placed this species into a subgroup with P. paracutisternus, P. acutisternus, and P. dusbabeki, because the female sternal plate of P. grandisoma has an acute projection on the anterior border (Fig. 12), but P. grandisoma is considerably different from the other three species. Its long idiosomal length is unique in the genus, as is its dorsal plate with celled and rounded foveae and its foveal row pattern of 1-5(2-3)-2-4-2-2/2-2. The anteromedial unpaired fovea is slightly enlarged and T-shaped (Fig. 5), coxa I has a diagonal coxal ridge, and coxae II-IV have a 2- or 3-curved ridge on each coxa (Fig. 13). The male also has a long idiosoma, a strong ridge on coxa I, and a very large sternogenital plate (Fig. 18). It is noted that this species may be found with P. paratorrealbai (a member of the torrealbai group) on Phylloderma stenops (Herrin and Tipton 1975) but, because of morphological differences, it is possible that P. grandisoma evolved from a different lineage than that of the torrealbai group. However, P. grandisoma appears to have a real affinity to the acutisternus-clade in that the primary characters of the lineage (one pair of anterolateral foveae and one diagonal curved ridge on coxa I of males) are present. The caligus-clade

Eleven species are included in the caligus-clade: Periglischrus caligus Kolenati, 1857, Periglischrus sp. C, P. vargasi Hoffmann, 1944, P. paracaligus Herrin and Tipton, 1975, Periglischrus sp. D, P. paravargasi Herrin and Tipton, 1975, P. hopkinsi MachadoAllison, 1965, P. herrerai Machado-Allison, 1965, P. iheringi Oudemans, 1902, P. ojastii Machado-Allison, 1964, and P. cubanus Dusbábek, 1968. All have the following morphological features: dorsal idiosoma with Pn1-Pn5 > 40 µm (except for some setae of P. ojastii in which Pn1-Pn5 have range 29–49 µm, and in P. iheringi in which only setae Pn1 are very small, 8–10); a foveae row pattern of 1-7-2-4-2-2-2 on the dorsal plate, including the presence of two pairs of separated, elongated or rounded, anterolateral foveae (Figs. 19–24); and the absence of a diagonal curved ridge on coxa I of males (Figs. 30–33). The caligus-clade is associated mainly with bats of the tribe Glossophagini, but also with two species of Stenodermatini and one species of the subfamily Desmodontinae (Fig. 37). The association of this clade with these groups of bats therefore reflects another evolutionary trend in Periglischrus. The caligus-clade species can be divided into four species groups and an additional independent species, based on their morphological similarities and evolutionary affinities with their bat hosts. These are discussed below. The caligus species group. Only two species belong to this group, Periglischrus caligus and the new species Periglischrus sp. C. Both species have a dorsal plate with a similar dark foveae pattern (Fig. 19), and a sternal plate with a subpentagonal outline and a pointed anterior border (Fig. 25). The males of both species have a small sternogenital plate with weakly sclerotised anterolateral borders and small sternogenital setae (Fig. 30).

ANALYSIS OF THE BAT WING MITES OF THE GENUS

PERIGLISCHRUS

Previous species groupings made by Herrin and Tipton (1975) showed P. caligus as closely related to P. vargasi, P. paravargasi and other related species, but the morphological evidence indicates that the caligus group is distinct from the vargasi group. Furthermore, the host genera of the caligus group, Glossophaga and Choeronycteris (Glossophagini), while closely related to each other, are distinct from the host genera of the vargasi group. The vargasi species group. This species group comprises four species, Periglischrus vargasi, P. paravargasi, P. paracaligus, and the new species Periglischrus sp. D. Their foveae row pattern is similar to that of the caligus group, but with less distinct celled foveae. The main characteristic of the vargasi group is a unique scale-like interfoveal ornamentation pattern on the female dorsal plate (Fig. 20), along with long proteronotal setae (62-124), and a subpentagonal sternal plate with anterior subtriangular border (Fig. 26). The sternogenital plate has medium sized setae and is well sclerotised, although in some species unsclerotised anterolateral corners may be present (Fig. 31). The vargasi group parasitises four bat species that belong to two related Glossophagini genera, Leptonycteris and Anoura. The hopkinsi species group. Only two species are included in this group, Periglischrus hopkinsi and P. herrerai. The sternal plate of females is similar in its subpentagonal outline with a subtriangular anterior margin (Fig. 27). Furthermore, the female and male dorsal plate of P. hopkinsi has an unsclerotised crack with a crossshaped form (Fig. 21), while in P. herrerai, a smaller cross-shaped crack was observed only in the male. This feature could reflect some morphological similarities of the two species. However, it is well known that P. herrerai is morphologically distinct from other species in the genus, because its males have a reticulated sternogenital plate that is unique (Fig. 32), and because it is associated with bats of the genus Desmodus, which have an uncertain phylogenetic position in the family Phyllostomidae, whereas P. hopkinsi is associated with a Glossophagini bat, Lionycteris spurelli. The iheringi species group. This group comprises only two species, Periglischrus iheringi and P. ojastii. Females in this group share pronounced shoulders on the anterolateral outline of the dorsal plate (Figs. 22–23), and similar outlines of the sternal (Fig. 28) and sternogenital plates (Fig. 33) (Herrin and Tipton 1975). However, females differ in the foveae pattern, particularly P. iheringi, which shows a unique foveae pattern. The small central pair of foveae are associated with a longitudinal medial keel, the end of which is joined with the anterocentral unpaired fovea, such that it looks like an arrow (Fig. 22). Both species of the iheringi group are parasites of two related Sternodermatini bat genera: P. iheringi on Artibeus and P. ojastii on Sturnira. The last species in the caligus-clade is Periglischrus cubanus. This species has two pairs of anterolateral foveae, which are divided on their posterior margin but joined on their anterior border (Fig. 24, top right of figure), and with a polygonal sternal plate with trapezoid anterior border (Fig. 29). This species is a parasite of an endemic bat, Phyllonycteris poeyi from Antilles, and this unusual morphology may reflect its isolation from the continental species of the genus.

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MITE PARASITES

Tonatia silvicola

P. sp. B

Tonatia evotis

P. paracutisternus

Trachops cirrhosus

P. acutisternus

Phyllostomus elongatus

P. dusbabeki

Mimon crenulatum

P. gameroi

Lonchorhina aurita

P. micronycteridis

Micronycteris megalotis

P. parvus

Micronycteris nicefori

P. torrealbai

Phyllostomus hastatus

P. sp. A

Tonatia bidens

P. paratorrealbai

Phylloderma stenops

P. grandisoma

Phylloderma stenops

P. delfinadoae

Macrotus waterhousii

P. ramirezi

Rhinophylla pumilio

P. ojastii

Sturnira spp.

P. iheringi

Artibeus spp.

P. herrerai

Desmodus rotundus

caligus

P. hopkinsi

Lionycteris spurrelli

clade

P. cubanus

Phyllonycteris poeyi

P. paravargasi

Anoura caudifer

P. vargasi

Anoura geoffroyi

P. sp. D

Leptonycteris nivalis

P. paracaligus

Leptonycteris curasoae

P. sp. C

Choeronycteris mexicana

P. caligus

Glossophaga soricina

acutisternus clade

Figure 37

P. tonatii

Phyllostominae

Macrotinae.......... (?)

Stenodermatini

Desmodontinae.. (?)

Glossophagini

Proposed grouping of the Periglischrus clades, related to their host bat phylogeny (based on Baker et al. 1989). The relationships between Phyllostominae, Stenodermatini and Glossophagini are relatively well established by Baker et al. (1989), and agree with the morphological groupings of their associated Periglischrus mites. The relationships between Macrotinae and Desmodontinae proposed by Baker et al. (1989) are not in accordance with the morphological groups of their associated mites and have been marked with question marks in the cladogram.

The validity of Mesoperiglischrus, and the position of Periglischrus natali

Originally Furman (1966) described the species Periglischrus natali as a member of the genus Periglischrus. However, when describing a new genus and species, Mesoperiglischrus nyctiellinus, Dusbábek (1968) considered Periglischrus natali to be a congener, and recombined the name to Mesoperiglischrus natali. The distribution of new morphological characters supports this conclusion. These characters are: short pectinate proteronotal setae (Pn1-

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Pn5), with the distance between Pn1-Pn1 < Pn1-Pn2; opisthosomal setae and some ventral leg setae short and usually pectinated; very short peritreme with normal width until the middle level of coxa III, but sometimes females with a long narrow anterior extension of peritreme to level of coxa I that looks like a filament; foveae pattern 1-7-2-2-2-2, with a wide longitudinal central keel associated on lateral borders with two pairs of central subdivided or celled foveae, looking like two opposed fans (Fig. 34); sternal plate with bottle shaped outline (Fig. 35), and sternogenital plate

NEW MORPHOLOGICAL

with subpentagonal outline, with concave anterolateral borders (Fig. 36). Furthemore, species of the genus Mesoperiglischrus are associated exclusively with bats of the family Natalidae.

DISCUSSION Some newly identified morphological elements on the dorsal and ventral idiosoma of all species of the genus Periglischrus include the patterns of foveae in both sexes, and the presence or absence of a diagonal ridge in the posterolateral area of coxa I in males. These proved to be important characters used to differentiate two principal clades, the acutisternus-clade and the caligus-clade, and can serve as the basis for further phylogenetic analysis. Each clade showed a very close relationship with its host bat subfamilies or tribes. This fact may partially support the most recent phylogenetic analysis of the phyllostomid bats proposed by Baker et al. (1989) and correlated with grouping analysis of the genus Periglischrus (Fig. 37). Likewise, the topography and appearence of proteronotals and poststigmal setae, the foveae pattern and interfoveal shape or ornamentation on the dorsal plate proved to be important to revalidate the genus Mesoperiglischrus. For this reason the species P. natali really belongs in this genus. Consequently Periglischrus has a total of 25 species including four undescribed species, and Mesoperiglischrus has only two valid species.

ACKNOWLEDGEMENTS I thank Ricardo Guerrero, Universidad Central de Venezuela; Robert L. Smiley, Systematic Entomology Laboratory, USDA where the mite collection of the United States National Museum, Smithsonian Institution is housed; Naomi Cuevo, Instituto de Ecología y Sistemática, Academia de Ciencias de Cuba, and Tila M. Pérez, Instituto de Biología, Universidad Nacional Autónoma de México, who lent me types and other additional material. Field collection of additional specimens in Venezuela and Cuba was possible through helpful assistance of Ricardo Guerrero, and Naomi Cuervo respectively. To G. López, A. Losoya, A. Ruíz, J. Monterrubio and M. Corona, for their helpful assistance in the field work in México. I express my appreciation to Homer A. Gamboa (Laboratorio de Microcine, Facultad de Ciencias, Universidad Nacional Autónoma de México) for providing facilities for phase contrast microscope micrographs. For their comments on drafts of the manuscript, I express my appreciation to Anita Hoffmann (Laboratorio de Acarología, Facultad de Ciencias, Universidad Nacional Autónoma de México), Juan José Morrone (Museo de Zoología, Facultad de Ciencias, Universidad Nacional Autónoma de México), Tila M. Pérez (above) and Graham

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Floater (Instituto de Ecología, Universidad Nacional Autónoma de México). This work was supported by grants from Dirección General de Asuntos del Personal Académico (PAPIIT-IN215796 and IN214599), UNAM.

REFERENCES Baker, R. J., Hood C. S., and Honeycutt R. L. (1989). Phylogenetic relationships and classification of higher categories of the new world bat family Phyllostomidae. Systematic Zoology 38, 228–238. Domrow, R. (1972). Acari Spinturnicidae from Australia and NewGuinea. Acarologia 13, 552–584. Dusbábek, F. (1968). Los ácaros cubanos de la familia Spinturnicidae (Acarina), con notas sobre su especificidad de hospederos. Poeyana serie A 57, 1–31. Furman, D. P. (1966). The Spinturnicid mites of Panama. In ‘Ectoparasites of Panama’. (Eds. R. L. Wenzel and V. J. Tipton.) pp. 125–166. (Field Museum of Natural History: Chicago.) Herrin, C. S., and Tipton, V. J. (1975). Spinturnicid mites of Venezuela (Acarina: Spinturnicidae). Brigham Young University Science Bulletin, Biological Series 20, 1–72. Hoffmann, A. (1944). Periglischrus vargasi n. sp. (Acarina: Parasitidae). Revista del Instituto de Salubridad y Enfermedades Tropicales de México 5, 91–96. Kolenati, F. A. (1857). Synopsis prodroma der Flughaut-Milben (Pteroptida) der Fledermäuse. Wiener Entomologische Monatsschrift 1, 59–61. Machado-Allison, C. E. (1964). Notas sobre Mesostigmata neotropicales II. Cuatro nuevas especies de Periglischrus Kolenati, 1857. (Acarina, Spinturnicidae). Revista de la Sociedad Mexicana de Historia Natural 25, 193–207. Machado-Allison, C. E. (1965). Notas sobre Mesostigmata neotropicales III. Cameronieta thomasi: nuevo género y nueva especie parásita de Chiroptera (Acarina, Spinturnicidae). Acta Biologica Venezuelica 4, 243–258. Machado-Allison, C. E., and Antequera, R. (1971). Notes on neotropical Mesostigmata VI: Four new Venezuelan species of the genus Periglischrus (Acarina; Spinturnicidae). Smithsonian Contributions to Zoology 93, 1–16. Morales-Malacara, J. B., and López-W, R. (1998). New species of the genus Spinturnix (Acari: Mesostigmata: Spinturnicidae) on Corynorhinus mexicanus (Chiroptera: Vespertilionidae) in Central Mexico. Journal of Medical Entomology 35, 543–550. Oudemans, A. C. (1902). Acarologische Aanteekeningen. Entomologische Berichten 1, 36–39. Wilson, D. E., and Reeder, D. M. (1993). ‘Mammal Species of the World, a Taxonomic and Geographic Reference’. 2nd. Ed. (Smithsonian Institution Press: Washington). Uchikawa, K., Zhang, M.-Y., OConnor, B. M., and Klompen, H. (1994). Contribution to the taxonomy of the genus Spinturnix (Acari: Spinturnicidae), with the erection of a new genus, Emballonuria. Folia Parasitologica 41, 287–304.

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APPENDIX Material examined of the species of the genus Periglischrus from different collections. The collections indicated below are: Colección Nacional de Acaros, Universidad Nacional Autónoma de México [CNAC], Instituto de Ecología y Sistemática, Academia de Ciencias de Cuba [IESACC], Universidad Central de Venezuela [UCV], United States National Museum, Smithsonian Institution [NMNH], and MoralesMalacara collection [MM]. Periglischrus acutisternus 3, 5 Type Series, ex Phyllostomus elongata, 6 Km S. Caripito, Monagas, Venezuela, 11.XI.63, J. Ojasti and C. Machado (901) [UCV]. P. acutisternus 1 , ex Phyllostomus hastatus , Armihuari, Río Camisea, La Convención, Cusco, Perú, 18.V.97, C. Ascorra (212-010597) [UCV]. Periglischrus paracutisternus Paratype , ex Trachops cirrhosus, Smithsonian Venezuela (9337) [UCV]. P. paracutisternus 7 , 4 , ex Trachops cirrhosus, Km 84, Carretera El Dorado Santa Elena de Uairen, Estado Bolivar, Venezuela, VIII.87, R. Guerrero (2679) (83-270887) [UCV]. P. paracutisternus 1 , 1 , ex Trachops cirrhosus, Cenote Yacmán, Tecoh, Yucatán, 16.XI.91, J. B. Morales-Malacara (JMM038) [MM]. Periglischrus dusbabeki Paratype , ex Mimon crenulatum, Smithsonian Venezuela (05297) [UCV]. P. dusbabeki 4 , 2 , ex Mimon crenulatum, Agropecuaria San José 10 Km SW Morón, Estado Carabobo, Venezuela, III.87, R. Guerrero (2482) (06130387-2) [UCV]. Periglischrus tonatii Allotype , ex Tonatia carrikeri, T.F. Amazonas, 163 Km ESE Pto. Ayacucho, Venezuela, 24.VII.67 (SVP28813) [NMNH]. P. tonatii Paratype DN, ex Tonatia brasiliensis, T.F. Amazonas, 163 Km ESE Pto. Ayacucho, Venezuela, 24.VII.67 (SVP30068) [NMNH]. P. tonatii 1 , ex Tonatia silvicola, Capibara, Río Casiquiare, Edo. Amazonas (no date), R. Guerrero (Nº19359-D) [UCV]. Periglischrus sp. B 5 , ex Tonatia evotis, Bacalar, Quintana Roo, México, 19.IV.83, H. Arita (CNMA/329 HAW) [MM]. Periglischrus sp. B 1 , ex Tonatia evotis , Bacalar, Quintana Roo, México, 19.IV.83, H. Arita (CNMA/339 HAW) [MM]. Periglischrus sp. B 2 , ex Tonatia evotis , Bacalar, Quintana Roo, México, 19.IV.83, R. Medellín (CNMA/1175 RAML) [MM]. Periglischrus sp. B 1 , 2 , ex Tonatia evotis , Estación Chajul, SEDUE, Reserva Montes Azules, Ococingo, Chiapas, México, 31.I.86, J. Galván (CNMA/778 JG) [MM]. Periglischrus gameroi Paratype , ex Lonchorhina aurita, Smithsonian Venezuela, 18 Km N Valera (El Cenizo), Trujillo State, Venezuela, 3.IX.65 (02502) [UCV]. P. gameroi Paratype , ex Lonchorhina aurita, Smithsonian Venezuela, 23 Km NW Valera (Agua Santa), Trujillo State, Venezuela, 18.IX.1965 (3004) [UCV]. P. gameroi 3 , 2 , ex Lonchorhina aurita, Cueva del Polvorín, Cerro de Oro, Ojitlán, Tuxtepec, Oaxaca, México, 30.VIII.92, M. Corona (LVFC/MCT920830) [MM]. Periglischrus micronycteridis Paratype , ex Micronycteris megalotis, Boringuen Canal Zone, Panamá, 24.X.1961, R. L. Wenzel and C. M. Keenan [UCV].

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Periglischrus parvus Holotype , 2  Paratypes, ex Micronycteris sp. (aff. hirsuta), 6 Km S Caripito Monagas, Venezuela, 11.XI.63, C. E. Machado and J. Ojasti (915) [UCV]. P. parvus 11 , 2 , Paratypes, ex Micronycteris nicefori, 6 Km S Caripito. MO, Venezuela, 11.XI.63 (904) [UCV]. Periglischrus torrealbai 2  Paratypes, ex Phyllostomus discolor, 3 Km SW El Claro (Barlovento), Edo. Miranda, 4.VI.64, J. Ojasti and C. Machado (1322) [UCV]. P. torrealbai 2  Paratypes, ex Phyllostomus hastatus, Caripe, Valle de Caripe, Edo. Monagas, 6.VI.1964, J. Ojasti and C. Machado (1359-60) [UCV]. P. torrealbai 1  ex Phyllostomus elongatus , Pakitza, Parque Nacional Manú, Perú, II.92, C. Ascorra (90–100292) [UCV]. P. torrealbai 1 , ex Phyllostomus hastatus , Armihuari, Río Camisea, La Convención, Cusco, Perú, 18.V.97, C. Ascorra (212-010597) [UCV]. P. torrealbai 3 , ex Phyllostomus discolor, Catemaco, Veracruz, 28.VII.65, A. Hoffmann [CNAC]. Periglischrus paratorrealbai Holotype , ex Phylloderma stenops, T.F. Amazonas, 84 Km SE Esmeralda, Boca Mavaca, Venezuela, 23.III.67 (SVP-17345) [NMNH]. P. paratorrealbai Allotype , ex Phylloderma stenops, T.F. Amazonas, 84 Km SE Esmeralda, Boca Mavaca, Venezuela, 23.III.67 (SVP-17345) [NMNH]. Periglischrus sp. A 4 , 1 , ex Tonatia bidens , Arroyo José, Estación Chajul, SEDUE, Reserva Montes Azules, Ococingo, Chiapas, 28.I.86, R. A. Medellín (CNMA/1628RAML) [MM]. Periglischrus delfinadoae Allotype , ex Macrotus waterhousei minor, Soroa, Prov. Pinar del Río, Cuba, 19.VIII.65, Dusbábek and de la Cruz [IESACC]. P. delfinadoae 1 , 1 , ex Macrotus waterhousii , 2 Km NW El Infiernillo, Michoacán, Mexico, 2.I.1994, M. L. Romero (TK45025) [MM]. P. delfinadoae 1 , ex Macrotus waterhousii , El Aguaje, 5 Km N Patzcuaro, Michoacán, 2.VIII.1994, C. Sánchez (TK45394) [MM]. Periglischrus ramirezi Paratype , ex Rhinophylla pumilio, 85 Km SSE El Dorado, Venezuela, 26.V.66 (8842) [UCV]. Periglischrus grandisoma Holotype , ex Phylloderma stenops, T. F. Amazonas, 163 Km ESE Pto. Ayacucho, Venezuela, 13.VII.67 (SVP26298) [NMNH]. P. grandisoma Allotype , ex Phylloderma stenops, T. F. Amazonas, 163 Km ESE Pto. Ayacucho, Venezuela, 13.VII.67 (SVP-26298) [NMNH]. Periglischrus caligus 6 , 2 , ex Glossophaga soricina, Gruta de Juxtlahuaca, Quelchultenango, Guerrero, México, 12.VI.82, J. B. Morales-Malacara [MM]. P. caligus 3 , ex Glossophaga sp., San Pablo Hidalgo, Plan de Ayala, Morelos, México, 12.XII.83, D. Garrido [MM]. P. caligus 3 , 3 , ex Glossophaga sp. , 1.5 Km E San Pablo Hidalgo, Plan de Ayala, Morelos, México, 10.III.84, D. Garrido [MM]. P. caligus 2 , ex Glossophaga sp., 1.5 Km E San Pablo Hidalgo, Plan de Ayala, Morelos, México, 10.III.84, D. Garrido [MM]. P. caligus 5 , ex Glossophaga sp., Túnel del Arco, San Juan Chinameca, Plan de Ayala, Morelos, México, 01.IV.84, D. Garrido [MM]. Periglischrus sp C 1 , ex Choeronycteris sp., Xochicalco, Morelos, 5.V.65, T. Alvarez [CNAC]. Periglischrus sp. C 4 , 1 , ex Choeronycteris mexicana, Río Salado, Zapotitlán de las Salinas, Puebla, 18.V.95, G. López (UAMI/GLO 669) [MM].

NEW MORPHOLOGICAL

Periglischrus vargasi 1 , 1, ex (?), Grutas de La Estrella, 10 Km de Tonatico, Estado de México, México, 22.III.51, A. Hoffmann (366) [CNAC]. P. vargasi 1 , ex Anoura geoffroyi, Cueva de San Juan, Tepoztlán, Morelos, México, 30.VI.79 M. L. Ayala [CNAC]. P. vargasi 1 , ex Anoura geoffroyi, Cueva de San Juan, Tepoztlán, Morelos, México, 9.XII.78, L. Becerra [MM]. P. vargasi 5 , 4 , ex Anoura geoffroyi, Gruta Aguacachil, Taxco, Guerrero, México, 29.XI.80, J. B. Morales-Malacara [MM]. Periglischrus paravargasi Holotype , ex Anoura caudifera, Barinas, 2 Km SW Altamira, Venezuela, 26.XII.67 (SVP-33740) [NMNH]. P. paravargasi Allotype , ex Anoura caudifera, Barinas, 2 Km SW Altamira, Venezuela, 26.XII.67 (SVP-33740) [NMNH]. Periglischrus paracaligus Holotype , ex Leptonycteris curasoae, Zulia, 36 Km NNE Paraguaipoa, Venezuela, 30.VI.68 (SVP23598) [NMNH]. P. paracaligus Allotype , ex Leptonycteris curasoae, Zulia, 36 Km NNE Paraguaipoa, Venezuela, 30.VI.68 (SVP23598) [NMNH]. P. paracaligus 3 , 2 , ex Leptonycteris sp. , San Pablo Hidalgo, Plan de Ayala, Morelos, México, 10.III.84, D. Garrido [MM]. P. paracaligus 2 , ex Leptonycteris sp. , San Pablo Hidalgo, Plan de Ayala, Morelos, México, 10.III.84, D. Garrido [MM]. P. paracaligus 2 , ex Leptonycteris curasoae , Cueva Rey de Oro, Emiliano Zapata, Veracruz, México, 11.VI.92, A. Ruíz (JMM090) [MM]. P. paracaligus 1 , ex Leptonycteris curasoae , Cueva Rey de Oro, Emiliano Zapata, Veracruz, México, 13.VIII.92, J. Monterrubio (JMM097) [MM]. Periglischrus sp. D 1 , ex Leptonycteris nivalis yerbabuena, Hierbabuena, Guerrero, México, 16.IX.38, A. Hoffmann [CNAC]. Periglischrus sp. D 1 , ex Leptonycteris nivalis, Cueva del Diablo, Tepoztlán, Morelos, México, 12.XI.77, J. B. MoralesMalacara [CNAC]. Periglischrus sp. D 2 , 1 , ex Leptonycteris nivalis, Cueva del Diablo, Tepoztlán, Morelos, México, 24.VII.78, J. B. Morales-Malacara [CNAC]. Periglischrus sp. D 1 , ex Leptonycteris nivalis, Cueva del Diablo, Tepoztlán, Morelos, 21.V.78, J. B. Morales-Malacara [MM]. Periglischrus sp. D 2 , ex Leptonycteris nivalis, Cueva del Diablo, Tepoztlán, Morelos, 24.VII.78, J. B. Morales-Malacara [MM]. Periglischrus hopkinsi Holotype , ex Lionycteris spurelli, Boca de Villacoa (Río Orinoco), Edo. Bolívar, Venezuela, 23.IV.1964, J. Ojasti and C. Machado (1076) [UCV]. Periglischrus herrerai Holotype , ex Desmodus rotundus, Caripe (Valle de Caripe), Edo. Monagas, Venezuela, 6.VI.1964, J. Ojasti and C. Machado (1379-83) [UCV]. P. herrerai 6  Paratypes, ex Desmodus rotundus, 3 Km W de ‘El Clavo’ (Barlovento), Edo. Miranda, Venezuela, 4.VI.1964, J. Ojasti and C. Machado (1289) [UCV]. P. herrerai 2 , 4 , ex Desmodus rotundus, Cueva del Salitre, Emiliano Zapata, Morelos, México, 24.XI.79, J. B. Morales-Malacara [CNAC]. P. herrerai 2 , ex Desmodus rotun-

ANALYSIS OF THE BAT WING MITES OF THE GENUS

PERIGLISCHRUS

dus, Cueva del Diablo, Tepoztlán, Morelos, México, 24.VII.78, J. B. Morales-Malacara [MM]. Periglischrus iheringi 9 , 4 , ex Artibeus sp. , Cueva Rey de Oro, Emiliano Zapata, Veracruz, México, 11.VI.92, J. B. MoralesMalacara (JMM087) [MM]. P. iheringi 4 , ex Artibeus sp. , Cueva Rey de Oro, Emiliano Zapata, Veracruz, México, 20.I.93, A. Ruiz (JMM111) [MM]. P. iheringi 1 , 1 , ex Artibeus sp. , Cueva Rey de Oro, Emiliano Zapata, Veracruz, México, 20.I.93, A. Ruiz (JMM113) [MM]. P. iheringi 1 , ex Artibeus jamaicensis , Palacio del Gobernador, Uxmal, Yucatán, México, 23.XI.93, A. Losoya (JMM155) [MM]. Periglischrus ojastii 3 , 1 , Holotype and Paratypes, ex Sturnira lilium, 10 Km S Caripito, Monagas, Venezuela, 7.XI.1963, J. Ojasti and C. Machado (792-93) [UCV]. P. ojastii 1 , 2  Paratypes, ex Sturnira lilium, 10 Km S Caripito, Monagas, Venezuela, 11.XI.1963, J. Ojasti and C. Machado (798–99) [UCV]. P. ojastii Paratype , 10 Km S Caripito, Monagas, Venezuela, 7.XI.1963, J. Ojasti and C. Machado (799-800) [UCV]. P. ojastii 2 , 2 , Paratypes, ex Sturnira lilium, 10 Km S de Caripito, Monagas, Venezuela, 7.XI.1963, J. Ojasti and C. Machado (807-10) (85) (CNAC000187) [CNAC]. P. ojastii 2 , 4 , ex Sturnira sp. , San Pablo Hidalgo, Plan de Ayala, Morelos, México, 29.X.83, D. Garrido [MM]. P. ojastii 5 , ex Sturnira sp. , San Pablo Hidalgo, Plan de Ayala, Morelos, México, 16.IX.88, A. Losoya [MM]. Periglischrus cubanus Holotype , ex Phyllonycteris poeyi, Cueva de Santa Catalina Camarioca, Matanzas, Cuba, 3.VIII.65, Dusbábek and de la Cruz (10–069) [IESACC]. P. cubanus 2  Paratypes, ex Phyllonycteris poeyi, Cueva de Santa Catalina Camarioca, Matanzas, 3.VIII.65, Dusbábek and de la Cruz (10–076) [IESACC]. P. cubanus 2 , ex Phyllonycteris poeyi, Cueva del Indio, Prov. Habana, Cuba, 18.V.95, J. B. Morales-Malacara (JMM246) [MM]. P. cubanus 1 , ex Phyllonycteris poeyi, Cueva del Mudo, Prov. Habana, Cuba, 18.V.95, A. Losoya (Ppoe002) [MM]. P. cubanus 1 , ex Phyllonycteris poeyi, Cueva del Mudo, Prov. Habana, Cuba, 18.V.95, A. Pérez (Ppoe005) [MM]. Periglischrus natali Holotype , ex Natalus mexicanus saturatus, San Lorenzo Caves, Pt. Sherman, C. Z., Panama, 15.Mar.61, coll. Keenan and Tipton (6729) [NMNH]. P. natali Allotype , ex Natalus mexicanus saturatus, San Lorenzo Caves, Pt. Sherman, C. Z., Panama, 15.Mar.61, coll. Keenan and Tipton (6729) [NMNH]. Mesoperiglischrus natali 5 , 1 , 4 NN, ex Natalus stramineus , Cueva Arroyo Bellaco, Puente Nacional, Veracruz, 12.VIII.92, J. B. Morales-Malacara (JMM096) [MM]. M. natali 2 , ex Natalus stramineus , Cueva Arroyo Bellaco, Puente Nacional, Veracruz, 1.XII.93, J. B. Morales-Malacara (JMM175) [MM]. M. natali 1 , ex Natalus stramineus , Cueva Ricardo Zuloaga, Miranda, Venezuela, 5.XI.95, J. B. Morales-Malacara (JMM295) [MM].

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ACAROLOGY

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

FUNCTIONAL MORPHOLOGY AND FINE STRUCTURE OF THE FEMALE GENITAL SYSTEM IN TYPHLODROMUS SPP. (ACARI: PHYTOSEIIDAE)

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G. Nuzzaci, A. Di Palma, P. Aldini Agricultural Entomology Institute, University of Bari, Italy

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Abstract The morphology and fine structure of the genital system of overwintering females in two species of Typhlodromus are described by means of light and transmission electron microscopy. An unpaired ovary is present in the idiosoma, posterior to the ventriculus, dorsal to the colon and anterior to the postcolon. Dorsally, the ovary displays a central dome-shaped elevation, the camera spermatis, and the oocytes seem to be subglobular in cross section with a distinct roundish nucleolus. The soma cells of the camera spermatis support and surround the oocytes. The camera spermatis is connected ventro-laterally with the lyrate organ, which is provided with two arms that are in contact with the ovary. The arms reach the dorsal region of the idiosoma, extend anteriorly as far as coxae III, and lie between the posterior caeca and the ventriculus. The lyrate organ presents large cells provided with a very distinct nucleus. These cells make up a nutritive tissue connected to the oocytes by nutritive cords that extend into the camera spermatis. The ovary continues ventrally into the oviduct I, which has a lumen with prismatic cell walls. Oviduct II (vagina) leads to the genital orifice and has cuticle-lined walls. Key words: mite, Gamasina, anatomy, predators, genitalia, reproductive system.

INTRODUCTION Phytoseiid mites are an important element in biological and integrated control of several pests. They have been intensively studied with regard to their ecology and biology and their use in agricultural ecosystems (Kostiainen and Hoy 1996) while few data on their internal morphology are available (Akimov and Starovir 1974, 1976, 1977; Starovir, 1973, 1977, 1979; Chant 1985; Akimov and Yastrebtsov 1986; Evans 1992; de Lillo and Aldini 1994; Flechtman et al. 1994; de Lillo et al. 1996; Nuzzaci et al. 1996). The phytoseiid genital system of Phytoseiulus persimilis Athias-Henriot was investigated by Petrova (1970) with light microscopy, and Alberti (1988) has given some information in a paper on the genital system of the Gamasida. The aim of the present study is to give an account of the female reproductive system of phytoseiid mites, to compare the results with

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published information and to discuss the function of the observed structures.

MATERIALS AND METHODS Overwintering females of Typhlodromus exhilaratus Ragusa and T. rhenanoides Athias-Henriot were collected in Bari, Apulia, Southern Italy, respectively from witches’ brooms on Salix babylonica L. and from Cotoneaster horizontalis Decne fruits. Typhlodromus rhenanoides specimens were fixed in Bouin’s alcoholic solution (Rothschild et al. 1986) and embedded in a methacrylate resin (Bioacryl) (Scala et al. 1991). Semi-thin (1 µm) and thick sections (5 µm) were stained according to Mallory’s trichrome method (Mazzi, 1977) and observed and micrographed by means of a Leitz Dialux and a Zeiss III photomicroscope. Specimens of T. exhilaratus and T. rhenanoides for ultrathin sections were

THE FEMALE GENITAL SYSTEM IN TYPHLODROMUS

Figure 1

SPP.

Typhlodromus rhenanoides, semi-thin frontal section showing the general anatomy and the position of the following cross sections. The frontal and cross sections do not have exactly the same organ topography because they belong to different specimens. Scale bar: 100 µm. Abbr.: br: brain, Ca: caecum, cal: calyx, cs: camera spermatis, lo: lyrate organ, pc: post colon, v: ventriculus.

dissected, pre-fixed in Karnovsky’s (1965) solution, postfixed in Osmium tetroxide and embedded in Araldite M medium. Observations and micrographs were made using a Zeiss EM109T transmission electron microscope.

RESULTS The internal morphology of the female reproductive system in both Typhlodromus species was the same. Two different regions can be distinguished: (1) an unpaired gonad, a single oviduct I (sometimes named uterus) and an oviduct II (vagina according to different authors); and (2) a sperm access system. Gonad

The gonad is composed of the ovary sensu stricto, the camera spermatis and the so-called lyrate organ (Michael 1892), and is situated in the idiosoma, posterior to the ventriculus, dorsal to the colon and anterior to the postcolon (Figs 1, 2, 4, 17). The ovary is subglobose in shape and the oocytes have a large roundish nucleus and a distinct nucleolus provided with areas of scattered

chromatin (Figs 2, 4–5). One large vitellogenic oocyte is present and is tightly surrounded by the adjacent tissues and located dorsal to oviduct I (Fig. 4). In the camera spermatis, there is a region with large roundish darkly stained granules (Figs 2–3) that lies opposite a central core where the oocytes are arranged (ovary) (Fig. 2). The granules are electron-dense, bounded by a membrane, and contain irregular small dark inclusions (Fig. 3). The camera spermatis is composed of soma cells and is traversed by nutritive cords (Fig. 8). Soma cells make up the supporting tissue of the camera spermatis and reach the hemolymph space. They have irregular cell bodies, a roundish nucleus and a large nucleolus (Fig. 7). The cytoplasm is rich in ribosomes and microtubules (Fig. 8). Soma cells closely surround the oocytes (Figs 5, 8). Ventral to the oocytes, the camera spermatis is composed of cells more or less prismatic in section (Figs 2, 4), and continues into the oviduct I (Fig. 6). The so-called lyrate organ is composed of two arms or lobes, one on each side of the idiosoma, enlarging laterally and extending

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Figures 2–6

Typhlodromus rhenanoides: (2), (4), (6), semi-thin cross sections; (3), (5), electron micrographs. (2) At the level of the anterior region of the camera spermatis; (3) detail of the granules in the camera spermatis; (4) showing the oocytes in the ovary; (5) detail of an oocyte; (6) at the level of the oviduct I. Scale bar: 100 µm in Figs 2, 4, 6; 5 µm in Figs 3, 5. Abbr.: c: colon, Ca: caecum, cs: camera spermatis, gr: granules, lo: lyrate organ, Nooc: nucleus of oocyte, NS: nucleus of somacell, od: oviduct I, ooc: oocyte, v: ventriculus.

anteriorly up to the level of coxae III (Fig. 17). These arms arise ventro-laterally to the camera spermatis, lie between the posterior caeca and the ventriculus and reach the dorsal region of the idiosoma (Figs 1, 2, 4, 6, 7, 9). The lobes are distally smaller and contain large uniformly stained cells, which are provided with a large centrally located nucleus and a conspicuous nucleolus (Figs 1–2, 4, 6, 9). The lyrate organ is composed of both supporting and nutritive tissue (sensu Alberti and Zeck-Kapp 1986). The supporting tissue surrounds the nutritive tissue (Figs 7, 10); it is more peripheral and lies on a basal lamina. The nuclei in the branching cells of the supporting tissue are variably shaped and provided with a large nucleolus. The cytoplasm is rich in ribosomes, mitochondria, and endoplasmic reticulum and is less electron dense than the nutritive tissue (Fig. 10). The cell boundaries in the nutritive tissue of the lyrate organ are indistinct. The cytoplasm contains many elongated mitochondria, a large quantity of ribosomes, and an extensive endoplasmic reticulum that make the cytoplasm remarkably dense

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(Figs 7, 10). Large dark nuclei, each provided with a conspicuous nucleolus, and extensive areas of heterochromatin, mostly peripherically located, are also present (Fig. 10). Nutritive cords arise from the lyrate organ and reach the oocytes through the camera spermatis (Fig. 8). They contain many ribosomes and converge towards a ‘connection zone’ (sensu Alberti and Zeck-Kapp 1986) placed between the ovary and the lyrate organ. At this level the nutritive cords and the supporting cells of the lyrate organ continue into the ovary (sensu stricto). Oviduct I

The unpaired oviduct I was empty in our specimens and the lumen possesses closely opposed walls. The oviduct is composed of prismatic cells that are uniformly stained, provided with an elongated, basally located nucleus that contains a small nucleolus (Fig. 6).

THE FEMALE GENITAL SYSTEM IN TYPHLODROMUS

SPP.

Figures 7–8

Typhlodromus rhenanoides, electron micrographs: (7) showing the camera spermatis with the oocytes and the somacells; (8) detail of the oocytes and the nutritive cords. Scale bar: 50 µm in Fig. 7; 5 µm in fig. 8. Abbr.: Ca: caecum, cs: camera spermatis, gr: granules, lo: lyrate organ, MT: Malpighian tubulus, Nc: nutritive cord, Nooc: nucleus of oocyte, NS: nucleus of somacell, od: oviduct I, ooc: oocyte, S: somacell, v: ventriculus.

Figures 9–14

Typhlodromus rhenanoides, (9), (10) (11), (13), (14); (12) T. exhilaratus. Figs (9), (11), (13) semi-thin cross sections: (9) at the level of the vagina; (11) at the level of the beginning of the tubulus; (13) showing the tubulus and the calyx; (10), (12), (14) electron micrographs of: (10) nutritive and supporting tissue in the lyrate organ; (12) and (14) the calyx. Scale bar: 100 µm in Figs 9, 11, 13; 5µm in figs 10, 12, 14. Abbr.: br: brain, Ca: caecum, cal: calyx, Cx: coxae, gp: genital plate, lo: lyrate organ, m: muscle M: mitochondrion, NNt: nucleus of nutritive tissue, NSc: nucleus of supporting cell, Nt: nutritive tissue, RER: rough endoplasmic reticulum, Tu: tubulus, v: ventriculus, Va: vagina.

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Figures 15–16

Figure 17

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Typhlodromus rhenanoides, electron micrographs: (15) at the level of the solenostomes and the tubuli; (16) detail of the calyx and the spermatheca. Scale bar: 50 µm in fig. 15; 5 µm fig. 16. Abbr.: br: brain, Ca: caecum, cal: calyx, m: muscle, MT: Malpighian tubulus, So: solenostome, St: spermatheca, Tu: tubulus, v: ventriculus.

Semi-schematic drawings of Typhlodromus spp. female reproductive system. (a) dorsal view; (b) lateral view. Abbr.: cal: calyx, cs: camera spermatis, lo: lyrate organ, od: oviduct I, ooc: oocyte, St: spermatheca, Tu: tubulus, Va: vagina, III: coxae III, IV: coxae IV.

THE FEMALE GENITAL SYSTEM IN TYPHLODROMUS

Oviduct II

The oviduct II (vagina) is flattened and folded, narrows towards the genital orifice, and its walls are cuticle-lined (Fig. 9). The plicated cuticle forms numerous ridges closely apposed to each other and directed towards the duct lumen (Figs 9, 11, 13). At the level of coxa IV, strong muscles involved in oviposition are connected to the vagina (Figs 9, 11, 13). Sperm Access System

The sperm access system opens by solenostomes (sperm induction pores) close to coxae IV (Fig. 15). These pores lead into thick cuticle-lined ducts (major ducts or tubuli) that extend into the body (Figs 11, 13). The major duct lumen appears large, filled with material, and continues into the calyx (Figs 12–14); likewise, it has thick cuticle-lined walls. The epithelial cells of the calyx show a rough endoplasmic reticulum, small dictyosomes and numerous electron-lucent droplets (Fig. 14). The calyx walls are highly folded and lead into a sac-like organ, the vesicle (spermatheca), whose less sclerotised walls (Fig. 16) are folded except when it contains a spermatophore. Electron dense material was observed in the vesicle lumen (Fig. 16). Calyx and vesicle are closely apposed to the arms of the lyrate organ (Figs 1, 17). In our observations, it was not possible to detect the minor duct, neither its origin nor its termination.

DISCUSSION The organisation of the female genital system of T. rhenanoides and T. exhilaratus follows the general scheme of Dermanyssina and Parasitina (Fig. 17). The differentiation of the gonad into a germinal region (ovary proper) and a trophic region (lyrate organ) has been described in other Dermanyssina and some Parasitina (Michael 1892; Neumann 1941; Warren 1941; Young 1968; Korn 1982; De Ruijter and Kaas 1983; Akimov and Yastrebtsov 1984; Alberti and Hänel 1986; Alberti and Zeck-Kapp 1986; Alberti 1988). Our observations agree with the information reported by Alberti (1988) while they disagree with Petrova’s (1970) reports of the lateral processes (lyrate organ in our observations) being a reserve of genital cells. There are several similarities with the descriptions made for Varroa jacobsoni Oudemans (Alberti and Hänel 1986; Alberti and Zeck-Kapp 1986), i.e. the lyrate organ is composed of a supporting and a nutritive tissue. Considering this morphological and histological similarity, a nutrimental function is supposed for the Typhlodromus lyrate organ. The presence of nutritive cords that connect, through the camera spermatis, the oocytes to the lyrate organ and the high number of ribosomes present in the nutritive tissue and nutritive cords, supports this hypothesis. Moreover, the differentiation of the gonad into an ovary and a lyrate organ and their morphological and histological relationship, suggest an analogy with the telotrophic-meroistic ovarioles of insects as reported by Alberti and Zeck-Kapp (1986). The camera spermatis appers to be composed of somatic cells that make it a solid structure surrounding and holding the growing oocytes in position. Alberti and Zeck-Kapp (1986) described two cell types composing the camera spermatis; in Typhlodromus only one kind of somatic cells was observed.

SPP.

The sperm access herein agrees with the information given by Alberti (1988) for Phytoseiulus, except for the minor duct that was not located. Likewise, we observed neither a connection between vesicle and oviduct I (Akimov and Yastrebtsov 1984), nor the presence of ‘inner cells’ in the vesicle and in the sperm duct (Alberti and Hänel 1986), as reported for Varroa (laelapid-type sperm access system). Thus, it has not been possible to establish a connection between the vesicle and the camera spermatis in the phytoseiid-type sperm access system. In conclusion, our findings on Typhlodromus spp. widen our knowledge of the phytoseiid reproductive system and confirm Alberti’s (1988) observations based on Phytoseiulus. Regarding the sperm access system, it is still not possible to trace the minor duct or to find its final end so as to clarify a possible implication in spermatozoa transport.

ACKNOWLEDGEMENTS We are grateful to Prof. S. Ragusa Di Chiara, Agricultural Entomology Inst., Palermo, Italy, for species identification, Prof. G. Alberti, Zoologisches Institut und Museum, Ernst Moritz Arndt Universität, Greifswald, Germany and Emeritus Prof. G. O. Evans for critical reading of the manuscript. The first and the second author have jointly planned the research, analysed and interpreted the observations; the third author has mainly been responsible for the preparation of the Figures.

REFERENCES Akimov, I. A., and Starovir, I. S. (1974). Morpho-functional features of the digestive system in Phytoseiulus persimilis Athias-Henriot (Gamasoidea, Phytoseiidae). Vestnik Zoologii 4, 60–64. Akimov, I. A., and Starovir, I. S. (1976). Structure of the digestive system of the mites Amblyseius andersoni and Amblyseius reductus (Parasitiformes, Phytoseiidae). Vestnik Zoologii 4, 7–13. Akimov, I. A., and Starovir, I. S. (1977). Morpho-functional features of the digestive system of the mite Amblyseius andersoni (Gamasoidea, Phytoseiidae). Vestnik Zoologii 3, 82–86. Akimov, I. A., and Yastrebtsov, A. V. (1984). Reproductive system of Varroa jacobsoni. 1 Female reproductive system and oogenesis. Vestnik Zoologii 6, 61–68. Akimov, I. A., and Yastrebtsov, A. V. (1986). Muscle system and skeletal elements in Phytoseiidae (Parasitiformes). Entomologischeskoe Obozrenie 65(4), 844–849. Alberti, G., and Hänel, H. (1986). Fine structure of the genital system in the bee parasite Varroa jacobsoni (Gamasida: Dermanyssina) with remarks on spermiogenesis, spermatozoa and capacitation. Experimental and Applied Acarology 2, 63–104. Alberti, G., and Zeck-Kapp, G. (1986). The nutrimentary egg development of the mite, Varroa jacobsoni (Acari, Arachnida), an ectoparasite of honey bees. Acta Zoologica 67, 11–25. Alberti, G. (1988). Genital system of Gamasida and its bearing on phylogeny. In ‘Progress in Acarology, vol 1’. (Eds G. P. Channa Basavanna and C. A. Viraktamath) pp. 197–204. (Oxford and IBH Publishing, New Delhi.) Chant, D. A. (1985). Internal anatomy. In: ‘Spider Mites, their biology, natural enemies and control. Vol. 1B’. ( Eds W. Helle and M. W. Sabelis) pp. 11–16. (Elsevier: Amsterdam.) de Lillo, E., Aldini, P. (1994). Contributo alla conoscenza delle parti boccali in femmine di Typhlodromus exhilaratus Ragusa (Acari: Phytoseiidae). In

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G. Nuzzaci et al. ‘Atti XVII Congresso nazionale italiano di Entomologia’. pp. 287–294. (Udine 13–18 Giugno.) de Lillo, E., Nuzzaci, G., Aldini, P. (1996). Fine structure of the mouthpart sensilla in females of Typhlodromus exhilaratus Ragusa (Phytoseiidae). In ‘Acarology IX Proceedings’. (Eds R. Mitchell, D. J. Horn, G. R. Needham and W. C. Welbourn.) pp. 287–295. (Ohio Biological Survey: Columbus.) De Ruijter, A., Kaas, J. P. (1983). The anatomy of the Varroa-mite. In ‘Varroa jacobsoni Oud. affecting honey bees: present status and needs’. (ed. R. Cavalloro.) pp. 45–47. (A. A. Balkema: Rotterdam.) Evans, G. O. (1992). ‘Principles of Acarology.’ (CAB International: Wallingford.) Flechtmann, C. H. W., Evans, G. O., and McMurtry, J. A. (1994). Some noteworthy features of the chelicerae and subcapitulum of Phytoseiulus longipes Evans (Acari: Mesostigmata; Phytoseiidae), with observations on the preoral channel in the Phytoseiidae. Experimental and Applied Acarology 18, 293–299. Karnovsky, M. J. (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. Journal of Cell Biology 27, 137–138. Korn, W. (1982). Zur Fortpflanzung von Poecilochirus carabi G. u. R. Canestrini 1882 (syn. P. necrophori Vitzt.) und P. austroasiaticus Vitzthum 1930 (Gamasina, Eugamasidae). Spixiana 5, 261–588. Kostiainen, T. S., and Hoy, M. A. (1996). ‘The Phytoseiidae as Biological Control Agents of Pest Mites and Insects. A Bibliography.’ (University of Florida: Gainesville.) Mazzi, V. (1977). ‘Manuale di tecniche istologiche e istochimiche.’ (Piccin Ed.: Padova.) Michael, A. D. (1892). On the variations in the internal anatomy of the Gamasidae, especially in that of the genital organs, and in their mode of coition. Transactions of the Linnean Society of London, Zoological Ser. 2. 5, 281–324. Neumann, K. W. (1941). Beiträge zur Anatomie und Histologie von Parasitus kempersi Oudms. (Parasitidae). Zeitschrift für Morphologie der Tiere 37, 613–682.

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Nuzzaci, G., and Vovlas, N. (1976). Osservazioni dei caratteri tassinomici degli Eriofidi al microscopio elettronico a scansione. In ‘Atti XI Congresso nazionale italiano Entomologia’. pp. 117–122. (Portici: Sorrento.) Nuzzaci, G., Di Palma, A., de Lillo, E., and Aldini, P. (1996). Prosomal glands in Typhlodromus spp. females (Mesostigmata: Phytoseiidae). In ‘Ecology and Evolution of the Acari’. (Eds J. Bruin, L. P. S. van der Geest and M. W. Sabelis.) pp. 637–650. (Kluwer: Dordrecht.) Petrova, V. I. (1970). Structure and development of the male genital system of the predaceous mite Phytoseiulus persimilis Athias-Henriot. Izvestiya Akademii Nauk Latviiskoi SSR 5, 24–27. Rothschild, M., Schlein, Y., Ito, S. (1986). ‘A Colour Atlas of Insect Tissues. Via the flea.’ (Wolfe Publishing Ltd.: Weert.) Scala, C., Cenacchi, G., Preda, P., and Pasquinelli, G. (1991). Formulazione e applicazione di un nuovo polimero acrilico per microscopia ottica e microscopia elettronica. In ‘Atti del XVIII Congresso di M.E.’ pp. 29–30 (Padova.) Starovir, I. S. (1973). Some peculiarities in the structure of the digestive and excretory systems in Phytoseiulus persimilis Athias-Henriot (Parasitiformes, Phytoseiidae). Vestnik Zoologii 5, 72–77. Starovir, I. S. (1977). Characteristic of the structure of the digestive system in the mite Amblyseius herbarius (Gamasoidea, Phytoseiidae). Vestnik Zoologii 2, 24–27. Starovir, I. S. (1979). Functional histology in the intestinal epithelium in Amblyseius herbarius (Gamasoidea, Phytoseiidae). Vestnik Zoologii 3, 40–44. Warren, E. (1941). On the genital system and modes of reproduction and dispersal in certain gamasid mites. Annals of the Natal Museum 10, 95–126. Young, J. H. (1968). The morphology of Haemogamasus ambulans. 2. Reproductive system. Journal of the Kansas Entomological Society 41, 532–543.

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

ANATOMY AND ULTRASTRUCTURE OF THE FEMALE REPRODUCTIVE SYSTEM OF SARCOPTES SCABIEI (ACARI: SARCOPTIDAE)

Department of Ecology and Evolutionary Biology, University of Connecticut – Hartford Campus, 85 Lawler Road, West Hartford, CT 06117

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Clifford E. Desch

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Abstract The female reproductive system of Sarcoptes scabiei is described using light and transmission electron microscopy. The system consists of two functional units: a sperm storage and transport component, and a pair of ovaries and a shell gland. The two units are not directly connected so that sperm must migrate through female tissues to reach the ovaries. The ‘nutritive’ type ovary consists of a large central cell surrounded by developing previtellogenic oocytes which are connected to the central cell via cytoplasmic bridges. Oocytes are fertilized in the ovary before moving to the paired oviducts where chorion formation and vitellogenesis take place. These two processes are carried out by the oocyte in that nurse and follicle cells are absent, and the ovary wall is nonsecretory. The oviducts converge on the shell gland which is made up of two cell types. Type 1 cells apply their secretory granules to the outer surface of the chorion to form an exochorion. Thus, the egg shell is a bipartite structure of dual origin. Release of the secretory material of Type 2 cells was not observed. The shell gland is the only part of the reproductive tract with intrinsic musculature. Mature eggs pass to the outside through the cuticle-lined vagina.

INTRODUCTION Although the ectoparasitic acaridid subfamily Sarcoptinae contains only four monotypic genera, one of its members, Sarcoptes scabiei, is cosmopolitan and is of considerable medical and veterinary importance. Current thinking is that primates are the ancestral hosts of the sarcoptines, with Sarcoptes originating on the hominoid line, which includes Homo. From man, S. scabiei transferred to domestic mammals and from them to wild hosts (Fain 1968; Andrews 1983). Presently 43 mammals species in eight orders are known to host this mite and experimental transmissions could greatly expand this number. In at least one host, Vulpes fulva, the red fox, infestation is 100% fatal (Stone et al. 1972; Tullar and Berchielli 1981). Given the health concerns caused by this mite, an understanding of its biology is important, including a thorough knowledge

of its anatomy. The external morphology of S. scabiei is known in detail at the level of light microscopy (Buxton 1921; Heilesen 1946; Fain 1968) and scanning electron microscopy (SEM) (Juhlin et al. 1975; Pascual et al. 1977; Andrews and Desch 1983). Heilesen (1946) also provided some cursory information on the internal anatomy of the nervous, digestive and reproductive systems. More recently, transmission electron microscopy (TEM) has been employed to describe spermatogenesis and the male reproductive system (Witali¡ski and Afzelius 1987), chorion structure and egg shell formation within the female reproductive tract (Witali¡ski 1993), the shell of oviposited eggs (Mazzini and Baiocchi 1983; Fimiani et al. 1997), and the digestive system (Desch et al. 1991). The following account of the female reproductive system using light microscopy and TEM adds to our knowledge of this parasite of medical and veterinary concern.

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Figure 1

Semidiagramatic longitudinal section near midline of female Sarcoptes scabiei. AMg = anterior midgut, C = chelicera, CC = central cell, CP = copulatory papilla, E = esophagus, Hg = hindgut, IC = inseminatory canal, Od = oviduct, Oo = oocytes, PD = pharyngeal dilator muscle, PMg = posterior midgut, SG = salivary gland, SGD = salivary gland duct, ShG1 = shell gland-cell Type 1, ShG2 = shell gland-cell Type 2, St = spermatheca, Sy = synganglion, V = vagina. Fold of vaginal wall not indicated in order to simplify the drawing.

MATERIALS AND METHODS Female Sarcoptes scabiei var. canis, taken from chronically infested New Zealand white rabbits, were prepared for TEM by first carefully removing one leg while immersed in a drop of fixative consisting of 2% glutaraldehyde and 2% formaldehyde in 0.1M Nacacodylate buffer (pH 7.2). Fixation was carried out for 1 hr at room temperature followed by an overnight buffer wash. They were postfixed in 1% OsO4 in 0.1M Na-cacodylate buffer for 1 hr at room temperature, dehydrated in a graded series of alcohol, and embedded in low viscosity resin (Spurr 1969). Sections were cut with a diamond knife, placed on coated or uncoated grids and stained with lead salts (Sato 1968) for observation with a JOEL 100 transmission electron microscope. Thick plastic sections were stained with a mixture of Azure II and methylene blue for light microscopy (Richardson et al. 1960).

RESULTS AND DISCUSSION The female reproductive system of Sarcoptes scabiei, as in other Acaridida, is anatomically and functionally of two parts: a sperm storage component and paired ovaries with a shell gland (Fig. 1). The unpaired spermatheca, the site of sperm capacitation and storage, is situated above the gut at the level of the junction of the posterior midgut and the cuticle-lined hindgut, and is approximately 35 µm anterior to the copulatory papilla (Fig. 1). It is nearly spherical, with an outer diameter of 25–30 µm (Figs 4, 5). The wall of the spermatheca is a double layer of flattened cells except for a pair of mound-shaped areas, 4–6 cells thick, protruding from the posterolateral wall. The latter cells, although not flattened, are similar to the other wall cells. They come into close proximity to the ovaries but do not fuse with them. These protru-

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sions may be functionally comparable to the ‘transitory cones’ in Acarus siro (Witali¡ski et al. 1990). The outer layer of cells of the spermathecal wall rests on an undulate basal lamina which is without apparent disruptions or gaps. The spermathecal chamber is spherical and lined with a thin, smooth to crenellate, electron dense lamina (Fig. 3). A similar lining in the spermatheca of A. siro is considered to be cuticular (Witali¡ski et al. 1990). The lumenal sides of the inner layer of wall cells follow the contours of this lamina and do not possess microvilli. In some individuals the chamber is filled with sperm which exhibit no pattern in their packing arrangement (Fig. 4). These may be recently inseminated females. The spermatheca in others contains few sperm and the intersperm spaces are filled with electron dense granules in a less dense matrix (Fig. 5). The granules vary in size and are packed in the manner of soap bubbles. Neither the spermathecal wall nor the sperm exhibit secretory activity and are not considered the source of this material. This material, however, does appear similar to that produced by the accessory gland in A. siro (Witali¡ski et al. 1990). Witali¡ski and Afzelius (1987) reported the presence of, but did not describe, an accessory gland in male S. scabiei. The cuticular copulatory papilla, positioned posterodorsal to the anus, is 5 µm long with the opening of the inseminatory canal at its apex (Fig. 2). This canal meanders gently forward to join the posterior face of the spermatheca between the two mound-shaped protrusions (Fig. 3). The lumen of the canal is lined with cuticle, 0.20–0.25 µm thick, which appears bipartite with high electron density along the lumen and with material of moderate density on the outer surface. Tangential sections of the cuticle lining strongly suggest a taenidia-like structure as in A. siro (Witali¡ski et al. 1990). The hypodermal cells of the inseminatory canal rest on an undulate basal lamina, which is contiguous with that of the

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Figures 2–5

SYSTEM OF SARCOPTES SCABIEI

TEM micrographs of female Sarcoptes scabiei. Figure 2. Copulatory papilla (CP) with inseminatory canal (IC). Cu = cuticle of body wall. Bar = 2 µm. Figure 3. Gently undulate region of inseminatory canal (IC) near its junction with the spermatheca. BL = basal lamina of spermatheca wall, Is = interstitial cell, Sp = sperm, * = sperm among cells of spermatheca wall. Bar = 2 µm. Figure 4. Longitudinal section through spermatheca tightly packed with sperm (Sp). Cu = cuticle of body wall, PMg = posterior midgut, SW = spermatheca wall. Bar = 2 µm. Figure 5. Longitudinal section through spermatheca with few sperm (Sp) and much secretory material (SM). Cu = cuticle of body wall, N = nucleus of spermatheca wall cell, * = sperm among cells of spermatheca wall. Bar = 2 µm.

spermatheca wall, and their lateral membranes are highly interdigitated (Fig. 3). The nuclei lie near the basal lamina, and are oval in shape with patches of scattered chromatin and a small nucleolus. The inner diameter of the inseminatory canal increases gradually from 0.5 µm in the genital papilla (Fig. 2) to 2.0 µm near its junction with the spermatheca (Fig. 3). Sperm and an amorphous material of electron density similar to the granular

material in the spermatheca fill the lumen. The increasing diameter of the inseminatory canal may facilitate sperm transfer by reducing friction (Walzl 1992) as well as retarding any backflow. The relatively thick cuticular lining of the lumen may prevent its collapse during body movements or when organs are displaced and compressed by growing oocytes, and may prevent rupture if sperm are introduced into the canal under pressure.

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Figures 6–8

TEM micrographs of female Sarcoptes scabiei. Figure 6. Mound-shaped cellular extension of spermatheca wall (SW) in close proximity with ovary wall (OW). CC = central cell, Hg = hindgut, IC = inseminatory canal, Is = interstitial cell, N = portion of nucleus of central cell, * = sperm among cells of spermatheca wall. Bar = 2 µm. Figure 7. Crystalline inclusions (XL) in cytoplasm of central cell (CC) of ovary. Arrows indicate close proximity of basal lamina of ovary wall (OW) and spermatheca wall (SW). Bar = 1 µm. Figure 8. Sperm cells within spermatheca. C = chromatin threads, F = filaments along inner surface of plasmalemma, L = lamellae parallel to plasmalemma, M = mitochondria, N = nucleus of spermathecal wall cell, SM = secretory material. Bar = 1 µm.

Regardless of whether the sperm are loosely or tightly packed in the spermatheca, they are of irregular shape. The cytoplasm is quite electron lucent with quantities of short lengths of straight to curved lamellae and small, round mitochondria with few cisternae (Fig. 8). Some of the lamellae are oriented to form a single noncontinuous layer beneath and parallel to the plasmalemma. Sim-

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ilar but longer lamellae in sperm of the house dust mites Dermatophagoides farinae and D. pteronyssinus are derived from the Golgi apparatus by longitudinal splitting of the cisternae (Walzl 1992). Unlike in these house dust mites, however, the lamellae in S. scabiei are not arranged to indicate an antero-posterior axis. Lamellar structures, in more or less parallel array, are also observed in sperm

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Figures 9–11

SYSTEM OF SARCOPTES SCABIEI

TEM micrographs of female Sarcoptes scabiei. Figure 9. Ovary with central cell (CC) and early oocytes (Oo). Is = interstitial cell, Mv = microvilli of central cell, N = multilobed nucleus of central cell, Sp = sperm. Bar = 4 µm. Figure 10. Detail of crystalline inclusions (XL) in peripheral cytoplasm of central cell of ovary. Bar = 1 µm. Figure 11. Cytoplasmic bridge (CB) in ovary connecting central cell (CC) and early oocyte (Oo). Mv = microvilli of central cell, Sp = sperm. Bar = 2 µm.

of Caloglyphus anomalus (Reger 1971) and Psoroptes equi (Alberti 1984). The sperm lack an obvious acrosome, although Walzl (1992) suggested that the lamellae below and parallel to the cell surface may function in this capacity. Mature sperm within the testis of S. scabiei have greater electron opacity (Witali¡ski and Afzelius 1987) than those in either the spermatheca or the ovaries. This difference may represent a capacitational change.

The cytoplasmic side of the plasmalemma is lined with close-set, parallel filaments. Despite the lack of cytological landmarks to reveal sperm symmetry, these filaments may indicate that the seemingly amorphous sperm is bilateral. However, it was not determined if these filaments are circular or longitudinal. In sperm of A. siro and Tyrophagus putrescentiae the filaments are reported to run ‘parallel to the long axis’ (Witali¡ski et al. 1986).

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Figures 12–14

TEM micrographs of female Sarcoptes scabiei. Figure 12. Region of ovary with early oocytes (Oo) and sperm (Sp). CC = central cell, Mv = microvilli of central cell, SC = somatic cell. Bar = 2 µm. Figure 13. Portion of ovary and adjacent oviduct. CC = central cell, Ch = chorion of fully developed oocyte in oviduct, M = mitochondria and N = nucleus of large, previtellogenic oocyte. Bar = 2 µm. Figure 14. Previtellogenic oocytes (PvO) in ovary and vitellogenic oocyte (VO) in adjacent oviduct. BS = blister-like swelling, Ch = developing chorion, ER = cisternae of endoplasmic reticulum, M = mitochondria. Bar = 2 µm.

The filaments are not present when sperm are still in the testis (Witali¡ski 1988; Witali¡ski and Afzelius 1987; Witali¡ski et al. 1986) and their appearance in sperm within the spermatheca may represent a capacitional change. The spermatozoon lacks a flagellum and there is no muscular tissue to affect sperm transport from the spermatheca to the ovary. Means of sperm motility, presumably amoeboid, may involve these filaments (Witali¡ski et al. 1986) although there is no direct evidence for this. As in other mite species studied, the nuclear envelope is absent in the mature sperm. The chromatin appears as a cluster of short,

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thick threads of great electron density. This feature, along with very small mitochondria and lack of an acrosome, may serve as preadaptations to the development of a very narrow inseminatory canal. There is no duct or clear passage between the spermatheca and the ovaries. Sperm are seen among the cells of the spermathecal wall (Figs 3, 5) including those of the posterolateral mound-shaped protuberances (Fig. 6) and within the ovaries among the early oocytes (Fig. 9). Sperm cells apparently must penetrate female tissues to reach the oocytes (see also Alberti 1988), but none has ever been observed in transit across the lamellar lining of the

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Figures 15–17

SYSTEM OF SARCOPTES SCABIEI

TEM micrographs of female Sarcoptes scabiei. Figure 15. Region of shell gland with Type 1 secretory cells and adjacent oviduct with vitellogenic oocyte (VO). BL = basal lamina of Type 1 cell, Ch = developing chorion, Mu = intrinsic muscle of shell gland, N = nucleus of Type 1 secretory cell, OW = ovary wall, RER = rough endoplasmic reticulum, SG = multivesiculate secretory granule. Bar = 2 µm. Figure 16. Shell gland showing both Type 1 (ShG1) and Type 2 (ShG2) cells. Is = interstitial cells, Lu = lumen of shell gland, Mu = intrinsic muscle of shell gland, N = nucleus of Type 2 cell. Bar = 4 µm. Figure 17. Accretion of secretory granules of Type 1 cell (SG1) onto chorion (Ch) of an egg (E). Mu = intrinsic muscle of shell gland, PMg = posterior midgut. Bar = 2 µm.

spermatheca, basal laminae of the spermatheca wall, or ovary wall. Migrating sperm are of irregular shape like those in the spermatheca. Occasionally sperm appear nearly oval in outline and measure 3.5 µm × 5.0 µm. Although sperm are common in the ovary none was ever seen entering or within an oocyte. The cytoplasm of the

sperm within the ovary is more electron lucent and appears less structured than that of sperm within the spermatheca. Perhaps these are failed sperm in the process of degeneration. Sperm have not been observed in oocytes of Notoedres cati (Witali¡ski 1988), but sperm chromatin was seen in early oocytes of T. putrescentiae

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(Witali¡ski et al. 1986). Sperm were never seen in the body cavity of S. scabiei outside the confines of the basal laminae of the ovaries or spermatheca, although the interlamellar distance between these two organs may be small (Figs 6, 7). The interstitial cells which surround the ovaries and the spermatheca are the same as those around the gut. These cells possess a large nucleus with prominent nucleolus, numerous mitochondria, rough endoplasmic reticulum (RER) with swollen cisternae and many crystalline concretions (Figs 3, 6, 9). Their distribution and contents suggest they are involved in processing and transfer of nutrients from the gut to other organs, such as the ovary, and processing and storage of nitrogenous wastes. A Malpighian tubule system is not present. The intercellular (haemocoelic) spaces between the various organs and these cells are greater than the intercellular spaces within the organs. This loose fit may allow organ displacement as large oocytes pass through the oviduct and the shell gland. The ovaries of S. scabiei are similar to those of A. siro (Witali¡ski et al. 1990) in consisting of a large central, ‘nutritive’ cell surrounded by oocytes of various sizes (Fig. 1). The ovary wall is a monolayer of highly flattened cells subtended by a basal lamina. The central cell is 25–30 µm in diameter with a very large, intricately multilobed nucleus in the center (Figs 6, 9). This nuclear structure probably reflects a high output of ribosomal and messenger RNAs. In D. farinae and D. pteronyssinus the central cell is considered to be a multinucleate syncytium (Walzl 1992). In S. scabiei each lobe of the nucleus has a prominent nucleolus and the chromatin tends to be scattered along the inner face of the nuclear envelope. The nuclear envelope has many pores. Rough endoplasmic reticulum occurs throughout the cytoplasm as single or sets of two or three parallel cisternae. Granules of crystalline material are also not uncommon (Figs 7, 10) and are very similar to structures, purported to be lysosomes, in cells lining the spermatheca of Varroa jacobsoni (see Alberti and Hänel 1986). The ground substance of the central cell is densely packed with free ribosomes. Mitochondria are not apparent. Folded and bent microvilli extend from the central cell to fill the spaces between the loosely packed early oocytes (Figs 9, 11, 12). More peripherally, these spaces are occupied by so-called somatic cells and sperm cells (Fig. 12).

dria, now more elongate, appear (Fig. 14). The nucleus takes on a less regular shape with very electron lucent nucleoplasm (Fig. 13). Condensed chromatin is not seen although the nucleoli remain prominent. The nuclear envelope has many close-set pores. In ovaries with a number of late previtellogenic and incipient vitellogenic oocytes, the oocytes are closely apposed to each other, to the exclusion of the somatic and sperm cells, and take on a polygonal shape. In ovaries with fewer late oocytes, and thus more space, the oocytes are more round and appear to be surrounded by a layer of attenuated somatic cells. The late stage previtellogenic oocytes may be larger than the central cell. Their increased volume causes the central cell to be distorted by pressing it against the posterior midgut wall (see Desch et al. 1991). This proximity may facilitate nutrient transfer from the gut wall to the central cell. The peripheral ooplasm of these larger oocytes contains cisternae of RER arranged more or less parallel to the oolemma. Their orientation suggests that they may be involved in deposition of chorion material. Oocytes of this stage move into the oviduct where chorion formation and vitellogenesis take place. An oviduct departs the ventral surface of each ovary to join, after a short distance, at the midline with the unpaired shell gland (Fig. 1). The wall of the oviduct is made up of a single layer of highly folded, non-secretory epithelial cells which occlude the lumen when an oocyte is not present. The folded nature of the cells allows the wall to stretch and bulge to accommodate a large oocyte at which time they become flattened and attenuated. No intrinsic muscles are associated with the oviduct walls. Yolk spheres, which are initially of low to moderate electron density, appear in large numbers as vitellogenesis commences. Subsequently two forms of yolk granules appear: uniformly electron dense granules of 2.0–3.5 µm diameter and electron lucent granules of 1.0 mm or less diameter (Fig. 14). Vitellogenesis is nearly complete by the onset of chorion formation.

The early oocytes are grouped around the posterior and lateral faces of the central cell (Fig. 9). The medial face, which is in close proximity to the gut, is devoid of oocytes. Each oocyte is attached to the central cell via a cytoplasmic bridge (Fig. 11) which in some instances is quite long since an oocyte may be 10 µm from the central cell. The earliest oocytes observed are more or less round and 3–4 µm in diameter. They possess a round nucleus 2.5 µm in diameter with dispersed clumps of chromatin and one or two round nucleoli. The cytoplasm has electron density similar to that of the central cell, being packed with ribosomes and many small mitochondria. It is presumed, based on the observation of sperm chromatin in the early oocyte of T. putresecentiae (Witali¡ski et al. 1986), that sperm entry occurs at a similar stage of oocyte development in S. scabiei.

Electron lucent, blister-like separations, some quite large, occur between the ooplasm and chorion (Fig. 14), and even between the chorion and oviduct wall. Witali¡ski (1993) reported these in S. scabiei and N. cati, and referred to them as ‘lenticular perivitelline spaces.’ Their flocculent content is believed to be incorporated into the developing chorion. The spaces seen in the present study had very little material of electron opacity. There is no direct morphological evidence of their origin or mode of formation and, because they also occur outside the chorion, they may represent fixation artifact. However, as Witali¡ski (1993) noted, when chorion formation is complete these spaces are no longer observed. When the chorion is first observed it is 0.2 µm thick and is electron lucent with dispersed flocculent material. The surfaces are not smooth (Figs 14, 15). By the time the oocyte leaves the oviduct the chorion has reached its full thickness of 1.2 mm and is smooth surfaced (Fig. 13). This portion of the chorion appears to be solely of oocyte origin and is designated as endochorion by Witali¡ski (1993).

As oocytes enlarge they become compressed between the central cell and the ovary wall. Presumably the intercellular bridges are maintained. The ovary wall is forced to bulge outward. In addition to the free ribosomes, great amounts of RER and swarms of mitochon-

Following completion of yolk and endochorion deposition, oocytes enter the unpaired shell gland which runs anteroventrally to terminate at its junction with the vagina (Fig. 1). Only one mature oocyte, now considered an egg, occupies the lumen of the shell

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gland at a time. The wall of the gland is a single layer of cuboidal cells subtended by a basal lamina, which is extensively folded when an egg is not present in the lumen (Figs 15, 16). Fine strands of intrinsic muscles attach to its outer surface and serve to move the egg along. Two types of secretory cells make up different regions of the gland. About 3/4 the length of the gland from the oviducts forward is lined with cells (Type 1) containing many spherical packets, up to 1.0 µm in diameter, of multivesiculate secretory material and much RER (Fig. 15). The secretory material and the contents of the RER cisternae exhibit similar electron density, and some cisternae appear to be confluent with the secretory spheres. The nucleus, located basally, has lobes and indentations, and the nucleoplasm contains clumps of chromatin and a nucleolus. The cells possess relatively few mitochondria which are scattered in the perinuclear region. The secretory granules are released from the apical cell membrane into the lumen where the contents loose their spherical groupings and become tightly packed while maintaining their vesicular form (Fig. 16). Their electron density does not change following release and their presence makes the gland lumen visible even when an egg is not present. The distal 1/4 of the shell gland , near its junction with the vagina, is made of a second type of secretory cell (Type 2) (Fig. 16). The contents of the spherical secretory granules, which measure up to 0.8 µm in diameter, are uniformly of medium to high electron density. These cells also contain a basal nucleus, few mitochondria and much RER. Release of their secretory material into the lumen or onto the egg surface was not observed. This latter cell type was not reported in S. scabiei by Witali¡ski (1993). As an egg passes through the shell gland, the secretory cells are stretched and flattened. The endochorion now contains uniformly distributed flecks of electron dense material (Fig. 17). This dense material does not form channels across the chorion. During the egg’s passage to the vagina, the multivesiculate material is accreted onto the outer surface of the endochorion to form a lumpy surface coat (Fig. 17), as observed on oviposited eggs (see Mazzini and Baiocchi 1983; Fimiani et al. 1997). Witali¡ski (1993) refers to this second layer as an exochorion. Thus the mature, fertilised egg has a shell of dual origin. The outer layer may serve to attach the egg to the floor of the tunnels excavated by the female mite in the host’s skin (Fimiani et al. 1997). These authors observed that the exochorion of eggs oviposited in situ dissolves in the area where the egg interfaces with the skin leaving the endochorion in close contact with the epithelial cells. The cuticle-lined vagina extends from the shell gland to the genital opening (Fig. 1), a distance of 45–60 µm, and is 65–70 µm at its widest. The thickness of the cuticular lining tapers from nearly equal to that of the body wall, just inside the transverse genital opening, to about 1/3 this thickness at the junction with the shell gland. The lumen for most of its length is triradiate, appearing as an inverted ‘T’ in cross section. This configuration allows for expansion to accommodate passage of an egg. The two lateral arms are each up to 35 µm long and the medial arm extends 25–30 µm dorsally. The dorsal arm, however, tapers from its maximum length behind the genital opening to disappear just anterior to the shell gland. In longitudinal view, the vagina is seen

SYSTEM OF SARCOPTES SCABIEI

to fold tightly back on itself about halfway along its length thus, effectively closing it off to the outside except during oviposition. The hypodermal cells are typical of those below the exoskeleton. There are no intrinsic muscles associated with the vagina. The force needed to push an egg through the folded vaginal canal must be generated by the muscles of the shell gland and by the hydrostatic pressure produced by contraction of body wall muscles.

ACKNOWLEDGEMENTS Lucy Yin (Electron Microscopy Center, University of Massachusetts) is gratefully acknowledged for her careful and skillful preparation of the mites for transmission electron microscopy. Thanks also to Larry Arlian (Wright State University) for providing the living mites, and to Xu Yue and Kevin Murphy (at the Biology Computer Resource Center, University of Massachusetts) for their assistance in computer processing of the figures. This research was funded, in part, by the University of Connecticut Research Foundation.

REFERENCES Alberti, G. (1984). The contribution of comparative spermatology to problems of acarine systematics. In ‘Acarology VI.’ (Eds D. A. Griffiths and C. E. Bowman.) vol. 1, pp. 479–490. (Ellis Horwood Ltd: Chichester, England.) Alberti, G. (1988). Genital system of Gamasida and its bearing on phylogeny. In ‘Progress in Acarology’. (Eds G. P. Channabasavanna and C. A. Viraktamath.) vol. 1, pp. 197–204. (Oxford & IBH Publishing Co. Pvt Ltd: New Delhi.) Alberti. G. and Hänel, H. (1986). Fine structure of the genital system in the bee parasite, Varroa jacobsoni (Gamasida: Dermanyssina) with remarks on spermiogenesis, spermatozoa and capacitation. Experimental and Applied Acarology 2, 63–104. Andrews, J. H. R. (1983). The origin and evolution of host associations of Sarcoptes scabiei and the subfamily Sarcoptinae Murray. Acarologia 24, 85–94. Andrews, J. H. R., and Desch, C. E. (1983). The morphology, life history, and habitat of Sarcoptes scabiei. In ‘Cutaneous Infestations of Man and Animals.’ (Eds L. Parrish, W. B. Nutting and R. M. Schwartzman) pp. 53–69. (Praeger Publishers, New York.) Buxton, P. A. (1921). The external anatomy of Sarcoptes of the horse. Parasitology 13, 114–145. Desch, C. E., Andrews, J. R. H., and Arlian, L. G. (1991). The digestive system of Sarcoptes scabiei (L.): light and electron microscope study. In ‘Modern Acarology.’ (Eds F. Dusbábek and V. Bukva.) vol. 1, pp. 271–279. (Academia: Prague, SPB Academic Publishing bv: The Hague.) Fain, A. (1968). Etude de la variabilité de Sarcoptes scabiei avec une révision des Sarcoptidae. Acta Zoologica et Pathologica Antverpiensa 47, 1–196. Fimiani, M., Mazzatenta, C., Alessandrini, C., Paccagnini, E., and Andreassi, L. (1997). The behaviour of Sarcoptes scabiei var. hominis in human skin: an ultrastructural study. Journal of Submicroscopic Cytology and Pathology 29, 105–113. Heilesen, B. (1946). Studies on Acarus scabiei and scabies. Acta DermatoVenereology (Supplementum) 14, 1–370. Juhlin, L., Brunk, U., and Fredriksson, B. A. (1975). Scanning electron microscopy of Acarus scabiei. Acta Dermato-Venereology 55, 35–37. Mazzini, M. and Baiocchi, R. (1983). Fine morphology of the egg-shell of Sarcoptes scabiei (L.) (Acarina: Sarcoptidae). International Journal of Parasitology 13, 469–473.

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Clifford E. Desch Pascual, A. M., Asensio, A., and Vazquez, R. (1977). Morphologie du Sarcoptes scabiei (variété hominis) au microscope électronique à balayage. Annales de Dermatologie et de Venereologie 104, 719–723. Reger, J. F. (1971). An unusual membrane organization observed during spermatogenesis in the mite Caloglyphus anomalus. Journal of Ultrastructure Research 36, 732–742. Richardson, K. G., Jarett, L., and Finke, E. H. (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technology 35, 313–323. Sato, T. (1968). A modified method of lead staining of thin sections. Journal of Electron Microscopy 17, 158–159. Spurr, A. R. (1969). A low viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research 26, 31–43. Stone, W. B., Parks, E., Weber, B. L., and Parks, F. J. (1972). Experimental transfer of sarcoptic mange from red foxes and wild canids to captive wildlife and domestic animals. New York Fish and Game Journal 19, 1–11. Tullar, B. F. and Berchielli, L. T. (1981). Population characteristics and mortality factors of the red fox in central New York. New York Fish and Game Journal 28, 138–149.

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Walzl, M. G. (1992). Ultrastructure of the reproductive system of the house dust mites Dermatophagoides farinae and D. pteronyssinus (Acari, Pyroglyphidae) with remarks on spermatogenesis and oogenesis. Experimental and Applied Acarology 16, 85–116. Witalin´ski, W. (1988). Spermatogenesis and postinseminational alterations of sperm structure in a sarcoptid mite, Notoedres cati (Hering) (Acari, Acaridida, Sarcoptidae). Acarologia 29, 411–421. Witalin´ski, W. (1993). Egg shells in mites: vitelline envelope and chorion in Acaridida (Acari). Experimental and Applied Acarology 17, 321–344. Witalin´ski, W. and Afzelius, B. A. (1987). Spermatogenesis in an itch mite, Sarcoptes scabiei (L.) (Acari, Sarcoptidae). Journal of Submicroscopic Cytology 19, 615–625. Witalin´ski, W., Jon´czy, J., and Godula, J. (1986). Spermatogenesis and sperm structure before and after insemination in two acarid mites, Acarus siro L. and Tyrophagus putrescentiae (Shrank) (Acari, Astigmata). Acarologia 27, 41–51. Witalin´ski, W., Szlendak, E., and Boczek, C. (1990). Anatomy and ultrastructure of the reproductive systems of Acarus siro (Acari: Acaridae). Experimental and Applied Acarology 10, 1–31.

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

THE USE OF AUTOFLUORESCENCE OF THE PHARYNGEAL PUMP COMPLEX IN PYGMEPHORIDAE (ACARI: HETEROSTIGMATA) AS A NEW TAXONOMIC AID

University of the Witwatersrand, Private Bag 3, Wits 2050, South Africa. 1) Electron Microscope Unit, [email protected]; 2) School of Animal, Plant and Environmental Sciences, [email protected]

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S. H. Coetzee 1 and A. M. Camerik 2

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Abstract We propose the use of confocal laser scanning microscopy (CLSM) to examine the shape of the pharyngeal pump complex in Pygmephoridae in order to distinguish among different genera and to distinguish among closely related species within genera. Heavily sclerotised structures in the exoskeleton obscure the real shape of the pharyngeal pump complex when using conventional light microscopy. The shape of examined pharyngeal pumps depended on the orientation of the gnathosoma of the mites after mounting. However, by making use of the muscular pharyngeal pump units that autofluoresce when illuminated with light of the correct wavelength, one is now able with CLSM to compile 3D virtual images of these structures and rotate them about different axes in order to determine their real shape.

INTRODUCTION Recently Camerik and Coetzee (1997, 1998) published the first confocal laser scanning microscope (CLSM) images of the autofluorecent pharyngeal complex pump system of Pygmephoridae. Cross (1965) and Suski (1983) previously employed light microscope (LM) images of these structures to distinguish among some genera in Pyemotidae, and Lindquist (1973, 1986) employed differential interference contrast photomicrographs to discuss their potential diagnostic value in Tarsonemidae. For technical reasons, these pumps have traditionally been ignored as a taxonomic tool in Pygmephoridae. Within this family, new species were mainly described by the characteristics of the exoskeleton of phoretic females. Their heavily sclerotised exoskeletons frequently obscure the pumps in question. Moreover, the apparent shape of the pump is dependent on the angle at which they are observed. In Pediculaster species, for example, the first pump is usually situated in the hypognathous gnathosoma. The angle at which the gnathosoma is tilted often prevents the observer from seeing its actual shape through the LM. In addition, the LM is limited by both its depth of field and resolution. Information

from out-of-focus planes, e.g. the exoskeleton, obscures the fine detail of the pumps in the in-focus plane. In contrast to the LM, the CLSM uses monochromatic wavelength-specific laser beams to excite the autofluorescing pharyngeal pump complex. A pinhole in the backfocal plane of the image in the CLSM allows an optical, in-focus, thin section of the object (Pauly 1995). Since laser beams are wavelength-specific, no pre-sample filters are needed. Optical sections of the object are taken in sequence and rendered into a 3D volume (US. Pat. 4,63,581). This volume can be rotated through any angle to obtain a clear visualisation of the real shape of the pump (Fig. 1). In addition, the 3D volume can be resectioned in any direction and any angle in order to obtain a clear 2D image. To obtain an interference-free image, unwanted frequencies from the emission spectrum of the object can be excluded by a set of Long Pass (LP) filters.

MATERIALS AND METHODS A. M. Camerik collected mite specimens from Cluny Boekenhoutskloof near Johannesburg and on the Innesfree farm at Sandton, Johannesburg, South Africa. The mites were identified by 213

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Figure 1

P. morelliae, rotation sequence of the through focus CLSM images of pharyngeal pump 1.

H. Dastych, A. M. Camerik, A. Fain, and G. Rack. The mites were preserved in 70% ethanol, cleared in lacto-phenol, mounted in Berlese mounting fluid, dried for at least 48 hours at about 40°C and ringed. The coverslips were pressed down gently onto the mites in order to retain their natural 3D morphology. When the coverslips were pressed down too strongly, standard procedure for convention LM sample preparation, the exoskeleton was displaced and often interfered with the optical sectioning. Due to the short working distance of the objective lens, it is important to mount the specimen as closely as possible to the coverslip and leave a gap between the mite and the microscope slide. Therefore, it is advisable to mount the mite on the coverslip rather than the glass slide. The optical sections of the pharyngeal pumps were collected with a Zeiss CLSM 410 using a 63/1.4 oil immersion objective. The

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pharyngeal pump complex autofluoresced at 488 nm and 568 nm wavelengths or a combination thereof. Unwanted emission wavelengths were removed with LP 515 nm or LP 590 nm filter sets. A clear image of the pump(s) (three in Pediculaster species) could be obtained in most cases using the optical sectioning capability and magnification zoom feature of the CLSM.

RESULTS AND DISCUSSION Using the CLSM as described above, we were able to discriminate between three different Pediculaster species, and we could also distinguish between different genera. We collected and reconstructed a through-focus series of images of the first pharyngeal pumps of P. morelliae, P. gautengensis and P. mesembrinae. The gnathosoma of the mounted specimen of P. morelliae was tilted vertically with respect to the body. When the pharyngeal pump

THE USE OF AUTOFLUORESCENCE

OF THE PHARYNGEAL PUMP COMPLEX IN

PYGMEPHORIDAE

Figures 2.1–2.9 P. morelliae, transmitted laser light DIC image of pharyngeal pump 1. Fig. 2.2. P. gautengensis transmitted laser light DIC image of pharyngeal pump 1. Fig. 2.3. P. mesembrinae transmitted laser light DIC image of pharyngeal pump 1. Fig. 2.4. P. morelliae, through focus CLSM image of pharyngeal pump 1. Fig. 2.5. P. gautengansis through focus CLSM image of pharyngeal pump 1. Fig. 2.6. P. mesembrinae through focus CLSM image of pharyngeal pump 1. Fig. 2.7. P. morelliae, through focus CLSM image of pharyngeal pumps 2 and 3. Fig. 2.8. P. gautengensis through focus CLSM image of pharyngeal pumps 2 and 3. Fig. 2.9. Microdispus through focus CLSM image of pharyngeal pumps 2 and 3.

was observed through a LM, in the laser light differential interference contrast (DIC) image, the shape of the pharyngeal pump appeared similar to that of P. mesembrinae (Figure 2.1 and Fig 2.3), and not P. gautengensis. Comparing the CLSM images of the same pharyngeal pumps (Figure 2.4–2.6) with a 3D rotated image of the pharyngeal pump of P. morelliae, the pharyngeal

pump shape resembled that of P. gautengansis rather than P. mesembrinae. This finding enabled definitive discrimination to be achieved between the three species when the real shapes are compared. The same technique was used to differentiate between genera. Pharyngeal pumps 2 and 3 are more alike within the same genus than between different genera. This becomes obvious when

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one compares the shapes of the pharyngeal pumps of P. morelliae with those of P. gautengensis sp. and Microdispus sp. (Fig 2.7–2.9).

REFERENCES Camerik, A. M., and Coetzee, S. H. (1997). The phoretic female of Pediculaster australis spec. nov. (Acari: Pygmephoridae) from South Africa and new synonyms for P. morelliae Rack 1975. Bulletin de L’ Institut Royal des Sciences Naturelles de Belgique: Entomology 67, 33–43. Camerik, A. M., and Coetzee, S.H. (1998). The phoretic females of two new species belonging to the genus Pediculaster (Acari: Pygmephoridae) from cattle dung in South Africa. International Journal of Acarology 24, 21–31. Cross, E. A., (1965). The generic relationships of the family Pyemotidae (Acarina: Trombidiformes). The University of Kansas Science Bulletin. 45, 29–275.

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Lindquist, E. E. (1973). Observations on the generic classification of tarsonemid mites (Prostigmata). In ‘Proceedings of the Third International Congress of Acarology, (Prague)’. (Eds M. Daniel and B. Rosiky.) pp. 293–295. (W. Junk: The Hague.) Lindquist, E. E. (1986). The world genera of Tarsonemidae (Acari: Herostigmata): A Morphological, phylogenetic, and systematic revision, with a reclassification of family-group taxa in the Heterostigmata. Memoirs of the Entomological society of Canada 136, 1–517. Pauly J. B. (1995). ‘Handbook of Biological Confocal Microscopy’. 2nd ed. (Plenum: New York.) Suski, Z. W. (1983). Structures associated with the esophagus and their taxonomical significance in grass mites siteroptes sp. (Acarina, Pygmephoridae). Polskie Pismo Entomologiczne 53, 405–410.

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

FUNCTIONAL MORPHOLOGY OF SOME LEG SENSE ORGANS IN PEDICULASTER MESEMBRINAE (ACARI: SITEROPTIDAE) AND PHYTOPTUS AVELLANAE (ACARI: PHYTOPTIDAE)

Dipartamento di Biologia e Chimica Agroforestale e Ambientale, Università degli Studi di Bari via Amendola, 165/A – 70126 Bari, Italy

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Enrico de Lillo, Pasquale Aldini

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Abstract Some of the sense organs on the tibio-tarsus of leg I of a phoretomorphic female of Pediculaster mesembrinae (Canestrini) (Pygmephoroidea: Siteroptidae) and on tarsi I and II of Phytoptus avellanae Nalepa (Eriophyoidea: Phytoptidae) were studied using transmission and scanning electron microscopy. The siteroptid solenidial shaft consists of a multiporous wall enclosing several dendritic branches. Its sensory components include a varying number of neurons depending on the particular solenidion on the leg. No tubular bodies are associated with this sensory structure. By contrast, the shaft of the phytoptid solenidion has very small apical pores and an aporous outer surface along its length. The solenidion on tarsus I has four neurons, and that on tarsus II has three. The outer dendritic segments are unbranched, penetrate the shaft and run up to its apex. As with the siteroptid, no tubular bodies are associated with this structure. These ultrastructural features are consistent with a chemoreceptive role involved in mite trophic activity and behaviour. In particular, the phytoptid solenidion is assumed to be gustatory, while an olfactory role is suggested for the structurally different siteroptid solenidion. In addition, ultrastructural descriptions are given for the tarsal setae and the empodium of P. avellanae, which have mechanoreceptive roles.

INTRODUCTION Current knowledge of the sensory receptors of Acari comes mainly from research on ticks (Ixodida) in which their function has been recognised, in most cases, by means of electrophysiological investigations and supported by ultrastructural studies. By contrast, few studies on these structures have been carried out on other Acari (Baker 1984, 1996; Alberti et al. 1994; Leonovich 1994; de Lillo et al. 1996; Alberti 1998; see other references in Nuzzaci 1994, 1995 and Alberti and Coons 1999), and many of them require further investigation. Knowledge of solenidia is based mainly on optical and external morphological observations and the studies of this sensory organ on Rhizoglyphus robini Claparède (Acaridida: Acaridae) by Baker

(1985), on chiggers (Trombiculidae) by Leonovich (1994), and on water mites (Hydrachnida) by Baker (1996). These studies support the hypothesis of a chemoreceptive function, as presented by Evans (1992). To gain further insight into the role of the solenidia in mycophagous and phytophagous mites, the present paper deals with the fine structure of the solenidia on the tibio-tarsus of leg I in a phoretomorphic female of Pediculaster mesembrinae (Canestrini) (Siteroptidae) and on the tarsus of legs I and II in adults of Phytoptus avellanae Nalepa (Phytoptidae). Non-solenidial sensilla on the phytoptid tarsi were also examined. In addition, the functions of these sensilla are discussed on the basis of the ultrastructural features which they share with similar organs that are well known in other arthropods.

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1

2

w2

WP

w1 ø2 ø1

WP

3

WP

k oD Cu

Figures 1–3

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Pediculaster mesembrinae (Canestrini): 1) scanning electron micrographs of tibio-tarsus I; 2-3) transmission electron micrographs of a solenidion on tibio-tarsus I: 2) tangential section showing smooth rings and slit whorls alternately placed on the shaft, 3) detail of a transverse section showing branched dendrites. CU, cuticle; k, pore kettle; oD, outer dendritic segments; w1, w2, ø1, ø2, solenidia; WP, wall pores. Bars = 10 µm for Fig. 1, 0.5 µm for Figs 2–3.

FUNCTIONAL MORPHOLOGY

WP

4

OF SOME LEG SENSE ORGANS IN

PEDICULASTER MESEMBRINAE

5

AND

PHYTOPTUS AVELLANAE

7 DB

HS

DS DB

Cu

HS 6 8

PT

HS

WP Cu CS

DS oD

Figures 4–8

M

Transmission electron micrographs of solenidia in Pediculaster mesembrinae (Canestrini): 4) sagittal and 5) oblique sections of solenidial shaft, 6) detail of a solenidial sagittal section; 7) longitudinal section of a solenidion showing the cellular components in the shaft lumen and its ciliary sinus; 8) detail of a ciliary sinus. CU, cuticle; DB, dendritic branches; DS, dendritic sheath; HS, solenidial shaft; M, mitochondrion; MT, microtubules; OD, outer dendritic segments; PT, pore tubules; WP, wall pores. Bars = 0.5 µm.

MATERIALS AND METHODS Live phoretomorphic females of P. mesembrinae, collected from mushroom substrates of Pleurotus eryngii (D.C. ex Fr.) Quél. infested by Trichoderma viride Pers., and living specimens of P. avellanae, collected from infested buds of Corylus avellana L., were used for transmission electron microscopy. The same methods were applied to both species. The body was dissected using a scalpel and the anterior part was fixed in Karnowsky’s fixative, rinsed in cacodylate buffer, postfixed in 1% buffered osmium tetroxide, rinsed as above, dehydrated in ethanol and embedded in Araldite M. Ultrathin transverse and longitudinal (only for

P. mesembrinae) sections of legs were cut using a diamond knife on an ultratome III LKB 8800, stained with 5% uranyl acetate and lead citrate, observed and micrographed using a Zeiss EM109T transmission electron microscope. Observations by means of a stereoscan Cambridge S100 were made on freshly killed specimens of P. mesembrinae, Aculops lycopersici (Massee) (Eriophyidae) and Diptacus hederiphagus Nuzzaci (Rhyncaphytoptidae). The description of fine structure and the classification of the observed sensilla were based primarily on Grandjean (1935), Altner and Prillinger (1980), Zacharuk (1985), and Solinas (1995).

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9 10 Cu So

CS

HS cD Cu Figures 9–10

Transmission electron micrographs of solenidia in Pediculaster mesembrinae (Canestrini): 9) oblique section at solenidial socket level; 10) transverse section at level of ciliary constrictions. cD, ciliary constriction; CS, ciliary sinus; CU, cuticle; HS, solenidial shaft; So, socket. Bars = 0.5 µm.

RESULTS Solenidia on tibio-tarsus of first legs in Pediculaster mesembrinae

Phoretomorphic females of P. mesembrinae have a fused tibiotarsus on leg I which is provided with 2 tarsal (w2 and w1) and 2 tibial (ø1 and ø2) solenidia (Fig. 1). The solenidial shaft seems to be rigid, straight and smooth-surfaced in scanning electron microscope (SEM) examination at low magnification (Fig. 1). Solenidia w1, ø1 and ø2 are distally about twice as wide as proximally (clavate), while w2 is almost constant in diameter along its length (baculiform). The apex of each is always rounded and does not form a knob (Fig. 1). Transmission electron microscopical (TEM) examinations of sections of the solenidial shaft reveals multiporous cuticular walls (Figs 2–3). In tangential sections, the pores look like slits which are parallel to the shaft axis and closely appressed to each other (Fig. 2). The outer part of the shaft wall shows an electrondense layer (L3, see Steinbrecht 1997) which is interrupted by pores, pore kettles connected to the pores, and an electronlucent material filling the pores and the kettles (Fig. 3). The slits are arranged in whorls (variable in number depending on solenidial length) which are stacked along the shaft axis. Each slit whorl is separated from the contiguous one by a smooth and entire cuticular ring (Fig. 2) whose wall is thickened (Fig. 4). Within the slit whorl level, the cuticular walls protrude slightly into the shaft lumen (Fig. 5). The alternation of smooth cuticular rings with slit whorls, which are so different in structure, gives a transversely striated appearance to the surface of the shaft when it is observed with light microscopy. Sections at the level of the slit whorl reveal connections between pores and shaft lumen by means of pore tubules (Fig. 6), which are difficult to observe in mites that are chemically fixed (see Steinbrecht 1997). The shaft lumen is surrounded by a single cuticular wall and is innervated by several dendritic branches (Figs 4, 6–7). Microtubules are evident in the branched dendrites (Figs 3, 5). More proximally, just under the insertion of the solenidion on the tibio-tarsus, the outer dendritic segments

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are surrounded by a dendritic sheath (Fig. 8). The base of the shaft is inserted into the tibio-tarsus cuticle where it is delimited by a short rim (Figs 1, 9). At this level, the cuticle displays a more electrondense outermost layer while a fibrillar area lies between the shaft base and the tibio-tarsus cuticle (Fig. 9). Going proximally, transverse serial sections show the gradual disappearance of the dendritic sheath while at least two ciliary constrictions appear in a ciliary sinus filled with an electronlucent liquor (Fig. 10). It was not possible to determine the exact number of ciliary constrictions per solenidion. The ciliary sinus extends into a deep labyrinth (Fig. 10) that reaches the perinuclear region of the sensory neuron bodies. The difficulty of correctly orientating the frontal section prevented our establishing the exact number of microtubules per ciliary constriction. Only one sheath cell has been found surrounding the dendritic sheath from the base of the shaft until the ciliary sinus. Unfortunately, it was not possible to describe separately the ultrastructure of each solenidion even if it was evident that different solenidia on tibio-tarsus have different properties. Solenidion and other sensory structures on leg tarsi of Phytoptus avellanae

The common set of sense organs on the tarsi of eriophyoid mites consists of a subdistal, dorsal solenidion (w), a distal empodium (e), which has a single or divided shaft with few to several rays (depending on the species), a subdistal, ventral minute unguinal seta (u’) and two proximal, subdorsal fastigial setae (ft’ and ft’’) (Lindquist 1996) (Figs 11–12). The solenidion is very close and usually dorsal to the distal empodium. A tibial solenidion (ø) is less frequently present in some genera of the family Phytoptidae. In P. avellanae, the solenidial shaft (Fig. 13) is rigid and slender and has a smooth outer surface. It is about 12 µm long, gradually tapers to the tip, and curves slightly along its proximal part. The apex is blunt and developed into a small knob as in other species, such as D. hederiphagus and A. lycopersici (Figs 11–12) in which the knob is more developed.

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w

11

AND

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13

TiS

ft

e

Ta

Ti

GeS

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w

Ge

u'

Fe

e

14

12

ft

15 w

Figures 11–15

P

e

11–12) Scanning electron micrographs of leg I in: 11) Diptacus hederiphagus Nuzzaci, 12) Aculops lycopersici (Massee); 13) semischematic drawing of tarsus I in Phytoptus avellanae Nalepa; 14–15) transmission electron micrographs of the solenidion on the legs of Phytoptus avellanae Nalepa: 14) apical transverse section showing a pore and a canal system (arrows), 15) subapical transverse section. e, empodium; Fe, femur; ft, fastigial setae; Ge, genu; GeS, genual seta; P, pore; Ta, tarsus; Ti, tibia; TiS, tibial seta; u', unguinal seta; w, solenidion. Bars = 2 µm for Figs 11–12, 0.1 µm for Figs 14–15.

In transverse sections examined by TEM, no pores occur along the shaft wall, whereas the apex is provided with a complex pore system connected with pore tubules (Figs 14–15). The pores are not visible in SEM. In subdistal sections, just below the porous apical area (Fig. 16), the shaft wall is provided with an outer, very

thin, electrondense layer, followed by a wider, less electrondense layer and, almost centrally, an amorphous and granulose electrondense substance. In more proximal sections, the solenidial shaft shows a cuticular wall with a central lumen appressed to the amorphous substance. Inside this lumen there are, on legs I and

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16

19 oD

Cu Ta

So

e

17 MT

20 cD

oD

CS 18

Cu

21 M oD iD

Figures 16–21

Transmission electron micrographs of solenidion on the legs of Phytoptus avellanae Nalepa: 16) subdistal and 17) intermediate transverse sections of the solenidial shaft (leg II), 18) distal transverse section of tarsus II showing the outer dendritic segments running towards the solenidion, 19) subdistal transverse section of tarsus II showing the empodium at socket level and of the solenidial sensillar sinus, 20) more proximal section showing three ciliary constrictions (leg II) belonging to the solenidial sensory neurons, 21) inner dendritic segments of the solenidion (leg I). cD, ciliary constriction; CS, ciliary sinus; CU, cuticle; e, empodium; iD, inner dendritic segments; M, mitochondrion; MT, microtubules; oD, outer dendritic segment; So, socket; Ta, tarsus. Bars = 0.1 µm for Figs 16–17, 0.5 for Figs 18–21. Note for Fig. 17: no resin filled the shaft lumen, so the gray in the latter is an artifact.

II respectively, four and three outer dendritic segments that extend into the tarsus (Fig. 17). The outer dendritic segments are unbranched, are immersed in an electronlucent matrix, display several microtubules and are surrounded by a thick cuticular wall (Fig. 18). Inwards, at the distal part of the tarsus, the sensillar sinus (Fig. 19) is crossed by the outer dendritic segments encased in a dendritic sheath. The solenidial shaft appears to arise directly from the tarsal cuticle. Going proximally, the dendritic sheath

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ends in the ciliary sinus, which extends into a labyrinth filled with an electronlucent liquor. The ciliary regions of four (leg I) and three dendrites (leg II) (Fig. 20) are evident in the ciliary sinus. It was not possible to exactly establish the microtubule arrangement. More proximally, four or three inner dendritic segments were observed (Fig. 21) in continuation with the ciliary regions. No tubular body associated with this sensillum was detected. Only one sheath cell surrounds the dendritic sheath from the base

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AND

PHYTOPTUS AVELLANAE

25

22 SS ML oD

Tb

23 e

26

ft

So Ta Tb

24 Figures 22–27

27

Tb

u'

Cu

Transmission electron micrographs of the leg tarsus of Phytoptus avellanae Nalepa: 22) sensillar sinus of the solenidion, 23) transverse section of the empodium, 24) detail of the empodium tubular body, 25) detail of the empodium and seta u’ tubular body; 26) socket and hair shaft base for ft setae; 27) detail of the tubular body of a ft seta. CU, cuticle; e, empodium; ft, fastigial seta; ML, microlamellae; oD, outer dendritic segment; SO, socket; SS, sensillar sinus; Ta, tarsus; TB, tubular body. Bars = 0.5 µm.

of the shaft (Fig. 22) to the ciliary sinus, though it has more than one fold. The cuticular component of the empodium consists of a rigid hair about 8 µm long, provided with a main axis which is branched into 5 sharp-tipped rays (Fig. 13). The shaft and its rays have aporous walls and the lumen is not innervated (Fig. 23); the shaft is inserted in a very deep socket surrounded by a rim (Fig. 19). The shaft base is connected with an outer dendritic segment which terminates with a tubular body located very deep in the tarsus and below the shaft base. The microtubules appear immersed in a moderately electrondense matrix and the bundle appears surrounded by an electronlucent area (Figs 24–25). It is encased in a thick, electrondense dendritic sheath and surrounded by a layer of a fibrous cuticle (Figs 24–25). Semicircular elements occur on the dendritic sheath facing the tubular body. No sheath cells have been recognised. The cuticular components of the other tarsal setae consist of a hair-like shaft which is short (unguinal seta) or attenuated (fastig-

ial setae) (Fig. 13); the shafts have aporous walls and their lumina are not innervated. The hair shafts arise from a discrete flexible socket surrounded by a rim (Fig. 26). The shaft base of the unguinal seta is innervated by one sensory neuron whose outer dendritic segment ends with a tubular body (Fig. 25). The shaft base of each fastigial seta is innervated by two sensory neurons whose outer dendritic segments terminate with tubular bodies (Fig. 27). The outer tubular body is larger than the inner. The outer dendritic segments of the unguinal and fastigial setae are individually encased in a thick and electrondense dendritic sheath. Neither sheath cells nor ciliary sinus has been observed.

DISCUSSION AND CONCLUSIONS Optical and external morphological criteria are not enough to describe the solenidia in siteroptid and phytoptid mites because they ignore internal structural features of functional relevance. Although the solenidia of both species are isotropic, they are of two different types, based upon clear differences in cuticular and cytological characteristics.

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The ultrastructural details of the cuticular components in the solenidia of P. mesembrinae, presented in this work, indicate that it is a wall pores-single walled (wp/SW) sensillum sensu Steinbrecht (1984) or a sensillum basiconicum sensu Schneider (1964).

and cellular components resemble those of other arachnid mechanoreceptors (McIver 1975). With respect to their position, it seems likely they perceive mechanical stimuli on contact with the substrate during locomotion.

Whilst chemoreceptive activity in a solenidion is yet to be determined by means of electrophysiological experiments, ultrastructural evidence, such as the presence of multiporous walls and a shaft lumen enclosing branched dendrites, is consistent with an olfactory function. From an ecological-behavioural point of view, this sensillum is strategically located on the tibio-tarsus, especially that of legs I, for the uptake of chemical signals.

The legs of P. avellanae, and many other eriophyoids, are equipped with only one chemoreceptor (the tarsal solenidion) and several mechanoreceptors (setae on tarsus, genu and femur, personal observations) and thus appear to be ideal for electrophysiological studies of the function of the solenidion. In fact, an entire leg could be considered a chemoreceptive organ and this would reduce the technical difficulties of dealing with a single sensillum.

Since the ultrastructure of solenidia of other mites is so poorly known, only a partial comparison can be made with those found in P. mesembrinae. The external and internal morphological features described above are partly similar to those described for Rhizoglyphus robini (Baker 1985), trombiculid mites (Leonovich 1994) and oribatids (Alberti 1998). Sensilla having a probable chemoreceptive function have been found in the stylets of Tetranychoidea (Nuzzaci and de Lillo 1989, 1991a), in the digitus mobilis of Penthaleus major (Dugès) (Nuzzaci and de Lillo 1991b; Di Palma 1995), and in the chelicera of Eriophyoidea (Nuzzaci and Alberti 1996; personal observations). However, these have a different ultrastructure. A gustatory function has been strongly suggested for the preoral groove sensilla in Tetranychoidea (Nuzzaci and de Lillo 1989, 1991a). Several reports and detailed accounts of olfactory sensilla are available for anactinotrichid mites (Coons and Axtell 1973; Jagers op Akkerhuis et al. 1985; De Bruyne et al. 1991), and the solenidia of P. mesembrinae are partly similar to multiporous sensilla in Haller’s organ on the foreleg tarsus of the Ixodida (Hess and Vlimant 1986). Nuzzaci and Alberti (1996) stated that the solenidial shaft in eriophyoid mites contains several dendrites and they suggested a probable chemoreceptive function; no mention was made of the other structures. Based on our observations of the ultrastructural characteristics of the cuticular components, the phytoptid solenidion is assumed to be a sensillum with a terminal pore system (TP-sensillum) sensu Steinbrecht (1984) and is considered a sensillum basiconicum sensu Schneider (1964). No evidence was found of a tubular body at the solenidial base. Moreover, its fine structure does not match that of P. mesembrinae and its shaft contains unbranched outer dendritic segments going to the shaft apex. The sensillum is dorsally and subdistally located on the tarsus and lays very close to the empodium. From its position near the tip of the tarsus and its structure, it is thought to be a gustatory chemoreceptor. It appears to be the first chemosensillum to come in contact with the substrate during locomotion, even before other chemoreceptors located on chelicerae and subcapitulum (personal observations). It probably plays an important role in trophic behaviour although involvement in pheromonal perception cannot be excluded. The structural aspects of the empodium, unguinal and fastigial setae are consistent with the descriptions of known cuticular mechanosensilla belonging to the hair-shaped type called sensilla trichoidea sensu Schneider (1964) and they are aporous sensilla (NP-sensilla) sensu Steinbrecht (1984). Moreover, the cuticular

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It is clear that the general classification of F. Grandjean (solenidia, setae, eupathidia, famuli) (1970), which is almost universally applied to setiform sensilla of actinotrichid mites, cannot be used to infer a specific use. We agree with G. O. Evans (in litteris) that it is essential to accumulate much more comparative information on the fine structure and function of such sensilla, from a variety of mite groups, before meaningful generalisations can be made.

ACKNOWLEDGEMENTS This research was partly supported by MURST and MAF [Miglioramento della produzione del cardoncello (Pleurotus eryngii)] grants. We are grateful to Prof. H. Dastych (Germany) for the siteroptid identification, Profs. G. Alberti (Germany), J. W. Amrine Jr. (U.S.A.), G. O. Evans (United Kingdom), E. E. Lindquist (Canada), G. Nuzzaci (Italy), M. Solinas (Italy), and R. A. Steinbrecht (Germany) for their helpful critical comments. The senior author has planned the research, analysed and interpreted the observations; the junior author has mainly provided for the preparation of the iconographic materials.

REFERENCES Alberti, G., and Coons, L. B. (1999). Acari – Ticks. In ‘Microscopic Anatomy of Invertebrates’ (Ed F. W. Harrison.), Vol. 8B, pp. 267–514. (Wiley & Sons: New York.) Alberti, G., Moreno, A. I., and Kratzmann, M. (1994). The fine structure of trichobothria in moss mites with special emphasis on Acrogalumna longipluma (Berlese, 1904) (Oribatida, Acari, Arachnida). Acta Zoologica, Stockholm 75, 57–74. Altner, H., and Prillinger, L. (1980). Ultrastructure of invertebrates chemo-, thermo-, and hygroreceptors and its functional significance. International Review of Cytology 67, 69–139. Baker, G. T. (1985). Morphology of the solenidia and famulus on tarsi I and II of Rhizoglyphus robini Claparède (Acarida). Zoologische Jahrbücher Anatomische 113, 85–89. Baker, G. T. (1996). Chemoreception in four species of water mites (Acari: Hydrachnida): behavioural and morphological evidence. Experimental and Applied Acarology 20, 445–455. Coons, L. B., and Axtell, R. C. (1973). Sensory setae of the first tarsi and palps of the mite Macrocheles muscaedomesticae. Annals of the Entomological Society of America 66, 539–544. de Bruyne, M., Dicke, M., and Tjallongii, T. F. (1991). Receptor cell responses in the anterior tarsi of Phytoseiulus persimilis to volatile kairomone components. Experimental and Applied Acarology 13, 53–58. de Lillo, E., Nuzzaci, G., and Aldini, P. (1996). Fine morphology of the mouthpart sensilla in females of Typhlodromus exhilaratus Ragusa (Phytoseiidae). In ‘Acarology IX. Proceedings.’ (Eds R. Mitchell, D. J.

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Horn, G. R. Needham and W. C. Welbourn.) pp. 287–295. (Ohio Biological Survey: Columbus.) Di Palma, A. (1995). Morfologia funzionale delle parti boccali di Penthaleus major (Dugés) (Eupodoidea: Penthaleidae). Entomologica, Bari 29, 69–86. Evans, G. O. (1992). ‘Principles of Acarology.’ (CAB International: Wallingford.) Grandjean, F. (1935). Les poils et les organes sensitif potrés par les pattes et le palpe chez les Oribates. Première partie. Bulletin de la Société Zoologique de France 60, 6–39. Hess, E., and Vlimant, M. (1986). Leg sense organs of Ticks. In ‘Morphology, Physiology, and Behavioural Biology of Ticks.’ (Eds J. R. Sauer and J. A. Hair.) pp. 360–390. (Ellis Horwood: Chichester.) Jagers op Akkherhuis, G., Sabelis, M. W., and Tjallingii, W. F. (1985). Ultrastructure of chemoreceptors on the pedipalps and first tarsi of Phytoseiulus persimilis. Experimental and Applied Acarology 1, 235–251. Lindquist, E. E. (1996). External anatomy and notation of structures. In ‘Eriophyoid Mites: Their Biology, Natural Enemies and Control.’ (Eds E. E. Lindquist, M. W. Sabelis and J. Bruin.) pp. 3–31. (Elsevier: Amsterdam.) Leonovich, S. A. (1994). Morphology of specialized setae on body limbs in chiggers (Trombiculidae). Parazitologiya (St. Petersburg) 28, 445–451. McIver, S. B. (1975). Structure of cuticular mechanoreceptors of arthropods. Annual Review of Entomology 20, 381–397. Nuzzaci, G. (1994). Recenti acquisizioni di morfologia funzionale negli acari. In ‘Atti XVII Congresso Nazionale Italiano di Entomologia.) (Ed. F. Frilli.) pp. 273–286. (Arti Grafiche Friulane: Udine.) Nuzzaci, G. (1995). Acari chemosensilla: structure and function. Atti Accademia Nazionale Italiana di Entomologia, Rendiconti 43, 165–185. Nuzzaci, G., and Alberti, G. (1996). Internal Anatomy. In ‘Eriophyoid Mites Their Biology, Natural Enemies and Control.’ (Eds E. E.

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Lindquist, M. W. Sabelis and J. Bruin.) pp. 101–150. (Elsevier: Amsterdam.) Nuzzaci, G., and de Lillo, E. (1989). Contributo alla conoscenza dello gnatosoma degli acari tenuipalpidi (Tetranychoidea: Tenuipalpidae). Entomologica, Bari 24, 5–32. Nuzzaci, G., and de Lillo, E. (1991a). Fine structure and functions of the mouthparts involved in the feeding mechanisms in Tetranychus urticae Koch (Tetranychoidea: Tetranychidae). In ‘Modern Acarology. Vol. 2’ (Eds F. Dusbabek and V. Bukva.) pp. 301–306. (Academia: Prague.) Nuzzaci, G., and de Lillo, E. (1991b). Contributo alla conoscenza delle parti boccali di Penthaleus major (Dugès) (Acari: Eupodoidea Penthaleidae). Atti XVI Congresso Nazionale Italiano di Entomologia, Bari-Martina Franca, 265–277. Nuzzaci, G., de Lillo, E., and Porcelli, F. (1992). Functional morphology of the mouthpart sensilla in female of Varroa jacobsoni Oudemans (Acari: Varroidae). Entomologica, Bari 27, 41–67. Schneider, D. (1964). Insect antennae. Annual Review of Entomology 15, 121–142. Solinas, M. (1995). Insect olfactory and gustatory sensilla: structure, function, possible peripheral integration. Atti Accademia Nazionale Italiana di Entomologia, Rendiconti 43, 61–163. Steinbrecht, R. A. (1984). Chemo-, hygro- and thermoreceptors. In ‘Invertebrates. Biology of the Integument. Vol. 1’ (Eds A. G. BereiterHahn, A. G. Matoltsy and K. S. Richards.) pp. 523–553. (Springer Verlag: Berlin.) Steinbrecht, R. A. (1997). Pore structures in Insect olfactory sensilla: a review of data and concepts. International Journal Morphology and Embryology 26, 229–245. Zacharuk, R. Y. (1985). Antennae and sensilla. In ‘Comprehensive Insect Physiology Biochemistry and Pharmacology. VI. Nervous system: sensory.’ (Eds G. A. Kerkut and L. I. Gilbert). pp. 1–69. (Pergamon Press: London)

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ULTRASONICATION, A TOOL FOR MICRODISSECTION OF ASTIGMATIC MITES INVESTIGATED BY SEM

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M. G. Walzl Institute of Zoology, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria.

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Abstract After special treatments, such as microwave fixation and enhanced osmification according to the osmium-thiocarbohydrazide-osmium technique, it is possible to separate internal organs of astigmatic mites by treatment in a commercial ultrasonic-cleaner device. Their microanatomy can then be investigated by scanning electron microscopy. This technique is a good tool to demonstrate different organs without large expenditure. A detailed description of the microdissection technique is given and the results are illustrated by means of the nervous, musculatory, digestive and reproductive systems of Glycyphagidae.

INTRODUCTION Precise three-dimensional imaging of biological structures is essential for understanding the structure and function of organisms. Scanning electron microscopy (SEM), which gives a threedimensional picture of surfaces, has been used much in acarology (Woolley 1988; Evans 1992). In order to investigate ‘in situ’ the structure and position of organs situated within the body, it is usually necessary to make a series of thin sections of the objects to be examined and to reconstruct these structures three-dimensionally by means of optical or transmission electron microscopy. These procedures are usually very laborious and time consuming. Techniques to enable a rapid three-dimensional presentation by SEM of surfaces hidden within the body have therefore been sought for a long time. Ultrasonication after special pretreatment of specimens is one technique that can separate different tissues and organs and thereby expose internal structures for SEM. Aldehyde- and osmium fixations, with the help of microwaves, yield the best results (Kok and Boon 1992). Additional increased osmification of the specimens, especially after treatment according to the

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osmium-thiocarbohydrazide-osmium (OTO) technique (Murphy 1978, 1980) produces greater hardness and brittleness in the tissues, which therefore respond to ultrasound action. Commercially available ultrasonic laboratory devices – commonly known as ‘tank cleaners’, produce ultrasonic mechanical vibrations in frequencies varying from 20 to 80 kHz. They are not only useful to remove precipitations but also for selective microdissection of biological tissues (Highison and Low 1982; Highison et al. 1988; Low 1989). Ultrasonic dissection techniques have been used in several investigations of vertebrate (particularly primate) tissues and organs (McClugage and Low 1984; Arnett and Low 1985; Johnson and Highison 1985; Highison and Tibbitts 1986; Rosinia and Low 1986; King and Hossler 1988; McCarthy and Kaye 1990; King1991), but not with invertebrate specimens. Early experiments carried out on house dust mites of the genus Dermatophagoides have shown that this technique yields satisfactory results and leads to a better understanding of the structure of the internal parts of the reproductive system (Walzl 1992). Several species of Glycyphagidae have been selected to elaborate a protocol for visualising internal organs with the ultrasonic microdissection technique.

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Figures 1–5

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Fig. 1. SEM of Glycyphagus domesticus after ultrasonic microdissection. Oesophagus surrounded by the circumoesophagial synganglion . Scale bar 10µm. Fig. 2 SEM of Glycyphagus destructor after ultrasonic microdissection. Striated dorsoventral muscles and leg muscles inserted to the endosternite. Scale bar 20µm. Fig. 3 SEM of Glycyphagus destructor after ultrasonic microdissection. Midgut covered by circular and longitudinal muscle cords. Scale bar 20 µm. Fig. 4 SEM of Glycyphagus destructor after ultrasonic microdissection. Surface of the ovary with bulges of the oocytes. Scale bar 10µm. Fig 5 SEM of Glycyphagus ornatus after ultrasonic microdissection. Inner view of the colon part of the midgut. Cell surfaces with numerous microvilli. Scale bar 5µm.

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MATERIALS AND METHODS Stock cultures of Glycyphagus destructor, G. domesticus and G. ornatus were kept at a temperature of 25°C and a relative humidity of 75%. To prepare for SEM, 100 males and females of each species were kept separately and processed according to the following protocol. 1

2

Primary fixation: Place selected specimens in a vial of transparent microwave material (a pressure-resistant Teflon vial is best) containing 4% aqueous formaldehyde solution. Microwave for 8–10 sec at full power level (e.g. 600 W with the Hoover Micromaster H 6318 household oven used in this experiment). Cool to room temperature (about 20 minutes). Pass through distilled water (three changes, 10 min each). Secondary fixation with the osmiumtetroxide-thiocarbohydrazide-osmiumtetroxide (OTO) technique. Immerse in 1% OsO4 in distilled water (30 min, 20°C). Rinse in distilled water (six times). Immerse in 1% aqueous thiocarbohydrazide (30 min, 20°C). Rinse in distilled water (six times). Immerse in 1% OsO4 in distilled water (30 min, 20°C). Rinse in distilled water (six times). To avoid precipitations it is important to follow these steps precisely. Steps 2–8 can be repeated several times until the specimens are nearly pure metallic.

3

Chemical dehydration with acidified 2,2-dimethoxypropane (2 drops of 1N HCl in 100ml DMP) (Johnson et al. 1976). The temperature will decrease, and the dehydration process is finished when the temperature rises again (about 10 min). DMP reacts with water to produce equal parts of methanol and acetone. Exchange excessive DMP for pure acetone. ( two times, 10 min each).

4

Ultrasonication in a commercial ultrasonic cleaning device (Transonic T460/H with a working frequency of 35 KHz). Dip the glass vials containing the mites into the working ultrasonic cleaner for 1–2 sec. This step can be repeated until the desired stage of microdissection is attained. Exchange for pure acetone. Impregnate specimens three times in hexamethyldisilazane (HMD) (Nation 1983)

5

Mounting: Pipette the specimens together with the HMD under a fume hood into a Petri dish onto a sheet of filter paper and let the HMD evaporate very slowly. For investigation with SEM sputtercoat with gold and/or mount without sputtering on stubs. The best mounting medium is TEMPFIX thermoplastic adhesive.

RESULTS AND DISCUSSION The experiments carried out by ultrasonic microdissection show that it is possible to obtain suitable scanning micrographs of the surfaces of different internal organs of mites. For example, it is possible to expose the exterior of the synganglion which surrounds the cuticularised oesophagus, as well as the location of emerging nerves (Fig. 1). The course and insertions of body muscles can easily be detected (Fig. 2) and the function of individual

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muscles can thus be inferred. Not only the body musculature but also the course of individual muscle fibers of the midgut can be exposed clearly; the longitudinal muscle fibers always lie above transverse fibers (Fig. 3). Ultrasonicated ovaries show very clearly that oocytes bulge the basal lamina of the surface of the ovary (Fig. 4). Prolonged ultrasonication destroys the connection of cells and finally the cells themselves but sometimes it is also possible to give an inner view of hollow organs for example the colon part of the midgut, where the cell surfaces with numerous microvilli can be seen (Fig. 5). Working properly with this technique always yields useful results with astigmatic mites. Osmification hardens the organs, which makes it easy to separate them from other organs by ultrasonication. In addition, the cuticule bursts and the individual organs are exposed for micrographing. Since the section planes do not always coincide with the surfaces of organs, there is some waste of material. For optimal results it is essential to limit the influence of ultrasonic waves by checking the progress of microdissection under the stereomicroscope. If mites are left in the ultrasonic bath too long they will be destroyed. When properly checked, at least 50% of all ultrasonicated mites are usable. After drying on filter paper these may be selected and used for SEM. It is crucial that the steps be followed precisely in order to avoid precipitations. Special attention must be paid to sufficient washing with distilled water when using the OTO-technique, since thiocarbohydrazide not bound to tissue covers the surface as precipitation during succeeding osmification with OsO4. Furthermore, chemical dehydration is preferred over critical point drying, since particles enclosed within a CP-chamber are easily deposited on the surface of the specimens. The principal advantage of the HMD technique is that debris floating in the liquid is washed from the objects onto the filter paper together with the mites.

ACKNOWLEDGEMENTS This study is dedicated to Prof. Dr Eduard Piffl (1921–1998), who introduced me to mites, who always supported me, and who gave me much encouragement. The study was supported by ‘Fonds zur Foerderung der Wissenschaften’ project number 4015. Thanks to E. Walzl-Wegenast for assistance in preparing the manuscript.

REFERENCES Arnett, C. E., and Low, F. N. (1985). Ultrasonic microdissection of rat cerebellum for scanning electron microscopy. Scanning Electron Microscopy 1, 247–255. Evans, G. O. (1992). ‘Principles of Acarology’. (C.A.B. International: Wallingford, UK.) Highison, G. J., and Low, F. N. (1982). Microdissection by ultrasonication after prolonged OsO4 fixation: a technique for scanning electron microscopy. Journal of Submicroscopical Cytology 14, 161–170. Highison, G. J., and Tibbitts, F. D. (1986). Ultrasonic microdissection of immature intermediate human placental villi as studied by scanning electron microscopy. Scanning Electron Microscopy 2, 679–685. Highison, G. J., Johnson, R. B., McClugage, S. G., and Low, F. N. (1988). Ultrasonic microdissection techniques for scanning electron microscopy. CRC Critical Reviews in Anatomical Sciences 1,193–227.

ULTRASONICATION , A TOOL FOR MICRODISSECTION

Johnson, R. B., and Highison, G. J. (1985). Ultrasonic microdissection of the mouse mandible: exposure of the vasculature of alveolar bone and myelinated axons of the pulp. The Anatomical Record 211, 96–101. Johnson, W. S., Hooper, G. R., Holdaway, B. F., Rasmussen, H. P. (1976). 2,2-Dimethoxypropane, a rapid dehydrating agent for scanning electron microscopy. Micron 7, 305–306. King, B. F. (1991). Scanning electron microscopy of primate chorionic villi following ultrasonic microdissection. Placenta 12, 7–14. King, J. A. C., and Hossler, F. E. (1988). The gill arch of the striped bass, Morone saxatilis. III. Morphology of the basal lamina as revealed by various ultrasonic microdissection procedures. Journal of Submicroscopical Cytology and Pathology 20, 371–377. Kok, L. P., and Boon, M. E. (1992). ‘Microwave Cookbook for Microscopists. Art and Science of Visualisation‘. (Coulomb Press: Leiden.) Low, F. N. (1989). Microdissection by ultrasonication for scanning electron microscopy. In ‘Cells and Tissues: A three-Dimensional Approach by Modern Techniques in Microscopy’. (Ed. P. M. Motta.) pp. 571–580. (Alan R. Liss Incorporated: New York.) McCarthy K. J., and Kaye, G. I. (1990). Comparison of osmium/sonication and EDTA/sonication microdissection techniques in exposing the

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adepithelial basal lamina surface in developing rat colon. Journal of Electron Microscopy Technique 14, 367–372. McClugage, S. G., and Low, F. N. (1984). Microdissection by ultrasonication: porosity of the intestinal epithelial basal lamina. The American Journal of Anatomy 171, 207–216. Murphy, J. A. (1978). Non-coating techniques to render biological specimens conductive. Scanning Electron Microscopy 1, 175–193. Murphy, J. A. (1980). Non-coating techniques to render biological specimens conductive; 1980 update. Scanning Electron Microscopy 1, 209–220. Nation, J. L. (1983). A new method using hexamethyldisilazane for preparation of soft insect tissue for scanning electron microscopy. Stain Technology 58, 347–351. Rosinia, F. A., and Low, F. N. (1986). Scanning electron microscopy of the besian ostia (microdissection by ultrasonication: enzymatic digestion). Scanning Electron Microscopy 4, 1363–1369. Walzl, M. G. (1992). Ultrastructure of the reproductive system of the house dust mite Dermatophagoides farinae and D. pteronyssinus (Acari, Pyroglyphidae) with remarks on spermatogenesis and oogenesis. Experimental and Applied Acarology 16, 85–116. Woolley, T. A. (1988). ‘Acarology. Mites and Human Welfare’. (John Wiley and Sons: New York.)

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

FINE STRUCTURE AND MINERALISATION OF CUTICLE IN ENARTHRONOTA AND LOHMANNIOIDEA (ACARI: ORIBATIDA)

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Gerd Alberti1, Roy A. Norton2, and Jörn Kasbohm3 1

University of Greifswald, Greifswald, Germany State University of New York, Syracuse, NY, USA 3 University of Greifswald, Greifswald, Germany 2

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Abstract Cuticular mineralisation by calcium carbonate or calcium oxalate occurs in various primitive and derived taxa of oribatid mites. We applied transmission and scanning electron microscopy to determine the nature of cuticular chambers in certain members of Enarthronota, and the involvement of these chambers in the deposition of minerals. In almost all cases, chambers were associated with the epicuticle and were filled with deposits. In Eniochthoniidae and Mesoplophoridae the chambers form caverns within the epicuticle; they are associated with all hardened cuticle of the body surface, and are clearly the site of calcium oxalate deposition. In Hypochthoniidae (including Nothrolohmannia) chambers are instead modifications of epicuticular indentations above pore canals, and the deposited mineral is calcium phosphate (probably apatite). Distribution of chambers varies within the family. In Hypochthonius they are in patches of various sizes and at various locations on the body and legs, while in Malacoangelia they are more generally distributed. The porose notogastral organs of Malacoangelia and Nothrolohmannia have extended pore canals that contain material similar to that of the chambers. Examined Lohmanniidae have cuticular chambers like those of Hypochthoniidae, and their distribution forms the pattern of transverse bands that has wrongly been considered evidence of primitive segmentation.

INTRODUCTION Two principal functions of the arthropod cuticle are perceived as being related to general or localised hardening. One is support, both for firm attachment of internal structures (e.g. muscles) and for provision of a more or less rigid casing that allows maximum control and efficiency of internal hydraulic actions. The other is protection from external forces, particularly from predators. In either role, hardening can result from two very different processes: sclerotisation, which is the most common, and mineralisation by the deposition of calcium salts. The latter is widespread in several arthropod groups, most notably Crustacea and Diplopoda, in which the hardening derives from calcium carbonate. Mineralisation is rare in insects, being found only in cuticles of some fly larvae (Richards 1951; Neville 1975). Exoskeletons containing calcium carbonate or calcium phosphate are common in the

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extinct Trilobitomorpha and Aglaspidida. The latter are regarded as early Chelicerata (Størmer 1955; Bergström 1979; Müller 1981), but among recent chelicerates (c.f. Dalingwater 1987), cuticular mineralisation is known only from the mite suborder Oribatida (Norton and Behan-Pelletier 1991a), where it must be regarded as apomorphic. Norton and Behan-Pelletier (1991a) used X-ray diffraction methods to demonstrate the presence of two crystalline calcium salts in oribatid mite cuticle. Calcium carbonate (in the form of calcite) was detected in several Ptyctima and the monohydrate calcium salt of oxalic acid (whewellite) was found in three species of Enarthronota (Eniochthonius minutissimus, Archoplophora rostralis, and Prototritia major). Crystalline deposits often result in strong birefringence of the cuticle, and these authors used this fact to infer that in several Phyllozetes species the calcium salts are located as

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Table 1

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Classification, provenance and fixation methods of oribatid mite specimens examined for cuticular mineralisation

Species (all adult specimens)

Family (Superfamily)1

Provenance2

Fixation3

Hypochthonius rufulus C. Koch

Hypochthoniidae (Hypochthonioidea)

Kiel, Germany

glut/OsO4

Malacoangelia remigera Berlese

Hypochthoniidae (Hypochthonioidea)

Florida, USA

ethanol

Eniochthonius minutissimus (Berlese)

Eniochthoniidae (Hypochthonioidea)

Kiel, Germany

glut/OsO4

Archoplophora rostralis Willmann

Mesoplophoridae (Hypochthonioidea)

New York, USA

glut/OsO4

Phyllozetes sp.

Cosmochthoniidae (Protoplophoroidea)

Hawaii, USA

ethanol

Mixacarus sp.

Lohmanniidae (Lohmannioidea)

Manaus, Brazil

glut/OsO4

Nothrolohmannia sp.

see text

Vanimo, New Guinea

ethanol

Explanation: 1) See Balogh and Balogh (1992a). 2) All specimens are from samples of soil or litter, extracted by Berlese-funnels. 3) glut/OsO4 = glutaraldehyde followed by osmium tetraoxide; ethanol = various terms of storage in 70–80% ethanol

thin plates within the epicuticle (Norton and Behan-Pelletier 1991b). Such epicuticular plates were previously known only from Crustacea. Another aspect of oribatid mite cuticular morphology was observed initially without reference to mineralisation. In a comparative study of acarine cuticle, Alberti et al. (1981) used TEM (transmission electron microscopy) to study a peculiar chambered cuticle in hypochthonioid mites. In Hypochthonius rufulus these chambers contained a dense material whereas the chambers of Eniochthonius minutissimus appeared empty. The Hypochthonius chambers were also described by Iordansky (1996), and Bernini et al. (1986) noted similar structures in a species of the confamilial genus Eohypochthonius. It became apparent during our various investigations of oribatid mite cuticle that the chambers were actually sites of mineral deposition. Our objectives herein are to support this idea with data from several microscopy methods, and to make preliminary speculations concerning the possible roles of mineralisation in oribatid mites.

dense homogeneous layer. In species with normal, unchambered cuticle, the distal termination of the pore canal is rather simple (see Alberti et al. 1981, 1997). In contrast, species with chambered cuticle have pore canals with complex terminations (not yet studied in Phyllozetes or Nothrolohmannia). The distal end of the canal forms a cup that partly encloses a deep, globular or almost tubular indentation of the epicuticle. The epicuticle is much thinner in these indentations than in the surrounding areas and the indentation is filled with an unidentified electron-dense material (Figs. 1–4, 6). In all species studied, cuticular chambers are formed in the inner regions of the epicuticle (cuticulin layer plus dense homogeneous layer). This confirms the suspicions of Bernini et al. (1986) and Norton and Behan-Pelletier (1991b) with regard to chambers in Eohypochthonius and Phyllozetes, respectively. Chambers are clearly not located in the procuticle, as was originally suggested by Alberti et al. (1981). However, the exact location, form and contents of the chambers differ strikingly among the species, and two general types can be distinguished.

MATERIALS AND METHODS Table 1 lists the taxa examined in this study and gives the general provenance of specimens as well as the type of fixation. All specimens were adult, and all had localised or extensive regions of chambered cuticle. The principal method of our study was TEM, supported by scanning electron microscopy (SEM) and light microscopy (LM). When possible, the contents of chambers were investigated using energy dispersive x-ray (EDX) analysis. For TEM, specimens were either conventionally stained (see for example Alberti and Nuzzaci 1996) or were studied unstained (see Table 1). Specimens were embedded in Araldite or EMbed 812 respectively, and ultrathin sectioning was performed using Reichert ultramicrotomes. The following electron microscopes were used: TEM (Zeiss EM 10 CR), SEM (Phillips SEM 505, Zeiss DSM 940A), EDX-analysis (Jeol; JEM 1210).

RESULTS As in other arthropods, the oribatid mite cuticle is composed of two principal parts, both secreted by the epidermis. An inner chitinous procuticle is covered by a thin, outer, non-chitinous epicuticle; each of these has layered subdivisions (see Norton et al. 1997, their Fig. 1). The procuticle is traversed by pore canals that terminate under the innermost layer of the epicuticle, i.e. the

Hypochthonius, Malacoangelia, Nothrolohmannia, and Mixacarus – in these mites the chambers represent greatly enlarged and modified versions of the epicuticular indentations above pore canals, described above. The pore canal ends as a cup-like space under these structures (Figs. 2, 3, 6). The chamber opens to the surface via a small pore (detected by TEM) in Mixacarus (Fig. 3) and in Hypochthonius (Iordansky 1996), and this may be true of the other taxa as well. These pores are hardly visible in SEM, since they are either filled with deposits (and hence obscured) or are extremely minute (Fig. 1). Chambers of this type have electrondense contents in TEM, which demonstrates that the material involved is not dissolved by the staining procedure. From EDXanalysis, both Ca and P are present in chambers of Hypochthonius, Malacoangelia, Nothrolohmannia and Mixacarus (Figs. 7a, 8a). Xray diffraction diagrams of this material from all these species indicates its crystalline nature, which suggests that apatite (calcium phosphate) is present in some form. In Nothrolohmannia a crystalline material of different but unknown composition seems present in the cerotegument (Fig. 6l). The distribution of chambers varies among taxa in this group. In Hypochthonius they are in patches of various size and location on the body and legs, while in Malacoangelia and Nothrolohmannia sp. they cover most of the exposed parts of the cuticle. In Mixacarus the chambers form the

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Figure 1

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SEM of some of the species investigated in the present study: (a-c) Hypochthonius rufulus. (a) General view of specimen. Scale 200 µm. (b) Detail showing areas of smooth and chambered cuticle. Scale 10 µm. (c) Detail of smooth cuticle showing openings of indentations above ‘normal’ pore canals. Scale 0.5 µm. (d-f) Mixacarus sp. (d) General view of specimen. Scale 200 µm. (e) Area of transverse band. Scale 2 µm. (f) Broken cuticle of macerated specimen in the region of a transverse band. Chambered cuticle partly opened and depressions over pore canals are visible (arrows). Walls of chambers surround pores. Scale 2 µm. (g-i) Eniochthonius minutissimus. (g) General view of specimen. Scale 100 µm. (h) Broken cuticle of macerated specimen. Note that chambers are filled with contents. Arrowhead points to spherical indentation under which pore canal terminates. Scale 0.25 µm. (i) Detail showing extremely fine pores of wall channels (arrowheads). Scale 0.5 µm.

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Figure 2

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TEM of: (a) Hypochthonius rufulus; cuticle without chambers and with normal, almost spherical indentations (large arrowhead) above pore canals. Small arrowhead points to the opening of the indentation to the exterior. Note layered procuticle. Arrow indicates pore canal. Scale 1 µm. (b) Same; detail showing indentations and strands of material within pore canals. Scale 0.25 µm. (c) Hypochthonius rufulus; chambered area. Scale 1 µm. (d) Malacoangelia remigera; cuticle of chelicera without chambers. Small arrowheads point to openings of indentations to the exterior, large arrowhead indicates pore canal. Scale 0.25 µm. (e) Same specimen showing chambered cuticle and termination of pore canal (arrowhead). Note indication of epicuticular spicule. Scale 0.5 µm. (f) Nothrolohmannia sp.; chambered cuticle close to disjugal furrow. Note epicuticular spicule. Scale 0.5 µm. (g) Detail of same specimen showing end of pore canal (arrowhead). Scale 0.5 µm.

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Figure 3

TEM of Mixacarus sp: (a) Normal pore canal. Arrowhead shows pore of indentation. Scale 0.25 µm. (b) Porose area. Small arrowheads show pores of indentations, large arrowhead points to nerve ending. Dense bodies, extracellular space and nerve endings are characteristic of this type of porose area (c.f. Alberti et al. 1997). Scale 2 µm. (c) End of pore canal of porose area. Scale 0.25 µm. (d) Chambered cuticle. Arrowhead points to pore of chamber. Scale 0.5 µm. (e) Termination of pore canal under chamber. Arrowhead shows end of pore canal close to wall between chambers. Scale 0.25 µm.

pattern of transverse bands that wrongly has been considered evidence of primitive segmentation (see below). Eniochthonius, Archoplophora, and Phyllozetes – the chambers of these mites represent caverns within the inner epicuticle (Figs. 4, 6i, j), and are clearly independent from the pore canals (at least in Eniochthonius and Archoplophora; pore canals have not yet been found in Phyllozetes). Each canal terminates by encompassing the sac-like end of an epicuticular indentation, as described above. This junction lies well beneath the chamber-layer, and the rest of the indentation forms a thin channel within the walls that separate the chambers (Figs. 4, 6i, j). In this group of mites the chambers are found in all hardened cuticle of the body surface, and they

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are clearly the site of calcium oxalate deposition in Eniochthonius and Archoplophora. In conventionally stained sections the chambers of these mites seem ‘empty’ (as reported by Alberti et al. 1981), but in unstained preparations electron-dense deposits are evident (Fig. 8b); the staining process therefore dissolves the contents. Even without staining, however, other preparation processes seem to destroy the crystalline structure of the contents. Such structure was not detectable in the diffraction diagrams even though clearly demonstrated by Norton and Behan-Pelletier (1991a, b). EDX-analysis of chamber contents of Eniochthonius and Archoplophora demonstrated Ca but no P (Fig. 7b, 8b), consistent with its being calcium oxalate, as determined by Norton and Behan-Pelletier (1991a). The chambers of Phyllozetes are

CUTICLE OF ENARTHRONOTA

Figure 4

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TEM (stained sections) of: (a) Eniochthonius minutissimus; note empty chambers and indentations of cuticle over pore canals (white arrowheads). Dark arrowhead points to proximal portion of pore canal. Scale 1 µm. (b) Phyllozetes sp.; note very thin walls (arrowheads) between wide chambers. Scale 0.5 µm. (c) Archoplophora rostralis; detail of chambered cuticle showing peculiar indentation (almost tubular) and the connection to the surface via a narrow channel which runs through the wall between two chambers (arrowheads). Scale 0.25 µm. (d) Same specimen; rostrum, showing dorsal side with chambered cuticle, ventral side not chambered. Large arrowheads indicate indentations, small arrowheads point to pore canals. Note differently layered procuticle. Scale 0.5 µm.

extremely large, as evidenced by the thin, widely spaced chamber walls that are visible in TEM. We have not viewed the chambers in unstained preparations, but their size and form are consistent with the natural presence of the crystalline plates observed by Norton and Behan-Pelletier (1991b). We also studied the cuticular structure of a peculiar porose organ in Malacoangelia that is located close to the anterior margin of the notogaster, and is often incorrectly called a ‘lenticulus’. This structure has epicuticular chambers like the rest of the cuticle, but also has enlarged pore canals. The latter, which are within the procuticle, contain material that in TEM seems similar to that of the

chambers (Figs. 5a, 6k), but insufficient material prevented EDXanalysis of its chemical composition. Nothrolohmannia sp. has a series of porose areas that form two arcs in a location similar to that of the ‘lenticulus’ of Malacoangelia. Their cuticle is also similar (Figs. 5b, 6l), but for the same reason the contents have not yet been analysed. Abbreviations in figures

B-bacterium; CE – cerotegument; ch – chamber ; cry – crystal within cerotegument; db – dense body ; dsj – dorsal part of sejugal furrow; dhl – dense homogeneous layer; EC – epicuticle;

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Figure 5

Porose areas in anterior region of notogaster (contents of modified pore canals are mostly lost during preparation). (a) Malacoangelia remigera. Note chambers. Scale 0.5 µm. (b) Nothrolohmannia sp. No chambers are present in the porose areas; indentations are very deep. Arrowheads point to proximal portions of pore canals. Scale 0.5 µm.

Es – extracellular space; ind – indentation of cuticle above termination of pore canal; mpoc – modified pore canal within porose area; mu-muscle; pa – porose area; PC – procuticle; po – pore of chamber; poc – pore canal; spi – spine of epicuticle; w – wall between chambers; wc – channel in wall between chambers connecting indentation of cuticle with exterior.

DISCUSSION From the current study, and those of Norton and Behan-Pelletier (1991a, b), it is clear that at least three calcium salts are involved in mineralisation of oribatid mite cuticle: calcium carbonate (calcite; see above), calcium oxalate (whewellite), and calcium phosphate (probably apatite). The first two are easily detectable by optical birefringence, but the third is not. Calcium oxalate and phosphate seem restricted to epicuticular chambers, although the contents of the special pore canals of Malacoangelia and Nothrolohmannia, described above, are as yet undetermined. The function of epicuticular chambers is now clear – they serve as locations for the deposition of minerals – but how and when they develop during cuticle formation, in relationship to mineral deposition, is unknown. Two earlier ideas about the role of epicuticular chambers can probably be discounted. Bernini et al. (1986) seem to have considered this region to constitute a protective layer in Eohypochthonius, one that could be gradually sloughed off and replaced, analogous to the cerotegument. Iordansky (1996) incorrectly interpreted the contents of the chambers of Hypochthonius

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rufulus as wax, and suggested that these chambers would represent ‘an intermediate stage of the cerotegument evolution.’ Our information about where calcium carbonate is deposited is more circumstantial. In some taxa known to deposit calcite it may be located within the procuticle, since no peculiar epicuticular structures have been reported (e.g. some Phthiracaridae). But in others, such as the euphthiracarid Rhysotritia ardua (C. Koch), the cuticle appears shagreened (see Märkel and Mayer 1959), similar to that of Eniochthonius and Archoplophora, i.e. taxa that have epicuticular chambers. In Crustacea, calcite is present in the epicuticle and procuticle (Richards 1951; Neville 1975; Stevenson 1985; Simkiss and Wilbur 1989). What is the function of these mineral deposits? In Crustacea and many Diplopoda, the mineralisation evidently contributes to cuticular hardening and thus improves skeletal and protective functions of the cuticle. There seems little doubt that hardening results when oribatid mite cuticle is mineralised. Untreated cuticle is hard and quite brittle, but if minerals are removed with acids it is much softened (Norton and Behan-Pelletier 1991a). In some cases, the distribution of mineralisation suggests a role that is primarily structural support. This is best seen in Hypochthonius rufulus, in which most of the mineral-filled chambers in the body cuticle are grouped in patches directly above muscle insertions. A rigid, mineralised support should be more efficient than a lightly sclerotised, elastic one. In Eohypochthonius juveniles, the chambers also are distributed in such patches, although they are nearly con-

CUTICLE OF ENARTHRONOTA

Figure 6

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Line drawings summarising cuticular peculiarities of: (a) Hypochthonius rufulus; peripheral layers of portion of cuticle in which no chambers are present. Note peculiar shape of pore canals and corresponding indentations of cuticle (c.f. Fig. 2a,b). (b) Hypochthonius rufulus; peripheral layers of cuticle in chambered region (c.f. Fig. 2c). (c) Malacoangelia remigera; dorsal region of chelicera free of chambers (c.f. Fig. 2d). (d) Malacoangelia remigera; dorsal region of rostrum with chambers (c.f. Fig. 2e). (e) Mixacarus sp.; pore canals in peripheral layers of cuticle between porose areas (c.f. Fig. 3a). (f) Mixacarus sp.; cuticle of porose area; note different shape of indentations (c.f. Fig. 3b,c). (g) Mixacarus sp.; peripheral layers of cuticle in region of transverse bands (c.f. Fig. 3d,e). (h) Nothrolohmannia sp.; region of porose areas on notogaster close to sejugal furrow. Note small muscle (c.f. Figs. 2f,g and 5b). (i) Chambered cuticle of Eniochthonius minutissimus. Note that pore canals do not contact the chambers. Wall channels connect cuticular indentation with the surface (c.f. Fig. 4a). (j) Archoplophora rostralis: similar to Eniochthonius, but indentations are elongated (c.f. Fig. 4c,d). (k) Line drawing of chambered cuticle of Malacoangelia remigera and enlarged pore canals contributing to the porose area (c.f. Fig. 5a). (l) Line drawing of porose area of Nothrolohmannia sp. (c.f. Fig. 5b). Note that in this species the otherwise thick procuticle is thinner under the porose area and the region over the enlarged pore canals is free of chambers. The cerotegument includes crystalline elements.

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Figure 7

Spectra of elements detected by EDX-analysis (U, Pb, Cu result from the staining procedure or the copper grid respectively; cps = counts per second. (a) Hypochthonius rufulus (stained specimen); note presence of large P peak. (b) Archoplophora rostralis (unstained specimen); note absence of large P peak.

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Figure 8

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Distribution of selected elements as detected by EDX-mapping. SE, reference figure showing region of analysis. (a) Hypochthonius rufulus (stained specimen). (b) Archoplophora rostralis (unstained specimen).

tinuous on the adult cuticle (RAN, unpublished). The bands of mineralised chambers in Mixacarus, which show in SEM as narrow grooves, may play a similar role – providing added strut-like support for the arched dorsum of these mites. Grandjean (1934, 1950) believed that these structures (‘sillons transversaux rubannés) delineate primitive segmentation in Lohmanniidae, but the bands are often more numerous than are the purported segments, and the specialised nature of the chambers that form the bands argues strongly against such a view.

Predation is a strong selective force that has shaped the evolution of oribatid mite morphology (Norton 1994), and extensive deposition of minerals may be one outcome. Mineralisation provides little protection from predators if it is localised, but when widespread it may be a considerable deterrent. At least in some cases (e.g. some Hypochthoniidae) extensive mineralisation may have derived from patches that originally had only a support role. The fact that all examined ptychoid mites have mineralised cuticle is a strong argument for the importance of hardening to this body form. Pty-

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choidy, in which the legs and podosoma are withdrawn into the body and the aspis closes over them, is a predator defense that has evolved at least three times in oribatid mites: once in the ancestors of Ptyctima, and twice within Enarthronota (Norton 1984). Impenetrability is fundamental to such a defense, but the support role of mineralisation is also pertinent, since a rigid cuticle seems essential for the unusual hydraulic demands of ptychoidy. Not all the peculiar patterns and sophisticated stuctures shown in some oribatid mite species are easily understandable in relationship to hardening, however. For example, comparable epicuticular chambers generally do not occur in Crustacea or Diplopoda (Stevenson 1985; Simkiss and Wilbur 1989; Hopkin 1992; Wägele 1992), so they are not essential to a protective role. Only the marine isopod Idotea is known to have a very complex epicuticle. The latter contains caverns with unknown function, contents and chemistry (Halcrow 1980), but has a structure entirely different from that of the oribatid mites investigated herein. An alternative, or perhaps complementary, hypothesis is that cuticle may play a role in calcium balance (see Crossley 1975 for general aspects of calcium balance). The cuticle may be an important storage location when Ca is available in excess or a reserve in circumstances when Ca is difficult to obtain. The different Ca compounds (derived from different nutritional regimes; c.f. Norton and Behan-Pelletier 1991a) may have resulted in different specific types or sites of deposition. Perhaps an argument against a role in calcium balance is that resorbtion of minerals from chambers would result in the collapse of their thin epicuticular walls. Also, when the cuticle of immature Eniochthonius is molted the birefringence remains and, hence, the calcium oxalate is not resorbed (Norton and Kethley 1994). Calcium also may be deposited within the digestive system of arthropods, in so called granules or spherites (Hopkin 1989). During the molting cycle of crustaceans there is a dynamic exchange between calcium stored in the cuticle and in the digestive system (Stevenson 1985). Many oribatid mites have preventricular glands (organes racémiformes; Michael 1884; Grandjean 1962; Bernini 1984), which seem to concentrate such granular material (Ludwig et al. 1992). These organs, and the cuticle also, can take up heavy metals after contamination (Ludwig et al. 1991). It would be of interest to determine whether oribatid mite species having specialised mineralisation sites actively deposit heavy metals there. If this is indeed a role, then one might expect a correlation between the specialised deposition sites and the absence of preventricular glands. While preventricular glands are widespread in oribatid mites, they have not yet been reported from Enarthronota or Lohmannioidea. Our observations on chambered cuticles are also relevant to systematics. As noted by Norton and Behan-Pelletier (1991a) cuticular mineralisation is apomorphic within Oribatida, but has evolved at least several times, and we can expect differences among lineages in how it is manifested. The similar, but sophisticated cuticular structure of Hypochthonius and Malacoangelia is consistent with their close phylogenetic relationship (Norton 1984). Our preliminary observations also support the suggestion by Norton (2001) that the previously enigmatic Nothrolohmannia

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is a close relative of these mites. The fact that Mixacarus also shares their apomorphic structures and mineral components supports a hypothesis, currently being developed by RAN, that Lohmanniidae are derived members of Enarthronota. Similarly, Eniochthonius and Archoplophora share close common ancestry (Norton 1984) and have synapomorphic cuticular specialisations that are entirely different from those of the previous group (Phyllozetes is incompletely known in this regard).

ACKNOWLEDGEMENTS The authors wish to thank the following persons for their skillful technical assistance: Mrs. Ch. Putzar, Mrs. S. Schade, Mrs. G. Schittek, Mr H. Fischer, Dr Th. Kaiser, and Mr M. Zander (all University of Greifswald). Dr E. Franklin (INPA, Manaus, Brazil) kindly provided specimens of Mixacarus sp.

REFERENCES Alberti, G. and Nuzzaci, G. (1996). SEM and TEM Techniques. In ‘Eriophyoid Mites – Their Biology, Natural Enemies and Control.’ (Eds E. E. Lindquist, J. Bruin and M. W. Sabelis.) pp. 399–410. (Elsevier: Amsterdam.) Alberti, G., Storch, V., and Renner, H. (1981). Über den feinstrukturellen Aufbau der Milbencuticula (Acari, Arachnida). Zoologische Jahrbücher, Anatomie 105,183–236. Alberti, G., Norton, R. A., Adis, J., Fernandez, N. A., Franklin, E., Kratzmann, M., Moreno, A. I., Weigmann, G., and Woas, S. (1997). Porose integumental organs of oribatid mites (Acari, Oribatida). 2. Fine structure. Zoologica (Stuttgart), 146, 33–114. Balogh, J. and Balogh, P. (1992a). ‘The Oribatid Mites Genera of the World, vol. 1.’ (Hungarian Natural History Museum: Budapest.) Balogh, J. and Balogh, P. (1992b). ‘The Oribatid Mites Genera of the World, vol. 2.’ (Hungarian Natural History Museum: Budapest.) Bergström, J. (1979). Morphology of fossil arthropods as a guide to phylogenetic relationships. In ‘Arthropod Phylogeny.’ (Ed. A. P. Gupta) pp. 3–56. (Van Nostrand Reinhold: New York.) Bernini, F. (1984). Notulae Oribatologicae XXXII. Some new galumnid mites (Acarina, Oribatida) from North Africa exhibiting sexual dimorphism with some observations on racemifrom organs. Animalia 11, 103–126. Bernini, F., Manicardi, G., and Avanzati, A. M. (1986). Notulae Oribatologicae- XXXVIII. On the first European record of an Eohypochthonius species in Italy (Acarida, Oribatida). International Journal of Acarology 12, 115–122. Crossley, D. A. 1977. Oribatid mites and nutrient cycling. In ‘Biology of Oribatid Mites.’ (Ed D. L. Dindal.) pp. 71–85. (State University of New York: Syracuse.) Dalingwater, J. E. (1987). Chelicerate cuticle structure. In ‘Ecophysiology of Spiders.’ (Ed W. Nentwig.) pp. 3–15. (Springer-Verlag: Berlin.) Grandjean, F. (1934). La notation des poils gastronotiques et des poils dorsaux du propodosoma chez les Oribates (Acariens). Bulletin de la Société Zoologique de France 59, 12–44. Grandjean, F. (1950). Étude sur les Lohmanniidae (Oribates, Acariens). Archives de Zoologie Expérimental et Générale 87, 95–161. Grandjean, F. (1962). Nouvelles observations sur les oribates. (2e série). Acarologia 7, 91–112. Halcrow, K. (1980). The epicuticle of a marine isopod, Idotea baltica (Pallas). Canadian Journal of Zoology 58, 305–308. Hopkin, S. P. (1989). ‘Ecophysiology of Metals in Terrestrial Invertebrates.’ (Elsevier: London.)

CUTICLE OF ENARTHRONOTA

Hopkin, S. P. (1992). ‘The Biology of Millipedes.’ (Oxford University Press: Oxford.) Iordansky, S. N. (1996). Fine structure of the cuticle in the oribatid (Oribatida) mites and its adaptive evolution. In ’Acarology IX – Proceedings.’ (Eds R. Mitchell, D. J. Horn, G. R. Needham and C. W. Welbourn) pp. 685–687. (Ohio Biological Survey: Columbus.) Ludwig, M., Kratzmann, M., and Alberti, G. (1991). Accumulation of heavy metals in two oribatid mites. In ’Modern Acarology, vol 1. Proceedings of the VIII International Congress of Acarology.’ (Eds F. Dusbábek and V. Bukva) pp. 431–437, pl. 19. (Academia, Prague and SPB: The Hague.) Ludwig, M., Kratzmann, M., and Alberti, G. (1992). Some observations on the proventricular glands (‘organes racémiformes’) of the oribatid mite Chamobates borealis (Oribatida, Acari): An organ of general interest for studies on adaptation of animals to acid soils. Experimental and Applied Acarology 15, 49–57. Märkel, K. and Meyer, I. (1959). Zur Systematik der deutschen Euphthiracarini (Acari, Oribatei). Zoologischer Anzeiger 163, 327–342. Michael, A. D. (1884). ‘British Oribatidae, vol. 1.’ (Ray Society: London.) Müller, A. H. (1981). ‘Lehrbuch der Paläozoologie. Bd. II. Invertebraten. Teil 2. Mollusca 2 – Arthropoda 1.’ (G. Fischer Verlag: Jena). Neville, A. C. (1975). ‘Biology of Arthropod Cuticle.‘ (Springer-Verlag: New York.) Norton, R. A. 1984. Monophyletic groups in the Enarthronota (Sarcoptiformes). In ‘Acarology VI, vol. 1.’ (Eds D. A. Griffiths and C. E. Bowman.) pp. 233–240. (Ellis Horwood: Chichester.) Norton, R. A. 1994. Evolutionary aspects of oribatid mite life-histories and consequences for the origin of the Astigmata. In ‘Mites: Ecological and Evolutionary Analyses of Life-History Patterns’ (Ed M. Houck) pp. 99–135. (Chapman and Hall: New York.)

AND

LOHMANNIOIDEA

Norton, R. A. 2001. Systematic relationships of Nothrolohmanniidae, and the evolutionary plasticity of body form in Enarthronota (Acari: Oribatida). In ‘Acarology: Proceedings of the 10 th International Congress’. (Eds R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff) pp. 58–75. (CSIRO Publishing: Melbourne). Norton, R. A. and Behan-Pelletier, V. M. (1991a). Calcium carbonate and calcium oxalate as cuticular hardening agents in oribatid mites (Acari: Oribatida). Canadian Journal of Zoology 69, 1504–1511. Norton, R. A. and Behan-Pelletier, V. M. (1991b). Epicuticular calcification in Phyllozetes (Acari: Oribatida). In ’Modern Acarology, vol 2. Proceedings of the VIII International Congress of Acarology.’ (Eds F. Dusbábek and V. Bukva) pp. 323–324. (Academia, Prague and SPB: The Hague.) Norton, R. A. and Kethley, J. B. (1994). Ecdysial cleavage lines of acariform mites (Arachnida, Acari). Zoologica Scripta 23, 175–191. Norton, R. A., Alberti, G., Weigmann, G., and Woas, S. (1997). Porose integumental organs of oribatid mites (Acari, Oribatida). 1. Overview of types and distribution. Zoologica (Stuttgart), 146, 1–31. Richards, A. G. (1951). ‘The Integument of Arthropods.’ (University of Minnesota Press: Minneapolis.) Simkiss, K. and Wilbur, K. M. (1989). ‘Biomineralization. Cell Biology and Mineral Deposition.’ (Academic Press: San Diego.) Stevenson, J. R. (1985). Dynamics of the integument. In ‘The Biology of Crustacea, vol. 9’ (Eds D. E. Bliss and L. H. Mantel.) pp. 1–42. (Academic Press: Orlando.) Størmer, L. (1955). Merostomata. In ‘Treatise on Invertebrate Palaeontology, part P. Arthropoda 2’ (Ed R. C. Moore) pp. P4–P41. (The University of Kansas Press: Lawrence.) Wägele, J.-W. (1992). Isopoda. In ‘Microscopic Anatomy of Invertebrates, vol. 9. Crustacea’ (Eds W. H. Frederickson and A. G. Humes) pp. 529–617. (John Wiley & Sons: New York.)

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ACAROLOGY

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

THE LEG CHAETOTAXY OF CALIGONELLIDAE (PROSTIGMATA: RAPHIGNATHOIDEA)

....................................................................................................

Sabina Fajardo Swift J. Linsley Gressitt Center for Research in Entomology, Department of Natural Sciences, 1525 Bernice Street, Honolulu, Hawaii 96817-0916, USA Present address: Department of Entomology, University of Hawaii at Manoa, 3050 Maile Way, Gilmore 310, Honolulu, Hawaii 96822, USA, e-mail: [email protected]

.................................................................................................................................................................................................................................................................

Abstract The leg setal ontogeny of a caligonellid mite is presented for the first time. Leg chaetotaxic notations and their relative positions in larva and adult legs are illustrated establishing setal homologies with those of the Stigmaeidae, Raphignathidae and sister families in the Acariformes. It is hoped that other workers will be stimulated to look closer into leg chaetotaxy because there is a wealth of anatomical information extremely useful in further understanding of Acari systematics and phylogeny.

INTRODUCTION The leg chaetotaxy of members of the superfamily Raphignathoidea has not been seriously examined by acarologists since Grandjean (1944) assigned setal notations and discussed the leg setal complements of Storchia robusta (Berlese, 1885) (= Apostigmaeus navicella Grandjean, 1944) (Wood 1973). Grandjean also noted the solenidial differentiation between male and female adults and the existence of what was referred to as tarsal clusters on tarsi I and II of larvae. For members of the family Stigmaeidae, a tarsal cluster includes a eupathid p and a normal seta tc, in the prime (') (when a seta is located anterior of leg segment relative to body or paraxial) location. An exception is Storchia robusta, with two clusters on tarsus I in prime (') and second (") (when a seta is located posterior of leg segment relative to body or antiaxial) locations. Summers (1960) doubted Grandjean’s setal notations and did not use the system because of the risk of perpetuating incorrect homologies in the superfamily Raphignathoidea by future workers. Instead he used a topographic or descriptive system derived from existing nomenclatures. Atyeo (1963) on the other hand, applied Grandjean’s system of leg chaetotaxy to the genus Raphignathus naming setae for each given segment and equally naming

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all possible setae for the same segment for other possible raphignathoid taxa, an attempt to establish setal homologies between various raphignathoid groups. He concluded that the leg setae of Raphignathus, with the exception of the tarsi, are similar to the Stigmaeidae. The leg setation of Coptocheles grandjeani Robaux, 1975 was partly discussed by Robaux (1975), noting only some of the prominent leg setae. However, even with the excellent review of the leg chaetotaxy of Oribatei by Norton (1977), making Grandjean’s work in French available to a wider audience, the previous works did not stimulate further interest among raphignathoid workers. Lindquist (1985) had included in his studies of leg setation of the Tetranychidae, representatives of the superfamily Raphignathoidea as outgroups. This paper partly reviews the taxic system for the stigmaeid mites developed by Grandjean, as applied to caligonellid mites. Concepts of verticils, distinctions of fundamental from accessory setae, appearance and disappearance of particular setae during ontogeny, and other generalities Grandjean discussed for oribatid mites, are equally applicable to members of the family Caligonellidae, the superfamily Raphignathoidea and Acariformes in general.

THE LEG CHAETOTAXY

Table 1

Leg II

Leg III

Leg IV

CALIGONELLIDAE

Setal ontogeny of Coptocheles solanii. In the absence of a protonymph, its probable setal complement is hypothesized in this table. Setal parentheses ( ) represent a pair. "–" means seta(e) is as in previous stase(s) (i.e. trochanter III of Adult has full complement of l ' and v' setae which appeared during N1 and N2, respectively). trochanter

Leg I

OF

femur

genu

tibia

tarsus (ft), (tc), (p), (pv), (pl), (u), a', vs

L

O

d, bv"

(v), (l)

d, (l), (v)

N1

–

–

d

–

(it)

N2

v'

(l)

–

–

a" vs lost

Ad

–

v'

–

–

(l), (v)

L

O

d, bv"

(v), (l)

d, (l), (v)

ft', (tc), (p), (pv), pl', (u), a', vs

N1

–

–

d

–

(it)

N2

v'

(l)

–

–

a" vs lost

Ad

–

v'

–

–

(l), (v)

L

O

d, ev'

(v), l"

d, (l), l'

(tc), (pv), (a), (u)

N1

l’

–

d

–

–

N2

v'

l'

l'

–

(it)

Ad

–

l"

–

–

(v)

N1

O

d, ev'

v', l

d, (v), l'

(tc), (pv), (a), (u)

N2

O

–

l"

–

–

Ad

v'

(l)

d

–

(v), (it)

MATERIALS AND METHODS Several species of Coptocheles, Molothrognathus, and a species of Neognathus from the Hawaiian Islands (Swift 1996) and from species descriptions by Smith Meyer and Ueckermann (1989) were used in this study ( see Table 2). Raphignathus sp. (Raphignathidae), Favognathus distinctus Swift (Cryptognathidae), Storchia robusta and Eustigmaeus kauaiensis Swift (Stigmaeidae), Neophyllobius sp. (Camerobiidae) and Saniosulus nudus Summers (Eupalopsellidae) were also examined. Leg chaetomes of larvae, adults and nymphs (N1 for protonymph and N2 for deutonymph), if available, were noted. Data presented in this study were taken from the Hawaiian species Coptocheles solanii Swift. The protonymph of C. solanii is unavailable thus the presence of setae is hypothesised in this study. Setal parentheses ( ) represent a pair. Setal priority for each leg segment refers to a list of setal organs that appear at the beginning of developmental ontogeny which have greater priority, or force, than the organs that come later during development. It means that these setal organs are less susceptible to evolutionary regression (Norton 1977).

RESULTS AND DISCUSSION The ontogeny of the leg chaetotaxy of C. solanii is presented in Table 1. Setal notations and their relative positions in the leg segments are shown in Fig. 1 for the female adult and in Fig. 2 for the larva. Tarsal clusters in larval raphignathoids represented by Saniosulus nudus (Eupalopsellidae), Neophyllobius sp. (Camerobiidae), Eryngiopus sp.(Stigmaeidae), Favognathus sp. (Cryptognathidae), Raphignathus sp. (Raphignathidae), and Molothrognathus conantae (Caligonellidae) show distinct variations in size, length, and even locations of the two setal elements p and tc (Fig. 3). Leg setal formulas (legs I–IV) of selected raphignathoid taxa (Table 2) show numerical variations which are systematic and phylogenetic clues in further understanding the group. Each segment is briefly discussed.

Larva – The term fundamental setae refers to setae which exist in the larval stase, especially of the tarsus (legs I–III) and in the protonymph (N1) (leg IV). In C. solanii, tarsus I has a maximum of 14 fundamental setae, excluding solenidion ω. Three pairs, the fastigials (ft', ft"), the tectals (tc', tc") and the prorals (p'ζ, p" ζ ) are situated dorsally, in order from proximal to distal; ft has a slight prime disjunction. Proral (p'ζ) however is in the tectal position in the larva. This will be discussed later in the analysis of tarsal clusters. Solenidion ω is set slightly distal of ft', ft" On the lateral side a pair of primilaterals (pl', pl") and antilateral (a') are located posterior and distal of each other, respectively. Antilateral a' is on the prime location. Below the antilateral is a pair of unguinals (u', u"), anterior of the unpaired subunguinal (vs') situated ventrally. Located posterior of vs, is a pair of primiventrals (pv', pv"). Tarsus II has 12 fundamental setae (excluding solenidion ω); ft" and pl" are missing. Tarsus III has 8 fundamental setae – (pv), (u), (a), and (tc) ; antilateral in the second position (a") has appeared on tarsus III. Leg IV of the protonymph has basically the same number of fundamental setae as Tarsus III as observed in S. robusta (Grandjean 1944). The tarsal cluster. This setal cluster is formed on larval tarsi I and II by a characteristic association of setiform organs. In S. robusta, there is a total of three tarsal clusters, two in tarsus I and one in tarsus II. These clusters are shown as tc', p' ζ and tc", p" ζ on tarsus I and the third one, on tarsus II, as tc', p' ζ. The three tarsal clusters are similar and only exist in the larval stage. In C. solanii, there are two tarsal clusters, one on tarsus I (tc', p' ζ) and one on tarsus II (tc', p' ζ), both in the same prime location. Grandjean's (1944) observation of S. robusta that as soon as the next stage N1 appears, the clusters dissociate and resume the normal arrangement as in other stages and legs, is probably true with C. solanii. Neophyllobius sp. (Fig. 3B) is unusual in that tc' is five times longer that p' ζ, the two setae are in the usual positions, p' ζ in proral and tc in

243

Figure 1

Legs 1-IV of Coptocheles solanii female. Setal equivalents: tc = tectal, ft = fastigial, p = proral; u = unguinal; a = antilateral; it = iteral; pl = primilateral; pv = primiventral; vs = ventral subunguinal; v = ventral; bv ‘= ventral on femurs I and II; ve '= ventral on femurs III and IV; (') = prime, anterior of leg; (") = second, posterior of leg; Greek z = eupathid.

Sabina Fajardo Swift

244

Legs I–III of Coptocheles solanii larva. Setal equivalents as in Figure 1.

OF

Figure 2

THE LEG CHAETOTAXY CALIGONELLIDAE

245

Figure 3

Leg I tarsus of larvae showing the tarsal cluster or lack of it as in Neophyllobius sp. A. Saniosulus nudus, (Eupalopsellidae); B. Neophyllobius sp. (Camerobiidae); C. Eryngiopus sp. (Stigmaeidae); D. Favognathus sp. (Cryptognathidae); E. Raphignathus sp., (Raphignathidae); F. Molothrognathus conantae (Caligonellidae). Setal equivalents as in Figure 1.

Sabina Fajardo Swift

246

THE LEG CHAETOTAXY

Table 2

OF

CALIGONELLIDAE

Leg setal formulas of caligonellid mite adults and representative genera of families Stigmaeidae, Raphignathidae, Cryptognathidae, Eupalopsellidae, and Camerobiidae. Trochanter

Femur

Genu

Tibia

Tarsus

Coptocheles kalapanaensis

1-1-2-1

5-5-4-4

5-4-4-4

5-5-4-5

21-18-12-12

Coptocheles nakaharai

1-1-2-1

4-4-3-3

5-5-4-4

5-5-4-4

20-19-12-12

Coptocheles solanii

1-1-2-1

5-5-4-4

5-5-4-4

5-5-4-4

20-18-12-12

Molothrognathus colei

1-1-1-1

2-2-2-2

5-5-2-2

5-5-4-4

15-10-9-9

Molothrognathus conantae

1-1-1-1

2-2-2-2

5-4-2-2

5-4-2-2

14-9-8-8

Molothrognathus tumipalpus

0-0-0-0

2-2-2-1

5-3-1-1

3-3-2-2

10-7-5-5

Neognathus spectabilis

1-1-2-1

4-3-2-2

5-5-3-3

5-5-5-4

14-9-8-8

Caligonella afroensis

1-1-1-1

2-2-2-2

6-5-2-2

5-5-4-4

15-11-9-9

1-1-2-1

6-6-4-4

6-6-4-4

5-5-5-4

19-15-13-13

1-1-1-1

4-3-2-2

2-2-1-1

9-8-8-7

10-10-8-7

Storchia robusta

1-1-1-1

4-4-3-2

5-4-2-2

5-5-5-5

13-9-7-8

Eustigmaeus kauaiensis

1-1-1-1

6-5-3-2

4-4-1-1

5-5-5-5

14-10-8-7

1-1-1-1

4-3-2-2

5-4-2-3

5-5-4-2

15-12-9-9

1-1-1-1

4-4-2-2

2-1-1-1

6-5-5-5

10-8-6-6

Family Caligonellidae

Family Raphignathidae Raphignathus sp. Family Camerobiidae Neophyllobius sp. Family Stigmaeidae

Family Cryptognathidae Favognathus distinctus Family Eupalopsellidae Saniosulus nudus

tectal positions, (tc) in prime disjunction as usual. Proral p" ζ is totally suppressed, although its pair tc" is in the tectal position, and one third the length of tc'. The notations for these setae and eupathidia imply some surprising homologies (Grandjean 1944). For example, the long, large tectal eupathids tc' ζ, of tarsus I and II are short setiform setae in the larval stase. In addition, and even more anomalous, the eupathids p' ζ of tarsi I and II left their usual proral location for a tectal location. Grandjean (1944) earlier observed this phenomenon on S. robusta and he believed that this proral movement has to be accepted because if not, certain fundamental rules would have been rejected: first, proral setae on tarsus I are always eupathidic in the larval stase in both Prostigmata and Oribatei; and second, to designate the eupathidial tectal pair of setae on tarsus I as tc primarily because of its tectal location is wrong and unacceptable as eupathidic tc had not been oberved on larvae of any mite. It is also possible to recognise the homologies of all the setae except that of tc and p. This movement of the prorals to tectal positions in the larvae was termed ‘anabasis’ by André (1981). According to Grandjean (1944), it is not unusual to observe tectal hairs becoming finer and shorter, since this is usually the fate of an ordinary hair when it is associated with a eupathid or a solenidion. It is also known in Oribatei that the diminution in size of the hair which is proximal has often benefited the anterior hair, which is distal (Grandjean 1935). Grandjean observed in the larvae and nymphs of Belba geniculosa that solenidia σ,ϕ1, ϕ in genu and tibia I, pair with a dorsal seta ds where the solenidia are positioned forward and the short ds located proximally covering and protecting the solenidia, which are usually large and long.

Thus, this seems to be a logical reason for the exceptionally large size of raphignathoid proral hairs when they are located in the tectal position. This grouping of tc and pζ is not at all rare. It is found in most raphignathoids with the exception of the genus Neophyllobius in the family Camerobiidae as discussed previously. The families Tydeidae (André 1981) and Eupodidae (Booth et al. 1985) exhibit the same tarsal grouping in the larval stase. Trochanter. Seta v' is absent in trochanters I–III of the larva of raphignathoids. In C. solanii v', which occupies the l' position in the trochanter, appears on legs I–III of the deutonymphs (N2), and in the adults. The second seta l' probably appears in the protonymphal (N1) stase on leg III, thus a complement of two setae, v' and l' is found on leg III. The three Coptocheles species and N. spectabilis have similar basic pattern of 1-1-2-1, whereas the two Molothrognathus species with a 1-1-1-1 pattern, seta l' is suppressed on trochanter III. In M. tumipalpus, an African species, v' is totally suppressed (Table 2). This basic setal pattern is also found in Tuckerellidae (Quiros-Gonzalez and Baker 1984), Tenuipalpidae and Tetranychidae (Lindquist 1985), and in Raphignathus sp. and Eustigmaeus, Saniosulus, and Favognathus of the Raphignathoidea. The setal priority of caligonellid trochanters is as follows: v', l'. Femur. The undivided femur is typical of the raphignathoids and their relatives. The presence of setae bv" on legs I and II and ev' on legs III and IV, shows that the caligonellid femur is a composite segment, with two remnant primitive verticils bv" and ev'. The larval stase has the dorsal seta d and the verticil bv" for legs I and II and d and ev' for legs III and IV. Coptocheles nakaharai with setal pattern 4-4-3-3 has the complement of d, bv", (l) for legs I

247

Sabina Fajardo Swift

and II and d, ev', l' for legs III and IV. For species with 5-5-4-4 setal pattern (S. kalapanaensis and C. solanii), v' is added on legs I and II and l" added on legs III and IV. The setal complement for Caligonella afroensis (2-2-2-2) is probably a complement of d, bv" on legs I and II, and d, ev' on legs III and IV.

the prorals, and are paired. Neophyllobius has a pair of iteral setae on legs I–IV. On Stigmaeus, tc' and tc" I become eupathids in N1, and the same is probably true in Caligonellidae. Setae ft' and ft" which appear only on leg I and ft' on leg II probably became eupathids during N2 as the stigmaeids (Grandjean 1944).

The setal priorities for caligonellid femur is as follows: (d, bv", ev'), l', l", v'.

Eupathidia. The eupathidia (or eupathids) are modified setae which are hollow, with a canal in the root. In caligonellids and most raphignathoids, these eupathids are inserted in large alveoli, sometimes in large tubercles, simple and more or less ceratiform. They are mostly found on tarsi I and II and never on tarsi III and IV, in any stase. When a normal seta changes to a eupathid during ontogeny, this is simply explained as loss of inhibitory mechanism acting on the normal ‘setal character’ (see Grandjean 1946; Norton 1977). The Greek letter zeta (ζ) signifies the eupathidic condition.

Genu. The genual setation for larval and protonymphal caligonellids on legs I–IV is 4-4-3-2; genua I and II each have setae l', l" and v' and v", while genua III has l', v', v" and genu IV has l', v'. Seta d on legs I–IV is probably protonymphal as in Stigmaeidae (Grandjean 1944). The minimum complement of genual setae is 5-4-2-2 of Molothrognathus with l',l", v', v", d on leg I, v" is retarded on leg II and setae v", l', d on legs III and IV. The maximum complement of 6-5-2-2 of Caligonella (Smith Meyer and Ueckermann 1989), setiform k was probably included in the count on genu I. The setiform seta most workers designate as k appears on leg I in all stases of stigmaeids. On legs II, III and IV, the seta disappears. In caligonellid mites, I saw a different seta that is not the setiform k , but is instead, a probable solenidion. I designate this spatulate seta as the genual solenidion σ. This genual spatulate solenidion is also found in the genera Favognathus (Cryptognathidae) (Swift 1996) and Cryptognathus (Cryptognathidae) (Robaux 1975). The setal priority of caligonellid genu is as follows: (l', l", v', v"), d. Tibia. Larval to adult stase tibial setation has the same five uneven verticils on legs I and II, of the normal type d, v',v", l',l". On leg III l' is lost while l" is lost on leg IV, and with v', v", l' and d remain in all stases. In Coptocheles and other raphignathoids examined, seta d remained normal, while in Storchia dI becomes eupathidial on N1. Neognathus dI and dII are eupathidial in the adult. The maximum tibial setal component is in Neophyllobius , with 9-8-87 setae on legs I–IV. With the exception of a solenidion (φ) located anterodorsal of the segment, it is difficult to determine which seta is dorsal and which is ventral, without examination of the early stase and of other related taxa. The minimum tibial component is that of Molothrognathus tumipalpus Smith Meyer and Ueckermann with 3-3-2-2 setae on legs I–IV. The specimens had to be examined to determine which setae were suppressed during ontogeny. The setal priorities for legs I and II are d, l', l",v', v" and for legs III and IV are (d, v', v", l"), l'. A separate examination of the leg chaetotaxy of Camerobiidae has to be conducted to establish homologies with the other raphignathoids. Tarsus. The larval chaetome of caligonellid mite larvae has a 1412-8 pattern on the tarsus of legs I, II, and III. Tarsi I and II of raphignathoid larvae, with the exception of Neophyllobius, exhibit one to three tarsal clusters in the larval stase as discussed above. Iteral setae it I and II are probably protonymphal. This pair of accessory setae were not reported as present in Stigmaeidae (Grandjean 1944) and Raphignathidae (Atyeo 1963), but Robaux (1975), in his description of Coptocheles grandjeani, indicated in his illustration the iteral setae on the tarsi of legs I-IV. The iteral setae are located anterodorsal of the tectals, posterior of

248

Tarsus I of caligonellid mite adults (Coptocheles) has a complement of ten eupathids: (ft), (tc), (p), (pv), and (pl). Tarsus II has six eupathids: ft', (tc), (p) and pl'. The tectals (tc) probably become eupathids in N1 as in stigmaeids, with the fastigials (ft) in N2. The primilaterals (pl) and primiventrals (pv) become eupathids in the adult stase. Compared to Storchia , which has a complement of six eupathids, (ft), (tc), (p) on tarsus I and two, tc' and p' on tarsus II, and to Neophyllobius with prorals (p) on tarsus I, Coptocheles or Caligonellidae is the more primitive of the raphignathoids if Grandjean’s (1935) belief that primitive Oribatida generally have more eupathids is correct. In Storchia, seta d on tibia I becomes eupathidic in N1 whereas it remains an ordinary seta in Caligonellidae and Eustigmaeus. The seta d of tibia II becomes eupathidic in N1 (Homocaligus) (Grandjean 1944), or in N2 (Stigmaeus, Eustigmaeus) or remains an ordinary seta (Eustigmaeus, Storchia, Coptocheles). Dorsal seta, d, of Neognathus is eupathidial on tibia I and II. Eupathids are not known to transform back to normal setae (Norton 1977). Solenidia. Solenidia among caligonellid mites are smooth, hollow and sometimes with distinct transverse striations, usually baculiform. They are found on the tarsus, tibia and genu of the legs and on the tarsus of the palps. The solenidial formula for legs I–IV of adult Coptocheles is: tarsus ω – ω -0-0, tibia φ, φρ - φρ - φρ - φρ, and genu σ-0-0-0. The same formula is true for the male except that in Coptocheles and in Raphignathus males, the accessory sexual solenidion ω male is not present unlike in other genera such as Storchia, Eryngiopus, Eustigmaeus and most raphignathoids.

ACKNOWLEDGEMENT I thank Robert Smiley and Ron Ochoa, of USDA, Systematic Entomology Laboratory, Beltsville, for the loan of type of Storchia pacifica (Summers); and M. Lee Goff, University of Hawaii at Manoa, for interesting discussions on mite legs.

REFERENCES André, H. M. (1981). A generic revision of the family Tydeidae (Acari: Actinedida) III. Organotaxy of the legs. Acarologia 22, 165–178. Atyeo, W. (1963). New and redescribed species of Raphignathidae (Acarina) and a discussion of the chaetotaxy of the Raphignathoidea. Journal of the Kansas Entomological Society 36, 172–186.

THE LEG CHAETOTAXY

Berlese, A. (1885). Acari, Myriopoda et Scorpiones hucusque in Italia reperta fasc. 22, No. 3–7. Booth, R. G., Edwards, M., and Usher, M. B. (1985). Mites of the genus Eupodes (Acari, Prostigmata) from maritime Antarctica: a biometrical and taxonomic study. Journal of Zoology, London (A) 207, 381–406. Grandjean, F. (1935). Les poils et les organes sensitifs portés par les pattes et le palp chez les Oribates, 1re partie. Bulletin de la Societé Zoologique de France 60, 6–39. Grandjean, F. (1944). Observations sure les Acariens de la famille des Stigmaeidae. Archives des Sciences Physiques et Naturelles 5 me periode 26, 103–131. Grandjean, F. (1946). Les poils et les organes sensitifs portés par les pattes et le palp chez les Oribates, Troisieme partie. Bulletin de la Societe Zoologique de France 71, 10–29. Lindquist, E. E. (1985). Chapter 1.1 Anatomy, phylogeny and systematics 1.1.1. External anatomy. In ‘Spider mites. Their biology, natural enemies and control.’ (Eds. W. Helle and M.W. Sabelis.) (Elsevier: Amsterdam.) Norton, R. A. (1977). A review of F. Grandjean’s system of leg chaetotaxy in the Oribatei and its application to the Damaeidae. In ‘Biology of oribatid mites.’ (Ed. D. L. Dindal) (State University of New York: Syracuse.) Quiros-Gonzalez, M. J. and Baker, E. W. (1984). Idiosomal and leg chaetotaxy in the Tuckerellidae Baker and Pritchard: ontogeny and nomenclature. In ‘Acarology VI (Proceedings of the VI International

OF

CALIGONELLIDAE

Congress of Acarology, Edinburg, Scotland, September 1982)’ (Eds. D. A. Griffiths and C. E. Bowman) (Ellis Horwood: Chichester.) Robaux, P. (1975). Observations sur quelques Actinedida (=Prostigmates) du sol d’Amerique du Nord. 1. Une nouvelle espece de Caligonellidae (Acari – Raphignathoidea): Coptocheles grandjeani n. sp. Acarologia 17, 236–242. Robaux, P. (1975). Observation sur quelque Actinedida (=Prostigmates) du sol d’Amerique du Nord. III. Description de deux nouvelle especes de Cryptognathus (Acari-Raphignathoidea-Cryptognathidae). Acarologia 17, 257–268. Smith Meyer, M. K. P and Ueckermann, E. A. (1989). African Raphignathoidea (Acari: Prostigmata). Entomology Memoir of the Department of Agriculture and Water Supply, Republic of South Africa 74, 1–58. Summers, F. M. (1960). Several stigmaeid mites formerly included in Mediolata redescribed in Zetzellia Ouds., and Agistemus, new genus. Proceedings of the Entomological Society of Washington 62, 233–247. Swift, S. F. (1996). Hawaiian Raphignathoidea: Family Caligonellidae (Acari: Prostigmata), with descriptions of five new taxa and a key to genera and species. Annals of the Entomological Society of America 89, 313–327. Swift, S. F. (1996). Hawaiian Raphignathoidea: Family Cryptognathidae (Acariformes: Prostigmata), with descriptions of three new species of the genus Favognathus. International Journal of Acarology 22, 83–89. Wood, T. G. (1973). Revision of Stigmaeidae (Acari: Prostigmata) in the Berlese Collection. Acarologia 15, 76–95.

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

....................................................................................................

AN ALARM PHEROMONE FUNCTION OF THE SECRETION FROM THE NYMPHAL STAGE OF THE ORIBATID MITE NOTHRUS PALUSTRIS (C. L. KOCH) (ACARI: NOTHRIDAE) Satoshi Shimano1, Tomoyo Sakata2, Yoshikatsu Mizutani3, Yasumasa Kuwahara2 and Jun-ichi Aoki3 1

Department of Upland Farming, Tohoku National Agricultural Experiment Station, Arai, Fukushima 960–2156, Japan 2 Department of Soil Zoology, Institute of Environmental Science and Technology, Yokohama National University, Hodogaya-ku, Yokohama 240–8501, Japan 3 Laboratory of Chemical Ecology, Division of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Sakyo-ku, Kyoto 600–8502, Japan

.................................................................................................................................................................................................................................................................

Abstract The presence of an alarm pheromone is demonstrated for the first time in the deutonymphal stage of the oribatid mite, Nothrus palustris (C. L. Koch). The active principle is identified as geranial (3,7-dimethyl-[E]-2,6-octadienal, active at 10–100ng).

INTRODUCTION We observed that if one or more specimens of Nothrus palustris (C. L. Koch) were crushed by forceps at their deutonymphal stage, mites aggregating around them started to disperse, and eventually the aggregation was completely dispersed within several minutes. The same behaviour was reproducible when a small piece of filter paper impregnated with the hexane extract of nymphal bodies was placed at the center of the aggregation. These findings suggest that on being crushed, deutonymphs of Nothrus palustris emit an alarm pheromone as a volatile compound, possibly from a pair of oil glands, and that the active compound could be extracted by hexane from nymphal bodies. We report here the detection and function of a secretion from the deutonymphal stages of N. palustris as an alarm pheromone. The active principle, geranial (3,7-dimethyl-[E]-2,6-octadienal), is one of the compounds commonly distributed among Astigmata, but is a recent discovery in the Oribatida. It supports the close evolutionary relationship between Astigmata and Oribatida suggested by OConnor (1984) and Norton et al. (1993).

MATERIALS AND METHODS Large numbers of N. palustris deutonymphs were collected on August 10, 1996 from litter and soil in the campus of Yokohama

250

National University, Hodogaya-ku, Yokohama, by Tullgren funnel extraction. The species is present in forest litter as a decomposer and has been recorded in many parts of the Palaeartic region (e.g. Sellnick and Forsslund, 1955) some of the nymphs were raised to adults to confirm the identify of the species. Twenty deutonymphs as a group were transferred in a open glass tube (1cm in diameter, 2 cm in height) placed on the test arena, and were allowed to settle for a time to off-set handling effects. The test arena was 1 cm in diameter. After removing the glass tube with the least disturbance, a filter paper (3 × 3 mm) with a candidate compound dissolved in 3 ml of hexane, or a freshly crushed mite body, was introduced at the center of the arena. Mites in the test arena were then counted every minute for five minutes. Filter paper treated with hexane 3ml was used as a control. Gas liquid chromatography (GLC) was carried out on an HP5890 series II plus equipped with an FID using an HP-5 capillary column (0.32 mm × 30 m, 0.33 mm in film thickness) at a temperature program of 60oC to 290oC at 10oC/min. with an initial 2 min. hold. Samples were analysed with a split-less mode using He as a carrier gas, and the chromatogram was processed by an HP 3396 series II Integrator. GC-Mass spectrometry (GC/MS) was performed by a Hewlett Packard 5989B mass spectrometer coupled with an HP-5890 series II plus gas chromatograph in

AN ALARM PHEROMONE FUNCTION OF THE SECRETION FROM THE NYMPHAL STAGE OF THE ORIBATID MITE NOTHRUS PALUSTRIS

Table 1

Alarm pheromone activity of a nymphal body of Nothrus palustris and geranial Number of mites staying in the test circle Time after introduction of sample (min.)

Control

0.1

1

10

100

Squashed mite body

0

20

20

20

20

20

20

Geranial (ng)

1

17

17

12

7

5

11

2

15

14

8

4

2

6

3

13

13

5

2

0

4

4

12

13

3

2

0

0

5

10

11

2

0

0

0

split-less mode, using the same capillary column under the same conditions as above. A mite (either a deutonymph, protonymph, larva, or adult) was transferred by a needle into a small conical-bottomed tube (handmade, 8 mm o.d. × 30 mm ht) and 3 ml of hexane was added. The resulting hexane rinse was collected by a micro-syringe at 3 min (exactly) after introduction of the solvent. All portions of the rinse were then subjected to either GLC or GC/MS analysis. Similar hexane rinses from a substantial amount of mites (not counted) were used for preliminary bioassay and SiO2 column chromatography.

RESULTS AND DISCUSSION Response to a piece of filter paper impregnated with the hexane rinse from deutonymphs indicated the alarm pheromone activity against deutonymphs. GLC and GC/MS analyses revealed that all of the hexane rinses from larva, protonymph and deutonymph were the same, and consisted of two peaks (relative ratio; 94:6, 97:3 and 96:4); peak 1 (the major component, tR: 8.371 min, M+: m/z 152) and peak 2 (the minor component, tR: 8.033 min, M+: m/z 152). These results were identical to those obtained from standard citral, a mixture (relative ratio; 65:35) of geranial (3,7dimethyl-[E]-2,6-octadienal) and of neral (3,7-dimethyl-[Z]-2,6octadienal). Both mass spectra were also identical with those reported by Kuwahara et al. (1980). As a result, the major component commonly present in larva, protonymph and deutonymph was identified as geranial. When the hexane rinse was subjected to an SiO2 column and separated by eluting with a sequence of hexane/ether mixture, the peaks 1 and 2 were both recovered as a mixture in a fraction of 10% ether/hexane eluate. The present chromatographic behavior on SiO2 column was also identical to that of citral. The crushed deutonymphs caused the same level of alarm pheromone activity as that of the filter paper impregnated with 10–100 ng of geranial (isomer purity more than 95%), as shown in Table 1. None of the corresponding activity was observed with neral (isomer purity more than 95%), which was at least 10 times less active (data not shown) than the corresponding geranial. The actual quantity of geranial, determined by GLC, was 91.4 +/20.4 ng (mean +/- S.D., n=10) per deutonymph, and the value was consistent with the bioassay result. As mentioned above, larva

and protonymph also contained geranial as the major component. These facts may suggest pheromonal function of geranial as well, though activities against those stages have not yet been confirmed. Adults indicated no activity against the adult extract or the crushed adult. The GLC profile differed radically from that of the larval-nymphal stages, and geranial was one of the trace components. However, geranial at 100 ng dose was active to adults, for reasons that we have not yet identified. In conclusion, the alarm pheromone found in deutonymphs of Nothrus palustris was identified as geranial. This is the first report of an alarm pheromone in an oribatid mite, though we know of a species of Oribatida that possesses citral, possibly as the component of an oil gland (Sakata et al. 1995), and the same gland is distributed among several cohorts of Oribatida. While many studies on the ecology and biology of this species were reviewed by Krivolutsky (1995) and Lebrun (1970) as a model species of oribatid mites, the occurrence of an alarm pheromone has never been reported. The present identification of the alarm pheromone is the first step in the semiochemical study of the oil glands of Oribatida, and many other examples will certainly be found in future. In the case of astigmatid mites, three kinds of pheromones are at present distributed among total 32 species of Astigmata examined: the alarm (16 species), the aggregation (2 species) and the sex pheromones (5 species), (Kuwahara 1991, 1995; Akiyama et al. 1997; Noguchi et al. 1998). Twelve compounds are now known to be responsible for alarm pheromone activity in a total of 16 species of Astigmata belonging to 7 families. Neral and neryl formate are the most widely distributed pheromones, and both compounds function in each of 5 species (Kuwahara 1995). Geranial is known as the alarm pheromone in only one species. This is the second example of geranial functioning as the alarm pheromone among Astigmata and Oribatida. The opisthosomal gland is a key morphological character shared by some cohorts of Oribatida and most of the Astigmata. Citral may function as a defensive substance, not as an alarm pheromone, due to its strong antifungal activity to environmental micro-organisms (Okamoto et al. 1981). Nothrs palustris occurs in many soil environments in close contact with fungi, and could secrete a small quantity of citral as a defense against them.

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ACKNOWLEDGEMENT This study was supported in part by a Grand-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan (No. 08406010, 09556010, 09876091 and 6379)

REFERENCES Akiyama, M., Sakata, T., Mori, N., Kato, T., Amano, H., and Kuwahara, Y. (1997). Chemical ecology of astigmatid mites. XLVI. Neryl formate, the alarm pheromone of Rhizoglyphus setosus Manson (Acarina: Acaridae) and the common pheromone component among four Rhizoglyphus mites. Applied Entomology and Zoology 32, 75–79. Krivolutsy, D. A. (1995). ‘Oribatid Mites, Morphology, Development, Phylogeny, Ecology, Methods of Study, Model Species Nothrus palustris (C. L. Koch, 1839).’ (Nauka Publishers: Moscow.) Kuwahara, Y. (1991). Pheromone study on astigmatid mites – alarm, aggregation and sex. In ‘Modern Acarology, vol. 1’ (Eds F. Dusbabek and V. Bukva) pp. 43–52. (SPB Academic Publishing bv: The Hague and Academia: Prague.) Kuwahara, Y. (1995). Sex pheromone study of Caloglyphus sp. (Astigmata: Acaridae). Reports of Chemical Materials Research and Development Foundation 10, 45–52. Kuwahara, Y., Fukami, H., Ishii, S., Matsumoto, K., and Wada, Y. (1980). Pheromone study on acarid mites. III. Citral: isolation and identification from four species of acarid mite, and its possible role. Japanese Journal of Sanitary Zoology 31, 49–52.

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Lebrun, P. (1970). Écologie et biologie de Nothrus palustris (C. L. Koch, 1839) Acarien, Oribate: IV. Survivance fécondité action d’un prédateur. Acarologia. 12, 827–848. Noguchi, S., Mori, N., Kurosa, K., and Kuwahara, Y. (1997). Chemical ecology of astigmatid mites. XLIX. ß-Acaridial (2(E)-(4-methyl-3pentenylidene)-butanedial), the alarm pheromone of Tyrophagus longior Gervais (Acarina: Acaridae). Applied Entomology and Zoology 33, 53–57. Norton, R. A., Kethley, J. B., Johnston, D. E. and OConnor, B. M. (1993). Phylogenetic perspectives on genetic systems and reproductive modes of mites. In ‘Evolution and Diversity of Sex Ratio in Insects and Mites’. (Eds D. L. Wrensch and M. A. Ebbert.) pp. 8–99. (Chapman and Hall: New York.) OConnor, B. M. (1984). Phylogenetic relationships among higher taxa in the Acariformes, with particular reference to the Astigmata. In ‘Acarology VI, Vol. 1’. (Eds D. A. Griffiths and C. E. Bowman.) pp. 19–27. (Ellis Horwood Ltd.: Chichester.) Okamoto, M., Mastumoto K., Wada Y., and Kuwahara Y. (1981). Studies on antifungal effect of mite alarm pheromone citral 2. Antifungal effect of the hexane extracts of the grain mites and some analogues of citral. Japanese Journal of Sanitary Zoology 32, 265–270. Sakata, T., Tagami, K., Kuwahara, Y. (1995). Chemical ecology of oribatid mites I. Oil gland components of Hydronothrus crispus. Journal of the Acarological Society of Japan 4, 69–75. Sellnick, M., and Forsslund H.-K. (1955). Die Camisiidae Schwedens (Acar, Oribat.). Arkiv for Zoologi 8, 473–530.

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ACAROLOGY: PROCEEDINGS OF THE 10TH INTERNATIONAL CONGRESS

ECOLOGY AND BIOLOGY OF SOIL MITES

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

REPRODUCTIVE AND NUTRITIONAL BIOLOGY OF TECTOCEPHEUS VELATUS (ACARI: TECTOCEPHEIDAE) IN DIFFERENT BIOTOPES

Department of Zoology Charles University, Vinicˇná 7, 12844 Praha 2, Czech Republic, e-mail: [email protected]

....................................................................................................

Martina Hajmová and Jaroslav Smrzˇ

.................................................................................................................................................................................................................................................................

Abstract Reproductive and nutritional biology of the oribatid mite Tectocepheus velatus were studied in populations inhabiting five adjacent or approximate biotopes in the Czech Republic – agroecosystem, shrubland, calcareous steppe, grassland and pine woodland – over two years. No males were found, and most adult females were gravid with one or two eggs. The juvenile/adult ratio fluctuated during the year and reached higher values at sites with higher value of dominance of T. velatus. Food consumption dynamics and food types did not vary seasonally, and were similar in all biotopes studied. With histological methods, food was observed throughout the year and in all parts of the alimentary tract in all juveniles. In adults, two basic types of food bolus were found: (1) a compact bolus with a surface coat, which sometimes contained hyphae and spores, and (2) a loose substance without any membrane. Bacteria were observed in the mesenteron. Hemocytes were more obvious in specimens with food in the alimentary tract. Thus, among the populations studied the nature of the biotope, including anthropological influences, has a negligible effect on the nutritive and reproductive biology of T. velatus.

INTRODUCTION Tectocepheus velatus (Michael) is one of the most frequent and common species of oribatid mites throughout the world. It is without doubt an extremely ubiquitous species with very wide ecological tolerance, whose habitat can include preserved natural areas or extremely disturbed biotopes, such as agroecosystems or urban environments. It occurs in various moisture regimes, from dry steppes to wet grassland, and from forests to the pioneer stages of succession (Rajski 1961; Kunst 1968; Fujikawa 1988; Stary 1990). Most other oribatids are unable to sustain populations under such a range of conditions. According to many authors, T. velatus is a parthenogenetic mite (Grandjean 1941; Solhøy 1975; Mitchell 1977; Luxton 1981a; Fujikawa 1988, 1995; Smrzˇ 1991). Tectocepheus velatus seems also to be a panphytophagous animal (Luxton 1972), i.e. an unspecialised feeder on plant material and fungi.

Our purpose was to compare populations of T. velatus among various adjacent biotopes. To do this, we studied differences in seasonal abundance patterns, dominance among the oribatid mite community, and several aspects of nutritional and reproductive biology.

MATERIAL AND METHODS Populations of T. velatus were sampled from five different but adjacent biotopes in the region of Prague (Czech Republic): agroecosystem, shrubland, calcareous steppe, grassland and pine woodland. Soil cores were taken monthly for two years – five from each biotope (except 10 cores from the agroecosystem) per month. Cores were in the form of cubes, measuring approximately 7–10 cm per side and weighing 150–200 g. Mites were extracted by Berlese-Tullgren funnels into 80% ethanol or into modified Bouin-Dubosque-Brasil fluid (Smrzˇ, 1989) and subsequently treated according to the following procedures.

255

Martina Hajmová et al.

Figures 1–4

256

Tectocepheus velatus – alimentary tract, sagittal sections. (1) adult mesenteron with food bolus covered with a membrane. (2) adult mesenteron and colon. (3) – juvenile with food in all parts of the alimentary tract. (4) adult mesenteron with fungal spores. Stained with Masson’s trichrome. Scales: 100 µm ( Figs 1, 2, 3), 50 µm (Fig. 4). Abbreviations: fb – food bolus, cns – central nervous system, co – colon, hem – hemocytes, me -mesenteron, rec – rectum, sp – spores.

REPRODUCTIVE

AND

NUTRITIONAL BIOLOGY OF TECTOCEPHEUS

VELATUS

120

Monthly rainfall (mm)

100

80

60

40

20

10/96

9/96

8/96

7/96

6/96

5/96

4/96

3/96

2/96

1/96

12/95

11/95

10/95

9/95

8/95

7/95

6/95

5/95

4/95

3/95

2/95

1/95

12/94

11/94

0

Date Figure 5

Monthly rainfall (in mm) in the vicinity of the study areas. Data from The State Meteorological Institute, in Prague.

AGROECOSYSTEM 50 45 adults

Number of specimens collected

40

juveniles

35 30 25 20 15 10 5 0 11/94 1/95

3/95

5/95

7/95

9/95 11/95 1/96

3/96

5/96

7/96

9/96

Date Figure 6

Monthly abundance of Tectocepheus velatus in an agroecosystem at Prague, Czech Republic, over a two year period. Numbers are pooled from 10 soil cores.

257

Martina Hajmová et al.

SHRUBLAND 70 adults

Number of specimens collected

60

juveniles

50

40

30

20

10

0 11/94 1/95

3/95

5/95

7/95

9/95 11/95 1/96

3/96

5/96

7/96

9/96

Date Figure 7

Monthly abundance of Tectocepheus velatus in a shrubland at Prague, Czech Republic, over a two year period. Numbers are pooled from five soil cores.

GRASSLAND 35

adults

Number of specimens collected

30

juveniles 25

20

15

10

5

0 11/94 1/95

3/95

5/95

7/95

9/95 11/95 1/96

3/96

5/96

7/96

9/96

Date Figure 8

258

Monthly abundance of Tectocepheus velatus in a grassland at Prague, Czech Republic, over a two year period. Numbers are pooled from five soil cores.

REPRODUCTIVE

AND

NUTRITIONAL BIOLOGY OF TECTOCEPHEUS

VELATUS

CALCAREOUS STEPPE 900 adults

800 Number of specimens collected

juveniles 700 600 500 400 300 200 100 0 11/94 1/95

3/95

5/95

7/95

9/95 11/95 1/96

3/96

5/96

7/96

9/96

Date Figure 9

Monthly abundance of Tectocepheus velatus in a calcareous steppe at Prague, Czech Republic, over a two year period. Numbers are pooled from five soil cores.

Mites extracted into ethanol were identified and counted. The abundance and dominance (as percent of the total oribatid mite community) of T. velatus, the presence or absence of males, and juvenile/adult ratios were recorded. Mites extracted into modified Bouin-Dubosque-Brasil fluid were used for histology. They were sectioned (thickness 5000–7000 nm), stained by a modified Masson’s triple stain (Smrzˇ 1989) and observed under the microscope (PROVIS AX 70, Olympus).

RESULTS During two years of sampling, 21,535 specimens of T. velatus were extracted: 10,789 adults and 10,786 juveniles. Among them, 732 adult specimens were studied histologically. Population dynamics varied among the biotopes. In the agroecosystem, abundance reached a maximum in summer and a minimum in winter (Fig. 6). Abundance, especially of juveniles, seemed to correlate with rainfall at this location (Fig. 5). In the shrubland, maximum abundance was in winter, the only period when 10 or more specimens per sample were recorded (Fig, 7); minium abundance was in summer. In the grassland and calcareous steppe biotopes, abundance did not seem to fluctuate with season, but the patterns differed (Figs 8, 9). In the pine woodland variation in abundance was non-periodical, but was higher in the second year of sampling, especially in autumn and winter (Fig. 10). The average dominance of T. velatus also varied among the biotopes. In the agroecosystem it comprised 42% of the oribatid mite community, 8% in the shrubland, 26% in the grassland, 48% in the calcareous steppe, and 58% in the pine woodland.

No males were found among 732 histologically examined adults. Gravid females occurred throughout the year, and comprised approximately 80% of females collected. A maximum of two eggs per female was observed (60–70% ). If the female contained only one egg, it was on the left side of the body cavity; if it contained two eggs, they were placed symmetrically on each side. Nutritional biology was also tested histologically, using specimens from calcareous steppe and pine woodland, where abundance was high. Food was observed in all parts of the alimentary tract in all juveniles from both biotopes, and over the whole year (Fig. 3). Two basic types of food bolus were observed: (1) a compact bolus with a surface membrane covering a mixture of spores and fragmented hyphae (Fig. 1), and (2) a loose bolus of a liquid nature, lacking a membrane, and containing fine granules and bacterial cells (Fig. 2). The first type was typical for mites from the pine woodland and the second was found mainly in specimens from the calcareous steppe, although there was a certain amount of overlap. No seasonal pattern was observed in the structure or occurrence of food boli. Hemocytes were observed irregularly and were conspicuous only in specimens having food in the alimentary tract (Fig.1).

DISCUSSION The population dynamics of Tectocepheus velatus in the vicinity of Prague did not follow any universal seasonal pattern; rather it varied with the biotope investigated. In no biotope did we observe the pattern of summer and winter minima that was reported for this species in Danish beech woodlands by Luxton (1981b).

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PINE WOODLAND 1400

Number of specimens collected

1200

adults juveniles

1000

800

600

400

200

0 11/94 1/95

3/95

5/95

7/95

9/95 11/95 1/96

3/96

5/96

7/96

9/96

Date Figure 10

Monthly abundance of Tectocepheus velatus in a pine woodland at Prague, Czech Republic, over a two year period. Numbers are pooled from five soil cores.

In fact, abundance in the shrubland was maximal in winter. In this biotope abiotic factors seemed to be more favourable (i.e. more effective temperature and moisture buffering) than in the agroecosystem, where a winter minimum was observed. In a similar case, Skaláková (1986) assumed that there was migration between two adjacent biotopes. Both Luxton (1981b) and Solhøy (1975) noted a positive correlation of density with rainfall, but in our locality we could see such a pattern clearly only in the agroecosystem population. The first peak of abundance (summer 1995) coincided with increasing rainfall, as did the second (summer 1996). Overall, 1996 was a wetter year than was 1995 and the number of specimens sampled was likewise higher. A similar general correlation was observed in the grassland and pine woodland biotopes. Various authors have discussed the parthenogenetic reproduction of T. velatus. Luxton (1981a) characterised it as having a strong tendency to parthenogenesis, and both Mitchell (1977) and Smrzˇ (1991) considered it facultatively parthenogenetic. Grandjean (1941) observed a male/female ratio of 1/143. Solhøy (1975) and Fujikawa (1988) found no males in the biotopes which they studied, consistent with our observations. According to some literature, egg production is seasonal. Luxton (1981a), for example, considered it to be linked with environmental conditions. Mitchell (1977) assumed that decreasing moisture and increasing temperature was the trigger for the development of eggs. Further, species with a tendency to parthenogenesis were thought to develop eggs mostly in spring. By contrast,

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no periodicity in the presence of eggs was seen in our study, where 80% of collected females were gravid. Similar results were obtained by Stary (1990); he recognised no regular seasonal peaks of egg production or any correlation with biotope. Our observations on the number of eggs that female T. velatus carried – one or (maximally) two – are rather consistent with the literature. Luxton (1981a) noted an average of 1.1–1.3 eggs per female, with a maximum of four. Fujikawa (1988) reported one or (usually) two eggs per female, with one instance of three eggs. In most botopes studied by Stary (1990) females carried one or two eggs, but in grassland there was an average of 3.5 per gravid female. Tectocepheus velatus seems to be an unspecialised feeder, panphytophagous in the sense of Luxton (1972), hence it is expected to graze the food available in any particular biotope, without specific selection. Our observations seem to confirm this. For example, mites from the pine woodland – with its coarse and acid humus that is dominated by fungal communities – had food boli of the compact type, having a surface membrane and containing spores and hyphae. By contrast, mites from the calcareous steppe, where bacteria are dominant, had boli of the liquid type, containing granules and bacteria.

ACKNOWLEDGEMENTS The authors wish to thank Ivo Lukesˇ, Olympus C & S, for his kind help with the technical preparation of this paper, and Olympus C & S for sponsoring of the authors’ attendance at the Xth International Congress of Acarology. We are grateful to Dr Malcolm Luxton, National Museum of Wales, Cardiff, for his kind

REPRODUCTIVE

linguistic and stylistic review, as well as for useful comments. This project was supported by grant GA¯R 526/96/0250.

REFERENCES Fujikawa, T. (1988). Biology of Tectocepheus velatus (Michael, 1880) and Tectocepheus cuspidentatus Knülle. Acarologia 29, 307–315. Fujikawa, T. (1995 ). Comparison among populations of Tectocepheus velatus (Michael, 1880 ) from forests, grasslands and crop fields. Edaphologia 55, 1–82. Grandjean, F. (1941). Statistique sexuelle et parthenogenese chez les Oribates (Acarines). Comptes Rendus Academie Sciencés 212, 463–467. Kunst, M. (1968). ‘Oribatid Mites of Czechoslovakia, Part I.’ (Dissertation Thesis, Charles University: Prague.) Luxton, M. (1972). Studies on the oribatid mites of a Danish beech wood soil. I. Nutritional biology. Pedobiologia 12, 434–464. Luxton, M. (1981a). Studies on the oribatid mites of a Danish beech wood soil. IV. Developmental biology. Pedobiologia 21, 312–340. Luxton, M. (1981b) Studies on the oribatid mites of a Danish beech wood soil.VI. Seasonal population changes. Pedobiologia 21, 387–409.

AND

NUTRITIONAL BIOLOGY OF TECTOCEPHEUS

VELATUS

Mitchell, M. J. (1977). Vertical and horizontal distribution of oribatid mites (Acari, Cryptostigmata) in an aspen woodland soil. Ecology 59, 516–525. Rajski, A. (1961). Studium ekologiezno-faunistyczne nad mechowcami (Acari, Oribatei) w kielku zespolach róstlinnych, I. Ekologia 15, 1–160. Skalakova, D. (1986). ‘Anatomy and Biology of Two Oribatid Mites of the Family Damaeidae (Acari, Oribatida).’ (Dissteration Thesis, Charles University: Prague.) Smrzˇ, J. (1989). Internal anatomy of Hypochthonius rufulus (Acari, Oribatida). Journal of Morphology 200, 215–230. Smrzˇ, J. ( 1991). ‘Comparative and Functional Microanatomy of Oribatid and Acaridid Mites (Acari).’ (Dissertation Thesis, Charles University: Prague.) Solhøy, T. (1975). Dynamics of Oribatei populations on Hardengervidda. In ‘Ecological Studies. Analysis and Synthesis. Vol, 17, Fennoscandian Tundra Ecosystems, Part 2.’ (Ed. F. E. Wielgolaski.) pp. 60–65. (Springer-Verlag: Berlin.) Stary´, J. (1990.) ‘Ecology of Oribatid Mites ( Acari : Oribatida ) in Succesion Within Soil Systém.’ (Dissertation Thesis, Institute of Soil Biology, Czech Academy of Science: Cˇ eské Budeˇjovice.)

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

FEEDING HABITS OF THE INDIAN ORIBATID MITES HOPLOPHTHIRACARUS RIMOSUS (PHTHIRACARIDAE) AND LOHMANNIA N. SP. (LOHMANNIIDAE) AND THEIR ROLE IN DECOMPOSITION

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N. Ramani and M. A. Haq Division of Acarology, Department of Zoology, University of Calicut, Kerala, India, 673 635 Email [email protected]

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Abstract Oribatid mites perform an active role in the decomposition of organic matter and serve as an important element in the humification process in the soil ecosystem. We examine the potential role in biodegradation of two common species of these mites that represent the important families Phthiracaridae and Lohmanniidae. Individuals of Hoplophthiracarus rimosus Mahunka, 1978 and Lohmannia n. sp. were subjected to a series of laboratory and field studies including food choice tests, gut content examination, enzyme analysis and assessment of nutrients in litter before and after consumption by these mites. Results of food choice tests and gut analysis clearly showed the ability of the two species to degrade higher plant material, particularly woody elements by H. rimosus and leafy components by Lohmannia n. sp.. This was further confirmed through enzyme assays, which demonstrated the release of cellobiase by both species. Concentrations of the macro and micronutrients N, P, K, Fe, Mn, Cu and Zn were significantly higher in litter of Artocarpus integrifolia, after it had passed through the gut of the two study species, confirming the positive involvement of these mites in litter degradation.

INTRODUCTION Organic decomposition represents an important and highly complex process accomplished through diverse types of interactions of various organisms. Soil mites, particularly oribatid mites, influence decomposition through their numerical abundance, feeding diversity and the subtle association they share with microbes in soil. The rate of decomposition is reported to be greater through the combined activities of microbes and mites over that by the microorganisms alone (Harding and Stuttard 1974; Seastedt 1984). It is estimated that 50% of annual leaf fall passes through the gut of oribatid mites (Berthet 1964; Rajski 1966; Coleman 1970). The significant role of macrophytophagous oribatid mites, particularly members of the Phthiracaridae and Lohmanniidae, in the degradation of plant structural polysaccharides has been elucidated qualitatively by many workers (Haq 1984, 1987; Haq and Konikkara 1988; Ramani and Haq 1991). A recent analysis of the nutritional diversity of oribatid mites in relation to soil fertility

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(Haq 1996) focussed on the role of these mites in biodegradation, mineralisation and consequently in nutrient cycling. The present study concentrates on the role of two macrophytophagous oribatid species: Hoplophthiracarus rimosus Maunka, 1978 and Lohmannia n. sp. in the degradation of litter from Artocarpus integrifolia, the common jack fruit.

METHODS Litter samples collected from forest floors at several locations in Kerala, India – Wynad, Silent Valley and Madathara – were extracted in Berlese funnels. Live specimens of H. rimosus and Lohmannia n. sp. were reared in the laboratory in large numbers on woody and leafy fragments, respectively, of A. integrifolia litter. Feeding habits of the species were studied in laboratory and field by food choice tests and the analysis of gut contents, following the methods of Haq (1982, 1984, 1996). Qualitative assays of the various enzyme complexes secreted by the mites followed the tech-

FEEDING HABITS OF HOPLOPHTHIRACARUS

Table 1

LOHMANNIA

Quantitative changes in the macro and micronutrients before and after feeding by Hoplophthiracanus rimorus and Lohmannia n. sp. in the wood and leaf litter of Artocarpus integrifolia. Each sample contains 2 gm weight of dried litter or faecal pellets. T-test results: * significant at P = 0.05, ** significant at P = 0.01. Hoplophthiracarus rimosus

Nutrient N (%)

RIMOSUS AND

Lohmannia n. sp.

No. of samples

Before feeding

After feeding (faecal pellets)

Before feeding

After feeding (faecal pellets)

10

0.34 ± 0.02

*1.23 ± 0.03

1.18 ± 0.01

*1.82 ± 0.85

P (%)

10

0.04 ± 0.01

0.005 ± 0.001

0.006 ± 0.001

**0.02 ± 0.01

K (%)

10

0.084 ± 0.001

*0.55 ± 0.02

0.31 ± 0.01

**0.125 ± 0.009

Fe (%)

10

0.24 ± 0.01

0.14 ± 0.01

0.14 ± 0.01

*0.74 ± 0.036

Mn (ppm)

10

96 ± 0.89

**180 ± 1.26

102 ± 2

*120 ± 0.89

Cu (ppm)

10

24 ± 1.8

*26 ± 0.5

24 ± 0

*56 ± 0.9

Zn (ppm)

10

32 ± 0.5

*46 ± 0.5

64 ± 0.9

**266 ± 0.9

niques of Haq (1982, 1996). The involvement of the mites in the decomposition of litter was assessed quantitatively by studying the nutrient release due to feeding activity of mites. Concentrations of the macro and micronutrients N, P, K, Fe, Mn, Cu and Zn in the leafy and woody litter fragments of A. integrifolia, and in the mite faecal pellets that resulted from feeding on these materials, were estimated. Ten 2 gm samples of each type of litter and faecal pellets were analysed according to the methods of Jackson (1967) and Haq (1996), and data were subjected to statistical analysis by the t-test. Changes in concentration of the various macro and microelements that resulted from mite feeding were taken as an index of the involvement of these mites in litter degradation.

RESULTS Both H. rimosus and Lohmannia n. sp. were abundant in moist litter samples. Results of food choice tests revealed the preference of H. rimosus for woody elements and Lohmannia n. sp. for leafy materials, though each species would feed on the other food if the preferred food was exhausted. Neither species would consume fungi, moss or animal matter. Feeding activity of adult H. rimosus on pieces of wood produced small holes, and combined feeding of many adults led to the appearance of small irregular cavities. These cavities were often used for oviposition and development of the larval and nymphal stages. Subsequent feeding activity of the new generation caused the formation of tunnels and compartments of varying sizes. Such inner cavities and compartments were mostly invaded by the developing immatures. Their faecal matter and exuviae were found packed as a unit and covered by the uneaten outer layer of the wood. Accumulation of moisture enhanced disintegration of the outer covering and scattering of its contents. With further feeding, the entire wood piece was transformed into small, thin strands and finally into a mass of faecal pellets. Lohmannia n. sp. on the other hand exhibited preference for the dead and decaying leaf tissues of A. integrifolia in the laboratory. The adults of Lohmannia n. sp. were found feeding on the surface layers of leaf tissues, producing minute holes. With further feeding such holes coalesced to form still larger holes. The gravid females laid round, white, solitary eggs within these holes. Adults and immatures often attacked parenchymal tissue of the leaves, leaving behind the veins, veinlets and the midrib and imparting a

skeletonised appearance. Continued feeding led to the disappearance of the entire leaf lamina including veinlets, veins and even the midrib. Guts of field collected specimens of H. rimosus contained predominantly partly digested bundles of closely packed fibrous materials, xylem vessels, spiral thickenings and also highly digested materials. The digestive tracts of Lohmannia n. sp. contained parenchymatous cells, guard cells, spiral thickenings and pitted vessels in various stages of decay. Very rarely, fungal spores were recovered from the gut of this species. Qualitative assessment of the various enzymes in the mites revealed the presence of three carbohydrases, maltase, cellobiase and cellulase, in both species. Trehalase was absent from both, indicating the inability of these mites to digest fungi. Results of quantitative analysis of the macro and micronutrients released due to feeding by H. rimosus and Lohmannia n. sp. are presented in Table1. The concentration of both macro and micronutrients generally increased after feeding by mites. After processing by Lohmannia n. sp., N increased in A. integrifolia leaf litter by 0.64% and P increased by 0.014%. However, the percentage of K decreased in the leaf litter. The concentration of the microelements Fe, Mn, Cu and Zn also showed slight increases of 0.6%, 18 ppm, 32 ppm and 202 ppm respectively. Except for P and Fe, concentrations of macro and micronutrients increased after processing of woody litter by H. rimosus; P decreased 0.035% and Fe decreased 0.1%. Most changes were statistically significant.

DISCUSSION Oribatid mites can be very abundant in organic profiles, with as many as 105 individuals per m2 (Crossley 1977) and they are important agents of organic decomposition. During this study, both Lohmannia n. sp. and H. rimosus were always found associated with litter accumulations, especially during the monsoon season. This suggests the dependence of these species on moist litter for their survival. It is possible that availability of moisture during the monsoon triggers microbial invasion of accumulated litter, and such microbially conditioned litter is selected by these two species for feeding. Such a pattern was reported for oribatid mites by various investigators (Jacot 1939; Murphy 1953; Hayes 1963).

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Food choice experiments in the laboratory and gut content analysis showed that both species could be assigned to the macrophytophagous feeding category (Schuster 1956; Luxton 1972) with affinity for higher plant materials. The recovery of fungal spores from the gut contents of Lohmannia n. sp. on a few occasions probably resulted from ingestion of decomposing litter invaded by fungus. During our laboratory feeding trials this species rejected all the fungal species offered. On the basis of food choice test Lohmannia n. sp. could be assigned to the ‘phyllophages’ under the macrophytophagous category showing primary preference for A. integrifolia leaf litter. By contrast, H. rimosus is a ‘xylophage’ with greater preference for woody ingredients of the litter. The enzymes necessary for degradation of the structural polysaccharides, maltase, cellulase and cellobiase were found in both species but trehalase was not recorded in either species. The above observation clearly supports the conclusion of Haq (1996) that the presence of cellulase or cellobiase or both without trehalase can be considered as an index for macrophytophagy. When considering the role played by oribatid mites in decomposition and resultant nutrient flux, panphytophages and microphytophages are considered of prime importance (Wallwork 1958, 1976) because of their stimulation and reactivation of the senescent microbial colonies by producing a ‘culling effect’ through feeding (Mitchell and Parkinson 1976; Wallwork 1983; Neena and Haq 1992) in different layers of the soil profile. These mites are designated as ‘catalysts’(Behan and Hill 1978) serving to unlock the ‘nutrient pools’ present in the ‘key industry’ of the soil ecosystem (Wallwork 1983). The macrophytophages, though not equipped to feed and digest fungal materials, are able to ingest quantities of litter and break it down mechanically through mastication. Mastication exposes the resistant compounds in litter, which later get concentrated in the faecal pellets, converting them to nutrient rich foci (Macfayden 1961). Moreover, comminution of litter by the macrophytophages results in an increase in surface area, accessible to activities of microbes, especially bacteria (Engelmann 1961). These faecal pellets of macrophytophages, with increased nutrient content, are easily colonised by microbes (Zachariae 1965; Labandeira et al 1997). Thus, fragmentation of litter by macrophytophages serves to enhance the rate of decomposition. This study showed that the feeding activity of H. rimosus and Lohmannia n. sp. increases the nutrient status of the litter of A. integrifolia. Both the macro and micronutrients were increased, though exceptions were evident. A decline in the concentration of P was visible in the woody litter of A. integrifolia, whereas the leafy litter showed a decrease in the concentration of K. The mobility of K is said to be greater and hence it is possible that the element might have been subjected to increased rate of leaching and hence rapid removal (Cromack et al. 1975; Wallwork 1983; Haq 1996). The decline observed in the accumulation of P may be due to chemical precipitation (McBrayer 1977). The quantitative increase in most of the nutrients observed as a result of feeding must be a reflection of the synergistic effect of the mites and their gut microbes. Faecal pellets accumulating on the soil surface are easily invaded by microorganisms. On subsequent hydration, the rate of leaching of hydrosoluble elements is accelerated (Van der

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Drift and Witkamp 1960; Witkamp and Crossley 1966) thereby creating a highly fertile environment in the soil ecosystem. This study shows the potential of two species of oribatid mites, representing the families Lohmanniidae and Phthiracaridae, in such processes. They respectively degrade the leafy and woody components of Artocarpus integrifolia litter, in both field and laboratory conditions, and are involved in the release of nutrients by action of their feeding.

ACKNOWLEDGEMENT The authors are grateful to the Department of Science and Technology, Government of India, New Delhi for the financial assistance extended through a major research project, during the tenure of the work.

REFERENCES Behan, V. M. and Hill, S. B. (1978). Feeding habits and spore dispersal of oribatid mites in the North American arctic. Revue d’ Ecologie Biologie du Sol 15, 497–516. Berthet, P. (1964). L’ activite des oribatides d’une chenaie. Memoires Institut Royal des Sciences Naturelles de Belgique 152, 1–152. Coleman, D. C. (1970). Food webs of small arthropods of a broom sedge field studied with radio-isotope-labelled fungi. In ‘Proceedings of .Symposium on Methods of Study in Soil Ecology.’ pp. 203–207. (HBP-UNESCO: Paris.) Crossley, D. A. Jr. (1977). Oribatid mites and nutrient cycling. In ‘Biology of Oribatid Mites.’ (Ed. D. L.Dindal.) pp. 71–85. (State University of New York: Syracuse, New York.) Cromack, K. Jr., Todd, R. L., and Monk, C. D. (1975). Patterns of basidiomycete nutrient accumulation in conifer and deciduous forest litter. Soil Biology and Biochemistry 7, 265–268. Engelmann, M. D. (1961). The role of soil arthropods in the energetics of an old field community. Ecological Monographs 31, 221–238. Haq, M. A. (1982). Feeding habits of ten species of oribatid mites (Acari: Oribatei) from the soils of Malabar, South India. Indian Journal of Acarology 6, 39–50. Haq, M. A. (1984). The role of microbes in the nutrition of a lohmanniid mite (Acari: Oribatei). In ‘Acarlogy VI, vol. 2.’ (Eds. D. A. Griffiths and C. E. Bowman.) pp. 819–825. (Ellis Horwood: Chichester.) Haq, M. A. (1987). Biodegradation of cellulose in the gut of Heptacarus hirsutus Wallwork, 1964 (Acari: Oribatei). In ‘Soil Fauna and Soil Fertility’ (Ed. B. R. Striganova.) pp. 93–98. (Nauka: Moscow.) Haq, M. A. (1996). Nutritional diversity of oribatid mites in relation to soil fertility. Journal of Karnatak University Science, Special Issue 76–96. Haq, M. A., and Konikkara, I. D (1988). Microbial associations in xylophagous oribatid mites. In ‘Progress in Acarology Vol. I.’ (Eds. G. P. ChannaBasavanna and C. A.Viraktamathi.) pp. 469–474. (Oxford and IBH Publishing: New Delhi.) Harding, D. J. L., and Stuttard, R. A. (1974). Microarthropods. In ‘Biology of Plant Litter Decomposition, vol. 2.’ ( Eds C. H. Dickinson and G. J. F. Pugh.) pp. 489–532. (Academic Press: London.) Hayes, A. J. (1963). Studies on the feeding preference of some phthiracarid mites. Entomologia Experimentalis et Applicata 6, 241–256. Jackson, M. L. (1967). ‘Soil Chemical Analysis.’ (Prentice Hall Inc.: Englewood Cliffs, New Jersey.) Jacot, A. P. (1939). Reduction of spruce and fir litter by minute animals. Journal of Forestry 37, 858–860. Labandeira, C. C., Philips, T. L., and Norton, R. A. (1997). Oribatid mites and the decomposition of plant tissues in Paleozoic coal swamp forests. Palaios 12, 319–353.

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Luxton, M. (1972). Studies on the oribatid mites of a Danish beech wood soil. Pedobiologia 12, 434–463. McBrayer, J. F. (1977). Contributions of cryptozoa to forest nutrient cycles. In ‘The Role of Arthropods in Forest Ecosystems.’ (Ed. W. J.Mattson.) pp. 70–77. (Springer. New York.) Macfayden, A. (1961). Metabolism of soil invertebrates in relation to soil fertility. Annals of Applied Biology 49, 215–218. Mitchell, M. J., and Parkinson, D. (1976). Fungal feeding of oribatid mites (Acari: Cryptostigmata) in an aspen woodland. Ecology 57, 302–312. Murphy, P. W. (1953). The biology of forest soils with special reference to the mesofauna or meiofauna. Journal of Soil Science 4, 155–193. Neena, P., and Haq, M. A. (1992). Mycophagy in oribatid mites. In ‘Man, Mites and Environment’ (Ed. M. A. Haq and N. Ramani) pp. 62–70. (Anjengo Publications: Calicut.) Rajski, A. (1966). Stosunki pokarmowe u mechowcow (Acari: Oribatei). Zeszyty Problemowe Postepow Nauk Rolniczych 65, 237–248. Ramani, N. and Haq, M. A. (1991). Potential of Meristacarus degradatus and Xylobates rhomboides (Acari; Oribatei) in the degradation of higher plant materials. In ‘Modern Acarology Vol.1’ (Eds. F. Dusbabek and V. Bukva.) pp. 411–415. (Academia: Prague and SPB Academic Publishing: The Hague.)

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LOHMANNIA

Schuster, R. (1956). Der Anteil der Oribatiden an den Zersetzungsvorgangen in Boden. Zeitschrift fur Morphologie und Okologie de Tiere 45, 1–33. Seastedt, T. R. (1984). The role of microarthropods in decomposition and mineralization processes. Annual Review of Entomolology 29, 25–46. Van der Drift, J. and Witkamp, M. (1960). The significance of the break down of oak litter by Eniocyla pusilla Burm. Archives Neerlandaises de Zoologie 13, 486–592. Wallwork, J. A. (1958). Notes on the feeding behavior of some forest soil Acarina. Oikos 9, 260–271. Wallwork, J. A. (1976). ‘The Distribution and Diversity of Soil Fauna.’ (Academic Press: London.) Wallwork, J. A. (1983). Oribatids in forest ecosystems. Annual Review of Entomology 28, 109–130. Witkamp, M. and Crossley, D. A. Jr. (1966). The role of arthropods and microflora in breakdown of white oak litter. Pedobiologia 6, 293–303. Zachariae, G. (1965) Spuren tierisher Tatigkeit im Boden des Buchenwaldes. Forstwissenschaftliche Forschungen 20, 1–68.

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EFFECTS OF MOISTURE REGIME ON THE NUTRITIONAL BIOLOGY OF SAPROPHAGOUS SOIL MITES (ORIBATIDA AND ACARIDIDA)

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Jaroslav Smrzˇ Department of Zoology, Charles University, Vinièná 7, CZ-12844 Praha 2, Czech Republic (e-mail [email protected])

.................................................................................................................................................................................................................................................................

Abstract Microbial communities commonly shift between fungal and bacterial dominance, but little is known of how the mites associated with such communities respond to these changes. Two mite species, Trichoribates trimaculatus (Oribatida) and Tyrophagus putrescentiae (Acaridida), which are respectively algophagous and mycophagous, were subjected to two moisture regimes in laboratory cultures using algal-covered bark as substrate and initial food source. Data were collected by histology, faecal pellet investigation and enzyme activity tests, and several phenomena were noted; (a) The mycophage gradually adapted to feeding on invading microbes, but the algophage did not; (b) Palatable food can be harmful under some circumstances (high moisture); (c) When palatable food is not available, excrements and bacteria, which have a low nutritional value for mites, can be substituted; (d) Feeding activity of the mycophage ameliorated culture conditions for the algophage, indicating that mycophages play an important role in the balance of simple mite communities, at least under experimental conditions; (e) The pattern in which species are introduced (together or separately) is a significant factor affecting the processes in simple mite communities.

INTRODUCTION There are three ways in which an organism can respond to changing environments: extinction, migration or adaptation. Particular responses differ according to the type and value of external factors as well as the predispositions of the organism. Previously (Smrzˇ 1996) I examined such responses of certain soil mites under the direct effects of extreme moisture conditions (inundation or drought). Soil moisture can affect mite communities directly through osmotic effects, by drying or invasion of water into the body (Madge 1964; Vannier 1978), and by increasing oxygen deficiency. But indirect effects also exist, and some relate to nutritional biology. These include the general influence of moisture on the environment, the potential available food and selection preferences and, subsequently, on the formation of intermetabolites. Most food selection experiments have been based on ‘cafeteria tests’ or investigation of the food in the gut of animals cleared in

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lactic acid (Czajkowska 1970; Behan and Hill 1978; PankiewiczNowicka et al. 1984) . However, it is also important to study certain internal processes in relation to the environment. These include the actual digestion in the gut and the assimilation of nutrients, enzyme production, and the internal microbial communities. Smrzˇ and Cˇ atská (1989) noted that the nutritional value of fungal food probably resulted in different patterns of consumption (sucking, crushing, etc.) and different assimilation inside the body of Tyrophagus putrescentiae. Again, these differences have resulted from the specificity of food, consumers and environmental conditions. This paper examines how two microphytophagous (sensu Luxton 1972; i.e. feeding on microorganisms including algae, fungi and bacteria) species of soil mites, Tyrophagus putrescentiae (Schrank) (Acaridida: Acaridae) and Trichoribates trimaculatus (C. L. Koch) (Oribatida: Ceratozetidae), respond to changes in moisture

NUTRITIONAL BIOLOGY OF SAPROPHAGOUS

regime. Feeding preferences, histology, faecal pellets and enzyme activity were all examined to better understand their nutritional biology.

MATERIAL AND METHODS Our laboratory has established several complementary methods to examine the nutritional biology of saprophagous soil mites, viz. histology, faecal analysis, enzyme (especially chitinase) production, plating of microorganisms (Smrzˇ 1989, 1992, 1994, 1996; Smrzˇ and Cˇ atská 1987, 1989; Smrzˇ et al.1991; Smrzˇ and Trelová 1995). In combination they can reveal the pathway of the consumed substrate inside the mite body and various nutritional processes. The two mite species were reared on algae (Protococcus sp.) growing on the bark of oak. Such algae have proven very palatable for many soil saprophagous mites (Sengbusch 1954, 1963; Littlewood 1969). Algal-covered bark fragments were placed on a plaster-of-Paris and charcoal mixture within glass jars, and 40 mites of each species were introduced. Tyrophagus putrescentiae is considered omnivorous, but with fungal preferences, while Trichoribates trimaculatus ate only the algae (algophagous specialist). Mites were introduced in two patterns: (1) both species were introduced simultaneously; (2) T. trimaculatus was introduced followed, after five days, by T. putrescentiae. Two moistening intervals were tested: three and six days. All experiments were performed at laboratory temperature (approx. 22°C). All experiments were triplicated and mites for analysis were sampled regularly up to the end of the experiments . The histological and enzyme tests have been described in previous papers (Smrzˇ and Cˇ atská 1987, 1989; Smrzˇ 1989, 1992, 1994, 1996).

SOIL MITES

T. putrescentiae fell due to the ‘white-body syndrome’ (Smrzˇ and Cˇ atská 1987), in spite of the clear palatability of food consumed. By contrast, the population of the algophagous T. trimaculatus fell after the initial active stage and no mites survived after several days. Fungal propagules appeared in food boli in the gut, but boli became smaller and eventually lost their usual spherical shape. Bolus structure was loose and mucoid, with scarce granules only. They were formed in the mesenteron, but were deformed or quite lacking in some parts. The usual accompanying phenomena (hemocytes, enzyme granulation in gut walls, glycogen deposits) also gradually disappeared. These phenomena occurred in experiments in which the mites were introduced sequentially, and especially under the three-day moistening regime. Under the six-day regime these effects were slower to develop or poorly expressed. If the mites were introduced to the algal cover simultaneously, the algophagous population survived until the algae was totally consumed, and even several days after that. The fungal community was poorer, if any mycelium was visible at all. The quantity of faecal pellets increased as algae and fungi were consumed. Under the three-day moistening regime a moist or slimy bacterial film developed. Mites of both species were able to consume faecal pellets. These seemed to be more palatable to juveniles, which exhibited food boli in all parts of their alimentary tract during the consumption of excrements. Again, the excrements were black, consistent with the consumption of fungi. Such food prolonged the survival of the mite populations despite the absence of algae. Chitinase activity decreased in parallel with the reduction of this food, as did population growth. Eventually, when all potential food was exhausted, mites of both species tried to leave the experimental jars. T. putrescentiae seemed to be more successful at this than T. trimaculatus.

RESULTS The first stage of consumption involved only algae, and this resulted in only algal cells being present in all parts of the gut and excrements. Tests for chitinase proved negative for both mite species. After several days, fungal spores and mycelium occasionally appeared in gut and faeces of both mites, although no visible fungi were detected on the algal cover. The excrements became dark to black. At this point chitinase activity was recorded in both mites. Fungi became gradually visible on the algae, and the numbers of fungal propagules increased within the mite gut and excrement, which was quite black. Simultaneously there was chitinase activity in the homogenate of each mite species. These processes were more rapid under the three-day interval of moistening. The fungal communities became gradually more diversified and included several sporulating species. The population of the mycophagous T. putrescentiae increased as they continued to graze on fungi. The assimilation of such palatable food was confirmed by food boli in all parts of the alimentary tract and by groups of hemocytes inside the body. Mycetome-like bodies filled by associated microorganisms were formed. This mite tended to adapt to several strains of fungi invading the experimental jars, and the time of such changes differed according to the strain or species of fungus. During the third week of the experiment under the three-day moistening interval, the population of

DISCUSSION The simultaneous introduction of both mites – algophagous and mycophagous – can balance the microhabitat. Mycophagous mites grazed and removed the gradually invading fungi and the algal cover remained relatively pure and favourable for algophagous mites for some time. Such nutritional specialisation can be one factor affecting the diversity and balance of both mite and microbial communities (Woodring and Cook 1962; Anderson 1977; Siepel and Ruiter-Dijkman 1993). On the other hand, sequential introduction of algophagous and mycophagous mites results in a more diversified and flourishing fungal community. Some fungal species are probably noxious to non-mycophagous mites, which are lost from the community. The onset of fungal development was not visible on the algal cover, but was revealed in the gut and excrements of the mites. Under moist conditions, the shift to bacterial communities gradually suppressed the fungal and mite populations. Bacteriophagous mites appear to be uncommon in soils (Luxton 1972). Moreover, high moisture can affect oxygen content and result in a great amount of metabolites from the dense bacterial population. The antagonistic activity of some bacteria probably suppresses the fungal population (Smrzˇ and Cˇ atská 1987, 1989; Smrzˇ et al. 1991).

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Faecal pellets can supply food for some time. Coprophagy seemed to be especially suitable for juveniles, perhaps as an intermediate food or a temporary substitute for more palatable food. Their nutritional value appeared to be lower, as indicated by the parameters mentioned above, but it was sufficient for some time. Faecal pellets might be called ‘hermit’s nutrition’ and such feeding was noted on fungal substrates as well (Smrzˇ and Cˇ atská 1987). Generally, processes and phenomena similar to those mentioned above for algal substrates can also be seen with fungus substrate (Smrzˇ et al. 1991), as well as with cellulose-rich substrates such as litter or filter paper (Smrzˇ 1996). Changes of food choices, brought about by changes of the microbial communities, invasion of fungal or bacterial species, and their antagonisms or synergies, can be induced by fluctuating moisture as well. The responses of the mite consumers result from a combination of external factors and the predisposition of the particular species.

ACKNOWLEDGEMENTS I wish to thank Ivo Lukesˇ, Olympus C & S, for his kind technical help, and Olympus C & S for supporting my attendance at the Xth International Congress of Acarology. I am grateful to Dr Malcolm Luxton, National Museum of Wales, for his kind linguistic and stylistic review of this paper and for very useful comments. This study was supported by grant GACR 526/96/0250.

REFERENCES Anderson, J. M . (1977). The organization of soil communities. Ecological Bulletin (Stockholm) 25, 15–23. Behan, V. M. and Hill, S. B. (1978). Feeding habits and spore dispersal of oribatid mites in the North American arctic. Revue de Écologie et Biologie de Sol 15, 497–516. Czajkowska, B.(1970). Development of acarid mites on some fungi. Zeszyty problemove Polske Nauk rolnicznych 109, 119–127. Littlewood, C. F. (1969). A surface sterilization technique used in feeding algae to Oribatei. In ‘Proceedings of the 2nd International Congress of Acarology.’ (Ed. G. O. Evans.) pp. 53–56. (Akadémiai Kiádó: Budapest.) Luxton, M. (1972). Studies on the oribatid mites of a Danish beech wood soil. I. Nutritional biology. Pedobiologia 12, 434–463. Madge, D. S. (1964). The humidity reactions of oribatid mites. Acarologia 6, 566–594.

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Pankiewicz-Nowicka, D., Boczek, J., and Davis, R. (1984). Food selection in Tyrophagus putrescentiae (Schrank) (Acarina, Acaridae). Journal of the Georgia Entomological Society 19, 317–321. Sengbusch, H. G. (1954). Studies on the life histories of three oribatid mites with observations on other species. Annals of the Entomological Society of America 47, 587–591. Sengbusch, H. G. (1963). Methods recommended for the preparation and culture of Oribatei. In ‘Advances in Acarology, vol. 1.’ (Ed. J. A. Naegele.) pp. 181–1.190. (Cornell University Press: Ithaca, New York.) Siepel, H., and Ruiter-Dijkman, E. M. (1993). Field guilds of oribatid mites based on their carbohydrase activities. Soil Biology and Biochemistry 25, 1491–1497. Smrzˇ, J. (1989). Internal anatomy of Hypochthonius rufulus (Acari, Oribatida). Journal of Morphology 200, 215–230. Smrzˇ, J. (1992). Some adaptive features in the microanatomy of mossdwelling oribatid mites (Acari: Oribatida) with respect to their ontogenetical development. Pedobiologia 36, 306–320. Smrzˇ, J. (1994). Survival of Scutovertex minutus (Koch) (Acari: Oribatida) under differing humidity conditions. Pedobiologia 38, 448–454. Smrzˇ, J. (1996). Some aspects of the life strategy of oribatid mites (Acari: Oribatida). In ‘Acarology IX, vol. 1. Proceedings.’ (Eds R. Mitchell, D. J. Horn, G. R. Needham and W. C. Welbourn.) pp. 253–255. (Ohio Biological Survey: Columbus.) Smrzˇ, J. and Cˇ atská, V. (1987). Food selection of the field population of Tyrophagus putrescentiae (Schrank) (Acari, Acarida). Zeitschrift für Angewandte Entomologie 104, 329–335. Smrzˇ, J. and Cˇ atská, V. (1989). The effect of the consumption of some soil fungi on the internal microanatomy of the mite Tyrophagus putrescentiae (Schrank) (Acari, Acaridida). Acta Universitatis Carolinae-Biologica 33, 81–93. Smrzˇ, J., Svobodová, J. and Cˇ atská, V. (1991). Synergetic participation of Tyrophagus putrescentiae (Schrank) (Acari, Acaridida) and its associated bacteria on the destruction of some soil micromycetes. Journal of applied Entomology 111, 206–210. Smrzˇ, J. and Trelová, M. (1995). The associations of bacteria and some soil mites (Acari: Oribatida and Acaridida). Acta Zoologica Fennica 196, 120–123. Vannier, G. (1978). La resistance a la dessication chez les premiers arthropodes terrestres. Bulletin Societé Ecophysiologique 3, 13–42. Woodring, J. P., and E. F.Cook (1962). The biology of Ceratozetes cisalpinus Berlese, Scheloribates laevigatus Koch and Oppia neerlandica Oudemans (Oribatei) with a description of all stages. Acarologia 4, 101–137.

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

TALUS FORMATIONS – REMARKABLE BIOTOPES FOR ACAROLOGICAL RESEARCH, WITH EXAMPLES FROM THE RHAGIDIIDAE (ACARI: PROSTIGMATA)

Institute of Landscape Ecology, Czech Academy of Sciences, Na sádkách 7, 370 05 Cˇ eské Budeˇjovice, Czech Republic

....................................................................................................

Miloslav Zacharda

.................................................................................................................................................................................................................................................................

Abstract Talus formations are distinct biotopes that previously have not been recognised and included in acarological field research. Sampling at 51 talus formations in the Czech Republic and Austria resulted in the collection of 34 species of the predatory mite family Rhagidiidae. Most of these are psychrophilous species known from such habitats as woodland or meadow litter, but six are new to science and several represent unusual, disjunct populations. Among the latter are Rhagidia gelida, R. breviseta, R. parvilobata, Coccorhagidia pittardi and Poecilophysis recussa which were previously known only from colder climates, and Foveacheles terricola, which was previously known only from caves.

INTRODUCTION Talus or scree formations develop through mechanical weathering of resistant bedrock and are abundant in zones of periglacial activity. At lower latitudes in central Europe, this occurred along vast periglacial zones facing northern continental and alpine glaciers during the Pleistocene glaciation. Presently, this weathering activity is dominant at high altitudes in mountains. In central Europe talus formations have a disjunct, island-like distribution. Research has documented remarkable horizontally as well as vertically diversified and stratified microclimate between upper and lower portions of these formations (Ru˚ ˇz icˇka et al. 1995; Molenda 1996). The upper portions have a warm, xeric surface whilst the lower portions are usually cool and moist. Remarkable microclimatic gradients usually develop between the top and bottom parts and in the deep internal spaces of the talus formations. Warm ascending air streams are characteristic of top areas of the formations in winter, whereas cool air streams out of fissures at the bottom of the talus formations during spring and summer. It has been discovered that internal spaces between talus fragments can retain an ice core, or an extrazonal permafrost,

throughout the year. In contrast, the internal spaces between talus fragments are characterised, at some depth, by a constant microclimate resembling that in large deep caves. In such talus formations, individual ecosystems have evolved that have remained virtually unchanged or only minimally altered by man through the Holocene. These ecosystems contribute significantly to the microclimatic and biological diversity of regional landscapes (Ru˚ ˇz icˇka 1993) and support little-known xeric as well as boreal or arctic relict taxa dwelling within the subterranean spaces between talus fragments (Ru˚ ˇz icˇka 1990; Zacharda 1993; Ru˚ ˇz icˇka and Zacharda 1994; Molenda 1996; Molenda et al. 1997). Different communities of invertebrates, mostly beetles, spiders and mites, occupy different vertical strata of the talus formations (Ru˚ ˇz icˇka and Zacharda 1994, Ru˚ ˇz icˇka et al. 1995). Included among the mite fauna of these formations are members of the predatory family Rhagidiidae, and my purpose is to summarise what is currently known about their associations with talus formations in central Europe.

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Miloslav Zacharda

MATERIAL AND METHODS Rhagidiid mites were collected at 51 localities with talus formations in the Czech Republic and Austria. In the Czech Republic, these localities are situated mostly in the ¯eské St≈edoho≈í Mts and along the northern mountainous state border facing Germany and Poland. In Tyrol, they are in Oetztal Alps, in the vicinity of Obergurgl (11º02'E, 46º52'N). The structure of the talus formations makes zoological investigations difficult, particularly in deeper subterranean strata. Mites living on the surface (epigeic) were collected by hand-sorting, using a small aspirator containing ethanol as a preservative, or were extracted from sod or litter by using Tullgren funnels. Mites (and other arthropods) inhabiting internal spaces between talus fragments, were collected with large winged pitfall traps made of rigid plastic, about 13 cm high and 10.5 cm in diameter (Ru˚ ˇz icˇka 1988). These were positioned approximately 10, 50, and 100 cm under the surface of the talus formation and contained a mixture of 7% formalin and 20% glycerol, plus a few drops of detergent. They were left in place for one year, after which they were removed and the catch processed in the laboratory.

RESULTS AND DISCUSSION To date, 34 species of rhagidiid mites have been found to inhabit the sampled talus formations. Usually only one to three species were collected in any particular talus formation. However, in the alpine zone of the Oetztal Alps, Tyrol, where the rhagidiid mites were collected mostly by hand sorting, three to eight species were collected in each locality. From an ecological viewpoint, most species collected in the talus formations are psychrophilous (humidity-loving) species known from such habitats as woodland or meadow litter. However, some have more interesting ecological, biogeographic and evolutionary aspects, and these are discussed below. Rhagidia gelida Thorell, 1872 is an arctic species with circumpolar distribution. Previously, this species has been collected in northern Scandinavia, Siberia, arctic Canada and Alaska (Zacharda 1993). The Czech Republic is the most southern country where R. gelida has been discovered. Disjunct populations of this large psychrophilous rhagidiid mite live in cool, moist talus formations located along the northern mountain border of the Czech Republic. In such sites ice is often preserved throughout the year. The disjunct populations of R. gelida dwelling in geographically segregated refuges in cool talus formations are hypothesised to be glacial relicts. Whether the Czech populations represent a separate, allopatric or parapatric speciation event has not been examined. Rhagidia breviseta Zacharda, 1995 and R. parvilobata Zacharda, 1995 were previously known only from northern Quebec, Canada, Alaska and northern Siberia (Zacharda 1995). Recently, R. breviseta was discovered in a talus formation retaining ice in central Bohemia, and R. parvilobata was collected in alpine talus formations in the Oetztal Alps in Tyrol. Similarly, Coccorhagidia pittardi Strandtmann, 1971 was known only from tundra in Alaska. Recently, this species was collected in talus formations in alpine habitats in the High Tatras, Slovakia, and in the Oetztal Alps, Tyrol. These three species, found in disjunct, cool talus for-

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mations of central Europe, are all considerd to be glacial, or even pre-glacial, relicts. Poecilophysis recussa (Thor, 1909) was previously known from northern Siberia, but recently was collected in alpine talus formations in the Krkonosˇe Mts (Zacharda 1993) and the Jeseníky Mts, North Bohemia and Moravia, respectively. This species is considered a glacial relict in the Czech Republic. Further, it is morphologically very similar to the derived species P. spelaea (Wankel, 1861) which occurs in European caves from Scandinavia (Zacharda 1980; Hippa et al. 1989) to Roumania (Baltac 1976). The troglobitic P. spelaea is considered a descendant species of P. recussa (Zacharda 1993). Recently, P. spelaea was collected in the Czech Republic in deep strata of various talus formations, where it lives in dark and moist spaces between talus fragments. Thus, like typical large caves, talus formations have offered an evolutionary setting for adaptive partitioning of this troglobiont mite lineage. Similar evolutionary trends were recently documented also in spiders dwelling in stony debris (Ru˚ ˇz icˇka 1999). Foveacheles terricola (C. L. Koch, 1835) has only been known from caves in western and central Europe (Zacharda 1980). Recently this species was discovered in the subterranean spaces of a talus slope in central Bohemia. F. terricola is probably a primarily psychrophilous species that dwells in moist, cool litter and subterranean spaces in talus formations from which it has migrated into caves. Six new species of rhagidiid mites from the genera Foveacheles, Rhagidia, Evadorhagidia and Troglocheles have been discovered in talus formations, and are being described separately. New species of Troglocheles from talus formations in alpine habitats of the Oetztal Alps, Tyrol, may represent adaptive sympatric speciation. These derivative talus formations are geologically young, and only recently became available for colonisation by mites having potential for adaptation to the talus environment. As with Poecilophysis recussa and P. spelaea, mentioned above, the environment of talus formations seems to offer the evolutionary opportunity for ecological partitioning, which is viewed as prerequisite for sympatric speciation and the establishment of novel phenotypes through interruption of gene flow (Brooks and McLennan 1991). In central Europe, and probably also in other parts of the world, talus formations are remarkable disjunctive, island-like biotopes that preserve unique communities of mites and offer various opportunities for acarological research. New or relict species of mites remain to be discovered and various aspects of their adaptive ecological speciation are open for study. It will be fruitful to apply molecular methods to studies of their systematics (e.g. Symondson and Hemingway 1997) and genetic differences among disjunct populations (e.g. Nei 1972; Thorpe 1982). From this aspect, those talus formations that retain ice or extrazonal permafrost are the most promising, and acarologists are encouraged to study such ecosystems throughout the world.

ACKNOWLEDGEMENTS I wish to thank Biocont Laboratory Ltd., Brno, Czech Republic, for supporting my attendance at the 10th International Congress of Acarology in Canberra. I am also indebted to Dr Valerie

TALUS FORMATIONS – REMARKABLE BIOTOPES FOR ACAROLOGICAL

Behan-Pelletier, Eastern Cereal and Oilseed Research Centre, Agriculture and Agri-Food Canada, Ottawa , Dr Malcolm Luxton, National Museum of Wales, and Dr Roy A. Norton, SUNY College of Environmental Science and Forestry, Syracuse, NY, USA, for their stimulating criticism, linguistic revision and help with preparation of this manuscript.

REFERENCES Baltac, M. (1976). Remarques sur quelques Rhagidiidae des Carpates Méridionales. Deux nouvelles espéces: Rhagidia strandtmanni n.sp. et Rhagidia grandjeani n.sp. (Acarina-Actinotrichida-Prostigmata). Travaux de l`Institut de Spéologie Émile Racovitza 15, 53–61. Brooks, D. R., and McLennan, D. A.(1991). ‘Phylogeny, Ecology, and Behavior, a Research Program in Comparative Biology.’ (University of Chicago Press: Chicago.) Hippa, H., Koponen, S., Mannila, R., and Zacharda, M. (1989). Invertebrates of Scandinavian caves VIII. Acari: Rhagidiidae. Notulae Entomologicae 69, 59–62. Molenda, R. (1996). Zoogeographische Bedeutung Kaltluft erzeugender Blockhalden im außeralpinen Mitteleuropa: Untersuchungen an Arthropoda, insbesondere Coleoptera. Verhandlungen des naturwissenschaftlichen Vereins in Hamburg 35, 5–93. Molenda, R., Wunder, J., und Möseler, B.M. (1997). Leptusa simoni Eppelsheim, 1878 (Coleoptera: Staphylinidae) in einer Kaltluft erzeugenden Basaltblockhalde im Hundsbachtal bei Gerolstein / Eifel. Decheniana (Bonn) 150, 321–327. Nei, M. (1972). Genetic distance between populations. American Naturalist 106, 283–292.

RESEARCH

Ru˚zˇicˇka, V. (1988). The longtimely exposed rock debris pitfalls. Veˇstník Cˇeskoslovenské Spolecˇnosti Zoologické 52, 238–240. Ru˚zˇicˇka, V. (1990). The spiders of stony debris. Acta Zoologica Fennica 190, 333–337. Ru˚zˇicˇka, V. (1993). Stony debris ecosystems-sources of landscape diversity. Ekológia (Bratislava) 12, 291–298. Ru˚zˇicˇka, V. (1999). The first steps in subterranean evolution of spiders (Araneae) in Central Europe. Journal of Natural History 33, 255–265. Ru˚zˇicˇka, V., Hajer, J. and Zacharda, M. (1995). Arachnid population patterns in underground cavities of a stony debris field (Araneae, Opiliones, Pseudoscorpionidea, Acari: Prostigmata, Rhagidiidae). Pedobiologia 39, 42–51. Ru˚zˇicˇka, V. and Zacharda, M. (1994). Arthropods of stony debris in the Krkonosˇe Mountains, Czech Republic. Arctic and Alpine Research 26, 332–338. Symondson, W. O. C., and Hemingway, J. (1997). Biochemical and molecular techniques. In ‘Methods in Ecological and Agricultural Entomology.’ (Eds D. R. Dent and M. P. Walton.) pp. 293–350. (CAB International: Wallingford.) Thorpe, J. P. (1982). The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. Annual Review of Ecology and Systematics 13, 139–168. Zacharda, M. (1980). Soil mites of the family Rhagidiidae (Actinedida: Eupodoidea), morphology, systematics, ecology, Acta Universitatis Carolinae-Biologica 1978, 489–785. Zacharda, M. (1993). Glacial relict Rhagidiidae (Acari:Prostigmata) from superficial underground enclosures in the Krkonosˇe Mountains, Czechoslovakia. Journal of Natural History 27, 47–61. Zacharda, M. (1995). New taxa of Rhagidiidae (Acari:Prostigmata) from North America. Part III-A. Genus Rhagidia Thorell, the gigas speciesgroup. Canadian Journal of Zoology 73, 1247–1258.

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ACAROLOGY

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

MYRIAD MESOSTIGMATA ASSOCIATED WITH LOG-INHABITING ARTHROPODS

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Owen Seeman Department of Entomology, The University of Queensland, St Lucia, Qld 4072, Australia.

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Abstract To test the hypothesis that passalid beetles (Coleoptera: Passalidae) have an exceptionally high diversity of symbiotic mites, I analysed species assemblages of Mesostigmata on large (> 1 cm) arthropods living within and beneath rotting logs at four sites in sub-tropical rainforests and three sites in tropical rainforests in Queensland, Australia. In total, I collected 740 log-inhabitants, representing about 42 species from 17 families. Passalid beetles were the most commonly collected log-inhabitant (426 individuals; 9 species); cockroaches, scarabaeid larvae and millipedes were also common. Of the 42 species of log-inhabitant, 29 carried at least one species of Mesostigmata, and I collected a total of 9374 mites, representing 71 species from 14 families. After removing the effects of the abundance of passalid beetles, they still had more species of mites associated with them than all of the other log-inhabitants combined. The diversity of mites on the Passalidae is at least double that of any other family of log-inhabitant. Indeed, if the number of associated mite families (24) is considered, Passalidae may have one of the most diverse assemblages of mites found on any family of animals.

INTRODUCTION Arthropods occupy a diversity of habitats, many of which require specialised techniques for sampling and, thus, are sometimes neglected. Examples are nests of vertebrates and arthropods, dung, leaf litter, soil, fungal sporocarps, epiphytes, tree-holes, mosses, flowers, rotting fruit, and bark (Hammond 1994; Walter et al. 1998). In association with the fauna occupying these habitats are an even more neglected, but important, component of biodiversity – the multitude of organisms living in various commensal, mutualistic, or parasitic relationships with their hosts. Indeed, May (1994) notes that if for every species of metazoan or vascular plant there is one species of nematode and protozoan specific to that host, estimates of biodiversity could be increased three-fold. Fallen, rotting wood is not an entirely neglected habitat (e.g. Fager 1968; Hamilton 1978), but it does not attract the attention given to, say, forest canopies (e.g. Stork et al. 1997). In compari-

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son with other habitats, the array of species in rotting wood is not diverse; however, the species that occur there are often unique to this habitat (Hamilton 1978; Walter et al. 1998). Additionally, rotting wood may be the primitive habitat for species basal in some orders of the Insecta (Hamilton 1978). One such group is the early derivative scarabeoid family Passalidae. Passalid beetles occur throughout the world’s wet forests, where they spend most of their lives tunnelling into and consuming rotting logs. Over 500 passalid species have been described (Reyes-Castillo 1970), but only a small portion of these have been sampled for mites. Nevertheless, over 200 species of mite from 21 families are recorded from passalids (Hunter 1993). Certainly, many more remain to be found, especially when one considers that 16 species, representing 11 families, are known from the well-studied passalid beetle Odontotaenius disjunctus (Illiger) (Delfinado and Baker 1975).

MYRIAD MESOSTIGMATA

Table 1

ASSOCIATED WITH LOG-INHABITING ARTHROPODS

Comparison of the diversity of Mesostigmata on five families of log-inhabitant versus the Passalidae. Numbers of families and species are based on equal numbers of log-inhabitants and passalids sub-sampled from a larger collection.

Host family Blaberidae

# collected

Species (Families) of Mesostigmata on family of log-inhabitant

Species (Families) of Mesostigmata on an equal number of Passalidae

50

5 (3)

10 (5)

Carabidae

41

2 (2)

11 (5)

Tenebrionidae

26

2 (2)

11 (6)

Julidae

80

4 (2)

13 (6)

Scolopendridae

25

3 (2)

10 (5)

Pearse et al. (1936) speculated, amusingly, that the reason passalids are home to so many mites is that they are a ‘… large, slow, stupid, vegetarian, which can always be found in the same sort of place and continues there for long periods of time.’ Other reasons for their myriad mite species may be the hydric stability of rotting logs (Pearse et al. 1936), and the possibility of a long historical association between mites and passalids (Hunter 1993). However, exactly how much more diverse the array of mites on passalids is in comparison with other families of log-inhabitants is unknown. Estimates of mite diversity could be inflated by the large numbers of passalid individuals and species that have been sampled. In this study, I surveyed the diversity of mites found on log-inhabiting arthropods, and focussed my attention on the supposed high diversity of mites found on passalid beetles. The question posed was whether there are more species of Mesostigmata on the Passalidae than on any other family of log-inhabitant, taking into account the abundance and diversity of passalid beetles.

MATERIALS AND METHODS I collected arthropods (adults and immatures > 1 cm in length) from rotting logs at seven sites in Queensland’s rainforests and subtropical rainforests. All large log-inhabitants were collected except for pill millipedes (Sphaerotheriinae) and tenebrionid larvae, because previous studies demonstrated that they are extremely abundant (thus using up limited collection resources) and only 5% of pill millipedes carried one species of mite (Cryptometasternum queenslandense Womersley). Sites and collection dates in Southeast Queensland were: Bunya Mountains (26°51’S, 151°03’E) on 12–14.ii.1996; Goomburra State Forest (28°02’S, 152°07’E) on 3.i.1997, 18.iii.1997; Jimna State Forest (26°39’S, 150°28’E) on 16–17.iii.1996, 24.x.1996, 21.xi.1996, 17–20.ii.1997, 16–18.ii.1998; and Lamington National Park (28°12’S, 153°10’E) on 25.v.1995, 25.ii.1996, 15.xi.1996, 2–3.xii.1996, 7.v.1997, 4.viii.1997. In Far North Queensland: Atherton Tablelands (17°15’S, 145°28’E) on 27–28.i.1996, 1.ii.1996; Cape Tribulation (16°08’S, 145°26’E) 29–30.i.1996; and Mossman-Mt Lewis Region (16°26’S, 145°16’E) on 31.i.1996. Log-inhabitants were collected by rolling logs over, breaking them apart, picking the loginhabitants up in forceps, and placing them into 80% ethanol-filled vials or empty plastic containers. Log-inhabitants placed into plastic containers were killed in 80% ethanol within one day. Mites collected this way were usually killed with the log-inhabitants, but sometimes mites were kept alive for rearing. All mites were removed from their host arthropod, counted, and representatives of species of Mesostigmata were slide-mounted in

Hoyer’s medium or Heinze polyvinyl alcohol medium. Identifications of life stage and, where possible, species, were made under a Leica microscope. Mites from the Uropodidae (Mesostigmata) and Acariformes were not identified past family-level because of lack of expertise, and because the Australian fauna of Uropodidae has hardly been studied (B¬oszyk and Halliday 1995). Some mites could be associated with a log-inhabitant by accident. Therefore, I considered a mite an associate of a particular host species if at least 10 mites of the same species were collected from two or more individuals of the same host species. Comparing the Passalidae with other log-inhabitants

To control for the effects of host abundance, I modified my collection data by randomly sampling equal numbers of passalids and other families of log-inhabitants from the same locations and times of collection. For example, if I collected five cockroaches from Jimna State Forest on 18th Feb, I randomly selected five passalids from my collections at the same site and time. When comparing passalid beetles with all other log-inhabitants, the modified data set had equal numbers of passalids and all other loginhabitants. When comparing passalid beetles to another target family of log-inhabitant, the modified data set had equal numbers of passalids and the target family of log-inhabitant. The first hypothesis tested was that the Passalidae have a higher diversity of Mesostigmata than other species of log-inhabitant. For each site, the number of associates on the Passalidae and ‘all other species of log-inhabitant’ was counted; these data were subjected to a paired t-test. The second hypothesis tested was that the Passalidae have a higher diversity of Mesostigmata than any other family of log-inhabiting arthropod. This was tested in the same way as the first hypothesis, except that a separate paired t-test was done for each passalid – family of log-inhabitant comparison.

RESULTS Altogether, I collected 740 large log-inhabiting arthropods, representing an estimated 42 species from 17 families. Passalid beetles made up the majority of collections (426), but numerous carabid beetles, blattid cockroaches and julid millipedes were also collected (Table 1). Species of Mesostigmata occurred on 29 species of loginhabitant, representing the families Anisolabidae, Blaberidae, Carabidae, Curculionidae, Julidae, Lucanidae, Passalidae, Scarabaeidae, Scolopendridae, Sphaerotheriidae, and Tenebrionidae.

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Owen Seeman

Figure 1

The diversity of Mesostigmata (Acari) on the Passalidae and all other log-inhabitants at five sites in Queensland. Numbers above columns = number of individuals from: (A) all collections and (B) equal numbers of log-inhabitant and passalids sampled from all the collections.

A total of 9374 individuals of Mesostigmata was collected, representing 71 species (22 previously described, 38 spp. undescribed or undetermined, 11 spp. Uropodidae) from 14 families (one undescribed). The Trigynaspida, a small supercohort of just over 225 described species, was represented by 37 species. Of the trigynaspid mites, seven were new species of Megisthanus, five were new species of Neofedrizzia, four were new species of Fedrizzia and Paradiplogynium (two each) and five were new species of Cryptometasternum, Diplogyniella, Micromegistus, Promegistus and a new family of Cercomegistina (D. E. Walter pers. comm.).

274

Only six of these species of Mesostigmata on log-inhabitants were not found on passalid beetles. Fifty-one species representing 10 families are, according to aforementioned criteria, valid associates of log-inhabitants. These mites are always associated with the adult life stage, and only eight species also occur on immature life stages of the log-inhabitants. Of these, only Coleolaelaps sp. occurs on a host that pupates (a scarab beetle). Furthermore, the other seven species are considerably more abundant on the adult stage of their arthropod hosts.

MYRIAD MESOSTIGMATA

The most diverse family of mites was the Fedrizziidae (Trigynaspida), which was represented by 16 species. Mite species displayed a high degree of host specificity: 33 species were found on one host species, 12 on two host species, one from three host species, three from four host species and two from five host species. The two species from five host species were one species of Uropodidae and a Hypoaspis sp. (Laelapidae). Families of log-inhabiting arthropods have distinct assemblages of mites associated with them: 48 species of mite are specific to one host family, two occur on two families and one on three families. Comparing the Passalidae with other log-inhabitants

In total, I collected 51 species of Mesostigmata, representing 10 families, from nine species of passalid beetle. I considered 37 species in seven families valid associates of passalid beetles. About half of the diversity comes from the Trigynaspida (24 species, three families). The families Fedrizziidae, Megisthanidae and Diarthrophallidae were found only on passalids. Another three families (Triplogyniidae, Pachylaelapidae, undescribed family) were also exclusive to passalid beetles, but each from only a single collection. More species of Mesostigmata are associated with passalid beetles than all other species of log-inhabitants combined at all sites (paired t-test, P = 0.01; Fig. 1a). This pattern remains even when the effect of abundance is removed (paired t-test, P = 0.006; Fig. 1b). At least twice the number of species of Mesostigmata are associated with the Passalidae than with any other family of log-inhabitant (Table 1), a pattern consistent for all families at all sites (all P < 0.05). After excluding the Passalidae, Blaberidae have the highest diversity of Mesostigmata, with five species (Table 1). The host species with the largest array of mites was the passalid Mastochilus quaestionis (Kuwert), with 15 species. Of similar diversity was Pharochilus dilatatus (Dalman) with 13 species, and the widespread species Aulacocyclus edentulus MacLeay with 11 species. Excluding the Passalidae, Panesthia tryoni Shaw (Blaberidae) had the highest number of associated mite species (five).

DISCUSSION The diversity of arthropods that live in rotting wood is not especially high, but the animals that live there are often restricted to their habitat (Hamilton 1978). Similarly, the mites associated with large log-inhabitants are found only in rotting logs (Walter et al. 1998). Further, many associates of log-inhabitants are specific to just one or two host species, and most species of Mesostigmata are restricted to just one host family. The same level of specificity to the log habitat is not expected for mites not associated with log-inhabitants. Many of these mites may live in the surrounding soil and litter habitats, and their presence in logs is probably transitory. Rotting logs are a patchily distributed, long-lasting habitat. Therefore, animals that live in rotting logs will eventually have to find another resource patch. For large log-inhabitants, this means a short flight or quick run over the forest floor, but for a mite, completing this same journey is improbable. Little wonder that most of the mites associated with log-inhabitants are phoretic, i.e.

ASSOCIATED WITH LOG-INHABITING ARTHROPODS

they use their host to carry them to another habitat. However, if the mites use the log-inhabitant for transport only, one would expect that most species of log-inhabitant would be a suitable phoretic host, especially within families that have a uniform morphology like the Passalidae. Apparently many mites are using their hosts for more than just transport, but for what other reason is not yet clear. The possibilities are numerous, although some species may be using their hosts as places to find a mate, similar to the harlequin beetle-riding pseudoscorpion Cordylochernes scorpioides (Zeh and Zeh 1994). More species and families of Mesostigmata occur on passalids than on any other family of log-inhabitant (Fig. 1; Table 1). Possibly, more species and families of mites are associated with passalids than with most other families in the animal kingdom. Hunter (1993) listed 21 families of mite associated with the Passalidae. Adding to his list, 21 becomes 24 families with the addition of Tarsocheylidae, Glycyphagidae and Promegistidae (Krantz 1978). From this survey, no new family-level associations are certain enough to be recorded, but Triplogyniidae (Funkotriplogynium iagobadius Seeman and Walter) and an undescribed family (undescribed species) were recorded from single collections of passalids. A passalid-triplogyniid association is doubtful (Seeman and Walter 1997), but seems more likely for the undescribed family because it is abundant in logs inhabited by passalids, and nine specimens were found on a dispersing passalid. The number of species of Mesostigmata associated with the Passalidae exceeds that of all mites known from the Lepidoptera (Treat 1975), and the number of mite species on passalid beetles probably rivals the number found on the largest families of Arthropoda (e.g. Curculionidae, Scarabaeidae and Formicidae). The high number of their mite families suggests that passalids have been colonised independently on many occasions. Within the Trigynaspida, assuming Kethley’s (1977) phylogeny is correct, passalids have been colonised on at least four separate occasions: Fedrizziidae + Klinckowstroemiidae; Megisthanidae + Hoplomegistidae; Schizogyniidae; and Diplogyniidae + Euzerconidae. Why have the Passalidae acquired such a diversity of mites when other groups of log-inhabitant have not? Pearse et al.’s (1936) first musings on the topic suggested the size and persistence of passalids in rotting logs (not to mention their vegetarianism and lack of intelligence) lent them to colonisation by mites. My study suggests that neither explanation, on its own, satisfactorily accounts for the diversity of mites on passalids. Some species of passalid are large (assuming a rectangular shape, M. quaestionis attains a surface area of 2940 mm2), but other log-inhabitants are of similar size. The largest of all common log-inhabitants collected was the cockroach P. tryoni at a surface area of 3830 mm2, yet it had only a few more species of mite compared with other species of loginhabitant, and half the number of species found on passalid beetles (Table 1). Passalid beetles occupy logs for long periods of time, often for multiple generations, but so do cockroaches and millipedes, yet neither group approaches the diversity of mites on the Passalidae (Table 1). Another possibility is that passalid beetles are the most reliable and safe carriers, i.e. passalids colonise logs more suitable for mites

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Owen Seeman

than logs colonised by other types of log-inhabitant (Pearse et al. 1936). This idea remains to be tested, but seems unlikely because most of the arthropods collected appeared to be restricted to wet, rotting logs. Finally, passalids may have many families of mites because of their historical association with rotting wood. Passalid beetles are not accomplished fliers, and the world-wide distribution of passalids and the many families of mites associated with them suggests the association of mites and passalids is ancient (Hunter 1993). Perhaps passalids have been accumulating families of associates since before the break up of Pangaea 250 mya. This may be true, but depends upon the length of the association of cockroaches and millipedes with rotting wood. If length of historical association alone was the vital factor, then the lower diversity on cockroaches and millipedes suggests that these ancient groups have recently colonised the rotting log habitat. One can conjure so many ideas about the reason a multitude of mites live with passalid beetles that disentangling the effect of each is difficult. Nevertheless, by comparison with other groups of log-inhabitants, some ideas can be discarded as explanations on their own – in this case, the size and persistence of passalid beetles in logs.

ACKNOWLEDGEMENTS I thank Dave Walter and Helen Nahrung for comments on various drafts of the manuscript, everybody who went on collecting trips with me, and the ARC Department of PGRS for funding towards field work.

REFERENCES B¬oszyk, J., and Halliday, R. B. (1995). A new species of Dinychus Kramer from Tasmania (Acarina: Dinychidae). Journal of the Australian Entomological Society 34, 187–91. Delfinado, M. D., and Baker, E. W. (1975). Mites (Acarina) associated with Popilius disjunctus (Illiger) (Coleoptera: Passalidae) in Eastern

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United States. Journal of the New York Entomological Society 33, 49–59. Fager, E. W. (1968). The community of invertebrates in decaying oak wood. Journal of Animal Ecology 37, 121–42. Hamilton, W. D. (1978). Evolution and diversity under bark. In ‘R.E.S. Symposium 9. Diversity of Insect Faunas’. (Eds L. A. Mound and N. Waloff). pp. 154–75. (Blackwell: London.) Hammond, P. M. (1994). Practical approaches to the estimation of the extent of biodiversity in speciose groups. Philosophical Transactions of the Royal Society of London B Biological Sciences 345, 119–136. Hunter, P. E. (1993). Mites associated with New World passalid beetles (Coleoptera: Passalidae). Acta Zoologica Mexicana Nueva Serie 58, 1–37. Kethley, J. B. (1977). A review of the higher categories of Trigynaspida (Acari: Parasitiformes). International Journal of Acarology 3, 129–49. Krantz, G. W. (1978). ‘A Manual of Acarology.’ (Oregon State University Bookstores: Corvallis.) May, R. M. (1994). Conceptual aspects of the quantification of the extent of biological diversity. Philosophical Transactions of the Royal Society of London B Biological Sciences 345, 13–20. Pearse, A. S., Patterson, M. T., Rankin, J. S., and Wharton, G. W. (1936). The ecology of Passalus cornutus Fabricius, a beetle which lives in rotting logs. Ecological Monographs 6, 455–90. Reyes-Castillo, P. (1970). Coleoptera, Passalidae: morfología y división en grandes grupos; géneros americanos. Folia Entomológica Mexicana 20–22, 1–240. Seeman, O. D., and Walter, D. E. (1997). A new species of Triplogyniidae (Mesostigmata: Celaenopsoidea) from Australian Rainforests. International Journal of Acarology 23, 49–59. Stork, N. E., Adis, J., and Didham, R. K. (1997). ‘Canopy Arthropods.’ (Chapman and Hall: London.) Treat, A. E. (1975). ‘Mites of Moths and Butterflies.’ (Comstock: New York.) Walter, D. E., Seeman, O., Rodgers, D., and Kitching, R. L. (1998). Mites in the mist: How unique is a rainforest canopy-knockdown fauna? Australian Journal of Ecology 23, 501–08. Zeh, D. W., and Zeh, J. A. (1994). When morphology misleads: interpopulation uniformity in sexual selection masks genetic divergence in harlequin beetle-riding pseudoscorpion populations. Evolution 48, 1168–82.

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

SOIL ACARI RESPONSE TO DEFORESTATION AND FIRE IN A CENTRAL AMAZON FOREST

Departamento de Ecologia, Instituto Nacional de Pesquisas da Amazônia (INPA), Av. Efigênio Sales 2239, 69.060–020, Manaus, Amazonas, Brasil. E-mail: [email protected]

....................................................................................................

Lucille M. K. Antony

.................................................................................................................................................................................................................................................................

Abstract This work examined the reaction of soil mites to deforestation and fire down to 15 cm depth, in a yellow latosol one-hectare primary forest plot prepared for a biomass burning experiment. It had been totally cut and its plant biomass left on site, drying for three months. Soil cores were collected from a non-disturbed neighbouring forest and, from the site before and after the fire, at weekly and monthly intervals during the first year and once during the fifth year after burning. Results are reported for the general soil fauna during the entire period and data on identification of mites include the following collections: logged forest, one day, two weeks and one year after burning. Acari made up 79% of the total fauna in the control forest, 90% in the logged plot, 35% one day after burning, 77% two weeks after burning, 95% one year after burning and 68% five years after burning. One-year after burning population densities increased at all three depths. Only five years after burning did group diversity reach numbers similar to those of non-disturbed forest, but instability of the system persisted. Long-term site monitoring is being conducted.

INTRODUCTION In the Amazon, the use of fire to clear forest and prepare the land for cultivation is a common practice among low-income rural people. The process is initiated at the beginning of the dry season (around July) and consists of cutting the forest totally, leaving its phytomass drying on site for approximately three months, and at the peak of the season (around October) the area is intensively burnt. When the rainy season starts (between the end of November and early December), the area is ready for planting, taking full advantage of rains (from January until end of May). The size of the area burnt (usually primary forest) varies from 1 to 4 hectares. The consequences of this type of practice to the Amazonian environment had not been determined until recently (Carvalho et al. 1995), when a biomass burning experiment was carried out in the dry season of 1991, as part of a major effort to quantify the amounts of carbon generated by this practice.

Several studies on the effect of fire on soil organisms have indicated that its impact is felt by the communities of the superficial soil (Rice 1932; Buffington 1967; Metz and Farrier 1973; Lussenhop 1976; Critchley et al. 1979; Moulton 1982; Majer 1984; Sgardelis and Margaris 1993; Oliveira and Franklin 1993; Webb 1994). Fire has three main effects on the soil environment: (1) it consumes the dead organic matter which represents the main food source for organisms; (2) it mineralises nutrients bound to the organic matter and (3) it produces high temperatures during the burning process (Moulton 1982). With few exceptions (Critchley et al. 1979; Oliveira and Franklin 1993), the majority of previous studies were undertaken in temperate regions, and in soils which are richer in nutrients than Amazonian soils. Except for Majer’s work in Western Australia (1984), none of these studies examined the soil fauna beyond the superficial layer (reaching a maximum of 5 cm depth including the litter layer). This work examines the reaction of soil fauna (including mites) to

277

Lucille M. K. Antony Table 1

Mean densities (individuals m–2) and maximum group diversity (parentheses) of soil arthropods from a non-disturbed forest and a forest plot (‘S8’) submitted to logging and burning. 0–5 cm

5–10 cm

10–15 cm

Control Forest (neighbouring Plot S8)

System

59704 (25)

16709 (17)

3056 (11)

Plot S8 (logged forest)

46493 (16)

2921 (10)

1290 (05)

Plot S8 – 1 day after burning

3770 (13)

2581 (12)

1087 (09)

Plot S8 – 1 week after burning

5909 (07)

883 (06)

679 (07)

Plot S8 – 2 weeks after burning

14569 (07)

3736 (12)

883 (09)

Plot S8 – 3 weeks after burning

6045 (08)

374 (05)

272 (05)

Plot S8 – 1 month after burning

6792 (13)

2513 (08)

917 (07)

Plot S8 – 3 months after burning

1494 (07)

679 (11)

475 (07)

Plot S8 – 4 months after burning

6588 (08)

3702 (10)

1053 (10)

Plot S8 – 6 months after burning

2989 (07)

1155 (09)

441 (04)

Plot S8 – 7 months after burning

7030 (08)

2377 (09)

894 (08)

Plot S8 – 1 year after burning

56206 (09)

6690 (06)

2038 (08)

Plot S8 – 5 years after burning

35045 (25)

9468 (19)

5582 (15)

deforestation and fire, considering their vertical distribution, density and dynamics before and after the burning process. This is the first time this type of work has been done in the Amazon region.

MATERIALS AND METHODS Study area

The study area is located at INPA’s Tropical Silviculture Experimental Station at BR-174 (Manaus-Caracaraí Road), Km 47, 2° 34' S, 60° 03' W, at an altitude of 44 metres. It consists of a dense upland forest standing on yellow latosol, with a vegetation biomass of 648 t/ha and a basal area of 22.74 m2/ /ha for individuals with diameter at breast height (DBH) above 20 cm (N=254). These values are amongst the highest found in other dense forests of Amazônia (INPA/INPE, unpublished), lower only than the values estimated for the Trombetas region (State of Pará, Brasil) with a basal area of 23.09 m2/ha (INPA/CPST, 1982, unpublished) and the Balbina region (State of Amazonas, Brasil), with a basal area of 29.38 m2/ha (INPA/CPST, 1983, unpublished). The climate type is ‘Am W’ in Koppen’s classification. The mean annual temperature is 26.7ºC, with mean maxima and minima of 31.2ºC and 23.7ºC. Precipitation ranges from 1705.4 mm/year to 2088.9 mm/year (Leopoldo et al. 1982) with a mean precipitation value of 2000 mm/year commonly used by researchers. A relatively dry period (June–October) alternates with a rainy season. The study was conducted in the one-hectare area prepared for a forest clearing combustion experiment described by Carvalho et al. (1995). The forest area was cut in July 1991, its phytomass estimated and left drying on site for three months. On November 3rd the area was burned, taking advantage of the lower precipitation characteristic of the dry season. The burning of areas for agricultural purposes is a common practice at this time of year. The total precipitation values for October, November and December of 1991 were 88.6 mm, 66.6 mm and 52.8 mm. The work on the soil fauna was initiated in the same year, just prior to burning, and continued for several months during 1992 up to the first year after

278

burning. The area continues to be monitored through collections of soil fauna made once a year. Soil samples were collected (at regular 15-metre intervals) from three 80 metre parallel transects at three depths (0–5 cm; 5–10 cm; 10–15 cm), using a 5 cm diameter soil core (v = 98.17 cm3 ). Fifteen sample units were taken from each of the depths, totaling 45 samples/collecting date. Concurrently, soil cores were taken for the determination of soil moisture. Samples were collected prior to burning when the area had been logged and the biomass left drying on site for three months (21/X/91); one-day after burning (04/XI/91); one, two and three weeks after burning; one, three, four, six and seven months after burning and one and five years after burning. The same sampling design was used for the control forest which was sampled only once – on the same day of the ‘7-month after burning’ collection (04/VI/92). The ‘5-year after burning’ collection was also done in June (18/VI/96). All samples were processed on the day they were collected. The fauna was extracted by conventional Berlese-Tullgren funnels over 8 days, using a temperature range of 25ºC on the first day, to 53ºC on the eighth day of extraction. Samples were collected into 1% formalin, then fixed in 75% alcohol +5% glycerine for identification and storage. Specimens other than mites were only identified to higher level (order or family). Permanent and temporary mounts of mites were prepared at the Acarology Lab of the Museum of Biological Diversity at The Ohio State University, Columbus, Ohio, U.S.A.

RESULTS On the first collecting occasion (October 21st), an average population density of 50,704 individuals m–2 was observed. In spite of having its phytomass cut and left drying on site for three months, the area was supporting an overall population density similar to that found by Adis et al. (1987) during the dry season in a secondary forest in Central Amazon (approximately 50,000 individuals m–2). The undisturbed forest (Control Forest) neighbouring the study area supported an average density of 79,469 individu-

Mean densities (Ind./m2)

SOIL ACARI RESPONSE TO DEFORESTATION

AND FIRE

60000 50000 40000 30000 20000 10000 0 0-5 cm 5-10 cm 10-15 cm

Figure 1

Forest Felling Day after 1 week 2 wks. 3 wks. 1 month 3 mos. 4 mos. 6 mos. 7 mos. 1 year 5 yrs.

Forest plot ‘S8’ : Abundance and vertical distribution of soil invertebrates in the non-disturbed forest; after logging, before burning (‘Felling’); 1 day after burning and up to 5 years after burning.

als.m–2 (Antony 1997), with about 75% at 0–5 cm, 21% at 5–10 cm and 4% at 10–15 cm depths. Compared to the control forest, deforestation (logged plot with biomass left drying) caused a reduction in mean population density and group abundance (the total number of higher-category faunal groups) respectively, of 22% and 36% (in the 0–5 cm depth), 82% and 41% (5–10 cm), 58% and 54% (10–15 cm). The immediate impact of fire (1 day after) was a further 92% reduction in microarthropod density and a 19% reduction in group abundance at the 0–5 cm depth. In the 5–10 cm and 10–15 cm horizons respectively, densities decreased by 12% and 16%, while group abundance increased by 20% and 80%. An apparent recovery by the superficial fauna (0–5 cm) was observed one and two weeks after the fire, with densities increasing by 56% and 146% respectively, while at lower depths densities remained reduced (Table 1 and Fig. 1). Among the abundant groups prior to burning (Acari, Collembola, Formicidae, Diptera, Coleoptera, Psocoptera, Pseudoscorpionida), Acari maintained high densities during almost the entire period of study. It comprised 79% of the total fauna in the control forest, 90% in the logged plot, 35% one-day after burning, 77% two weeks after burning, 95% one-year after burning and 68% five years after burning (Fig. 2). Tables 2–5 list the families of Acari collected in the logged plot ‘S8’ prior to burning, one-day after burning, two weeks after burning and one-year after burning. Among the Acari, the logged plot had Oribatida as the dominant group in terms of number of families and species, followed by Prostigmata, Mesostigmata and Astigmata (with second highest abundance, predominantly of

hypopodes). One day after burning, the number of families in all four suborders dropped sharply, and continued doing so for up to two weeks. One year after burning, Prostigmata took over with densities and diversity higher than Oribatida, showing their role as bioindicators of disturbance.

DISCUSSION Comparing the maximum number of groups encountered at each depth in the non-disturbed forest with those of the logged plot prior to and immediately after burning, Table 1 shows that logging had a greater impact upon the diversity of faunal groups than did burning. Antony (1996, 1997) found that selective logging can cause a strong impact upon the soil fauna, but its effects are more short-lived than those of burning. In this study, the mean number of groups captured one-day after burning was lower than that of the logged plot by 50%, 20% and 33% at the 0–5 cm, 5–10 cm and 10–15 cm depths respectively. This reduction in diversity remained throughout the study for at least one year. While population densities reached the same levels of the non-disturbed forest after 1 year, faunal diversity did not recover until 5 years after burning (Table 1). During the forest clearing by biomass burning experiment, Carvalho et al. (1995) measured soil temperatures below ground (at 3, 6, 12 and 24 cm), soil heatflux at 5 cm below ground, and air temperatures (at 8, 12, and 20 m above ground). Measurements were taken before (02/XI/91), during (03/XI/91) and after (04/XI/91) burning. They observed a maximum rise of about 3°C at 3 cm below ground during combustion (from 27.8°C to 31°C).

279

Abundance of groups (% of total catch)

Lucille M. K. Antony

Figure 2

5

100 80 60 40 20 0 For Fel

Day 1 w

2w 3w 1m

3m 4m 6m 7m

5y

Plot ‘S8’: Dynamics of major soil groups in the non-disturbed forest; after logging, before burning (‘Felling’); 1 day after burning, and up to 5 years after burning.

The temperatures at 6 cm, 12 cm and 24 cm increased by 2°C, 1°C and 0.5°C respectively during combustion, confirming the strong insulating capacity of soil, as has been shown in other studies (Whittaker 1961; Whittaker and Gimingham 1962; Webb 1994). The heat fluxes to the ground were altered during combustion (from approximately –70 W/m2 to 60 W/m2), and remained high for the following day. The air temperatures increased to about 60°C at 8m above ground during combustion but rapidly dropped back to normal temperatures (around 40°C at 8 m). Webb (1994) considers it unlikely that fire kills many animals and that the faunal decline occurs because of the drastic changes in microclimate which accompany the loss of the above-ground vegetation. He found that the number of species of Oribatida increased from 7 to 16 during a post-fire succession study, and the densities of these species increased from 4,319 individuals.cm-2 to Table 2

1y

ACARI DIPTERA COLLEMBOLA COLEOPTERA FORMICIDAE HOMOPTERA ISOPTERA PSEUDOSCORPIONIDA PSOCOPTERA

22,581 individuals.cm-2 over a 27-year period. However, the development of fauna (Oribatida) was slow, taking about 15 years to completely recover, and closely followed the growth cycle of the studied site (a heathland). Moulton (1982) observed that soil and litter arthropods were much less abundant immediately after the scorch treatment compared to the no-scorch treatment, but around 19 days after, they were not as different. He suggests that there is likely to be no effect of fire on soil arthropods that would disrupt ecosystem function and that they will re-establish in litter and carry out their functions as litter returns. Sgardelis and Margaris (1993) studied the effects of a wild fire on a coastal sage in Greece and observed that the abundance of most taxa exhibited more spatial variation between sites (control and fire treatments) and microsites (around bushes and under stones) than between sampling years. Among the Acari, they found that Mesostigmata (except for Rhodacaridae) and Oribatida were more affected than

Families of Acari captured in the superficial soil of a logged forest plot ‘S8’.

Depth

Oribatida

Prostigmata

Mesostigmata

Astigmata

0–5 cm

Galumnidae Haplozetidae Hypochthoniidae Lohmaniidae Malaconothridae Nanhermanniidae Oribatulidae Oppiidae Parakalummidae Plasmobatidae Rhynchoribatidae

Alicorhagiidae Bdellidae Cheyletidae Eupodidae Lordalychidae Oehserchestidae Rhagidiidae Tarsonemidae Tydeidae

Rhodacaridae Uropodidae (+1 Non determined Uropodina family)

Histiostomatidae Winterschmidtiidae

5–10 cm

Damaeolidae Epilohmanniidae Gehypochthoniidae

10–15 cm

280

Uropodidae

Alicorhagiidae Tarsonemidae

Rhodacaridae

Winterschmidtiidae

SOIL ACARI RESPONSE TO DEFORESTATION

Table 3

Families of Acari captured from forest plot ‘S8’: One-day post fire.

Depth

Oribatida

Prostigmata

Mesostigmata

Astigmata

0–5 cm

Epilohmanniidae Galumnidae Gehypochthoniidae Haplozetidae Nanhermanniidae Nothridae (+ 1 Non det. family)

Alicorhagiidae Eupodidae

Rhodacaridae Uropodidae

Histiostomatidae

5–10 cm

Epilohmanniidae Galumnidae Haplozetidae (+ 2 Non det. families)

Alicorhagiidae

Rhodacaridae

10–15 cm

Epilohmanniidae, (+ 2 Non det. families)

Rhodacaridae

Prostigmata. Also, Oribatida immatures seemed more tolerant of fire than adults. Rhodacaridae was not affected by fire. Most taxa exhibited a tendency to recover in the second year post-fire. The authors estimated that in less than 3–4 years soil animal populations would recover, following the quick process of vegetation recovery observed in that type of system. Lussenhop (1976) observed distinct soil arthropod responses to burning, raking and no disturbance in a pairie system submitted to biennial spring burnings. Among Acari, some species of Prostigmata (adults of Eupodes sp. and Microtydeus sp.) and Oribatida (immatures of Oripoda sp.) increased in density in burned-and-raked blocks, as well as in burned blocks (Nanorchestes sp2. adults and imatures; Epilohmannia sp. immatures), in contrast to unburned blocks. Some of these responses were attributed to a probable increase in root detritus (Eupodes sp) or to an increased prey density (Microtydeus sp.). Oliveira and Franklin (1993) studied a central Amazon 4-hectare forest plot which was felled and burned for pasture establishment. Burning was not homogeneous and formed a patchwork of well-burnt and unburnt areas, from which the soil fauna was compared. Sampling was carried out 1-day after fire and proceeded to 15, 30, 40, 60, 125, 145, 200, 270, 320 and 370 days after fire. They concluded that the soil fauna population densities were drastically affected by fire. In the well-burnt patches the total density of Oribatida was lower than those of the other Acari and the total density of Collembola was inferior to the total density of the other insect orders combined. A reverse situation was observed in the unburnt patches, where both Oribatida and Collembola had higher densities than the other orders. No indications were given in relation to the necessary time for total recovery of the system. Table 4

In this study, the high number of mite families (Oribatida 14, Prostigmata 9, Mesostigmata 3, Astigmata 2) found in the logged plot prior to burning was unexpected and impressive (Table 2). The entire area was covered by dead tree trunks and dry leaves and twigs, and was being exposed to bright sunlight and high temperatures for about three months when sampling was carried out. Acari populations accounted for 90% of the total fauna captured at 15 cm. One day post fire (Table 3), the Epilohmanniidae, Galumnidae and Haplozetidae (all well-sclerotised groups) contrasted with the Alicorhagiidae and Eupodidae. Lussenhop (1976) also found that members of the Epilohmanniidae, Eupodidae, Nanorchestidae and Tydeidae increased in burned sites. Two weeks post fire (Table 3) the less sclerotised mite families prevailed, but overall Acari populations decreased while Diptera populations increased. The demographic development of Diptera was noteworthy. One day after burning, the group already represented the second highest in abundance. One week after burning they supplanted the Acari at the 0–5 cm and 10–15 cm depths and during the following weeks remained as the second most abundant group. The main stimulus for such a population growth may have been the immediate availability of food – organic matter released during burning – made into a rich soil solution by the rain that started to fall on November 4th. The accumulated precipitation from November 4th (1 day after burning) through December 2nd (1 month after burning) was 128.4 mm, which accounted for 62% of the total precipitation registered in October, November and December of 1991. Soil moisture and soil temperature were not correlated with density or diversity.

Families of Acari captured from forest plot ‘S8’: 14 days post fire.

Depth

Oribatida

Prostigmata

Mesostigmata

0–5 cm

Gehypochthoniidae Nothridae (+ 2 Non det. families)

Pyemotidae

Uropodidae

Pygmephoridae

1 Non det. family. (immatures, only)

5–10 cm 10–15 cm

AND FIRE

Astigmata

Nothridae Oppiidae (+ 1 Non det. family)

281

Lucille M. K. Antony Table 5

Families of Acari captured from forest plot ‘S8’: One-year post fire.

Depth

Oribatida

Prostigmata

Mesostigmata

0–5 cm

1 Non det. family

Eupodidae Nanorchestidae Tydeidae (+ 2 Non det. families)

2 Non det. family

5–10 cm

Gehypochthoniidae Haplozetidae

Eupodidae Oehserchestidae Tydeidae

Rhodacaridae (+1 Non det. family)

10–15 cm

Mesoplophoridae Oribatulidae

Eupodidae Rhagidiidae Tydeidae

As for Collembola, which, under natural conditions, is the second most abundant soil arthropod group, burning seemed to trigger a hemi- and euedaphic response, with its populations inhabiting the lower depths, especially the 10–15 cm depth. Total numbers of Coleoptera were not affected by burning, maintaining stable populations distributed throughout the three depths, although with higher densities at the 5–10 cm depth. The response of Formicidae – the other abundant group in the superficial soil – was similar to that of Collembola. Their populations became more numerous at lower depths, especially at 5–10 cm. In general terms, the immediate impact of fire upon the soil arthropod communities was drastic, but not terminal. Some groups were actually stimulated to increase in numbers – perhaps due to the prompt release of organic matter to the system, made digestible by the growing microflora. This may also account for the increased number of immatures observed in various taxa. As for the total recovery of the soil communities of the studied site, it took at least one year before population numbers similar to those of non-disturbed forest were reached, and at least five years to reach the original level of diversity. However, because instability of the system persists with accentuated fluctuations in population densities, long term site monitoring is being conducted.

ACKNOWLEDGEMENTS This study was supported by Research Grant no 460022-93.8 from CNPq (National Research Council) and INPA. I am grateful to EMBRAPA Station personnel in Manaus, who kindly provided the climatic data for the year of 1991. Many thanks to Cláudio Sena and Eudes Ramos for help in the field and for sorting of the soil fauna.

REFERENCES Adis, J., Morais, J. W., and Ribeiro, E. F. (1987). Vertical distribution and abundance of arthropods in the soil of a neotropical secondary forest during the dry season. Journal of Tropical Ecology 28, 174–181. Antony, L. M. K. (1996). Influência do corte seletivo sobre a biota do solo de uma floresta de ‘terra-firme’ na Amazônia Central. In CDROM Proceedings, Solo-Suelo 96, XIII Congresso Latino Americano de Ciência do Solo, Águas de Lindóia, SP, 1996.

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Astigmata

Acaridae

Acaridae

Antony, L. M. K. (1997). Abundância e distribuição vertical da fauna do solo de ecossistemas amazônicos naturais e modificados. In CDROM Proceedings, XXVI Congresso Brasileiro de Ciência do Solo, Rio de Janeiro, RJ, 1997. Buffington, J. D. (1967). Soil arthropod populations of the New Jersey Pine Barrens as affected by fire. Annals of the Entomological Society of America 60, 530–534. Carvalho, J. A., Santos, J. M., Santos, J. C., Leitão, M. M. and Higuchi, N. (1995). A tropical rainforest clearing experiment by biomass burning in the Manaus region. Atmospheric Environment 29, 2301–2309. Critchley, B. R., Cook, A. G., Critchley, U., Perfect, T. J., Russell-Smith, A., and Yeadon, R. (1979). Effects of bush clearing and soil cultivation on the invertebrate fauna of forest soil in the humid tropics. Pedobiologia 19, 425–438. Leopoldo, P. R., Franken, W., Matsui, E., and Salati, E. (1982). Estimativa da evapotranspiração da floresta amazônica de terra firme. Acta Amazonica 12, 23–28. Lussenhop, J. (1976). Soil arthropod response to prairie burning. Ecology 57, 88–98. Majer, J. D. (1984). Short-term responses of soil and litter invertebrates to a cool autumn burn in Jarrah (Eucalyptus marginata) forest in Western Australia. Pedobiologia 26, 229–247. Metz, L. J., and Farrier, M. H. (1973). Prescribed burning and population of soil mesofauna. Environmental Entomology 2, 433–440. Moulton, T. P. (1982). ‘The effect of prescribed burning and simulated burning on soil and litter arthropods in open forest at Cordeaux, N.S.W., Australia.’ PhD Thesis, Macquarie University, NSW Australia. Oliveira, E. P., and Franklin, E. (1993). Efeito do fogo sobre a mesofauna do solo: Recomendações em áreas queimadas. Pesquisa agropecuária brasileira 28, 357–369. Rice, L. A. (1932) . Effect of fire on the prairie animal communities. Ecology 13, 393–401. Sgardelis, S. P. and Margaris, N. S. (1993). Effects of fire on soil arthropods of a phryganic ecosystem. Pedobiologia 37, 83–94. Webb, N. R. (1994). Post-fire succession of cryptostigmatic mites (Acari, Cryptostigmata) in a Calluna-heathland soil. Pedobiologia 38, 138–145. Whittaker, E. (1961). Temperatures in heath fires. Journal of Ecology 49, 709–715. Whittaker, E., and Gimingham, C. H. (1962). The effects of fire on regeneration of Calluna vulgaris (L.) Hull from seed. Journal of Ecology 50, 815–822.

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

NICHE SEGREGATION AND CAN-OPENERS: SCYDMAENID BEETLES AS PREDATORS OF ARMOURED MITES IN AUSTRALIA

1

Department of Entomology, Wageningen Agricultural University, Binnenhaven 4, Wageningen, The Netherlands. Present address: EEW Evolutionary Biology, Leiden University, Kaiserstraat 63, 2300 RA Leiden, The Netherlands. 2 Department of Zoology and Entomology, The University of Queensland, St Lucia, Queensland 4072, Australia, [email protected]

....................................................................................................

Freerk Molleman1 and David Evans Walter2

.................................................................................................................................................................................................................................................................

Abstract As adult Oribatida and Uropodina are well sclerotised, it has been assumed that most predation is limited to the immature stages; however, some mites, ants and beetles have been observed feeding on armoured mites. We studied scydmaenid beetles (Coleoptera: Scydmaenidae) from rainforest in south east Queensland and tested the hypothesis proposed by Schmid (1988) that scydmaenids are restricted to armoured mite prey. Of the 43 scydmaenids that we observed in small arenas, 32 (74%) fed on armoured mites. These included representatives of at least five genera and 22 morphospecies; however, 15 individuals (representing three of the five genera) also scavenged on dead arthropods such as ants and springtails. Although some Australian species of Horaeomorphus and Stenichnus appeared to be specialised on Oppioidea (Oribatida), certain species of Euconnus were extreme generalists feeding on many types of armoured Oribatida and Uropodina. Additionally, we observed predation on armoured mites by Enicocephalidae (Hemiptera), but not by Pselaphidae (Coleoptera).

INTRODUCTION A well-armoured body is a common defence strategy against predation and is especially common in molluscs, turtles and arthropods, although many other animal taxa and even plants may be armoured. The effectiveness of armour has been studied in bivalves and gastropods in living populations as well as the fossil record. Vermeij (1987) attempted to correlate changes in shell shape and thickness in gastropods and bivalves through time with the adaptations developed by predators using the specific marks predation leaves on the shells. However, arthropod armour has never been studied systematically (Vermeij 1987). Among mites, armour has evolved convergently in a number of different groups, and two of these, the Oribatida and Uropodina, have radiated extensively. Armour morphology is highly variable both between and within the Uropodina and Oribatida (Schmid 1988; Norton and Behan-Pelletier 1991). In forest humus, armoured mite densities can be staggering, with hundreds of thousands per square metre commonly reported.

However, very little is known about the regulation of their populations. Considering their abundance, armoured mites should represent a major food source for any predators that can overcome their armour. For a long time it had been assumed that predation was mainly limited to the unarmoured immature stages; however, there now are several records of predation on armoured mites. Apart from amphibians who swallow the whole mite (Pengilley 1971; Maiorana 1978), a number of arthropods have been reported to penetrate the armour: Formicidae (Hymenoptera) (Masuko 1994), Pselaphidae (Coleoptera) (Park 1947), Ptiliidae (Coleoptera) (Riha 1951; Cancela da Fonseca 1975), and Scydmaenidae (Coleoptera) (Schuster 1966; Schmid 1988). Schmid (1988) demonstrated that scydmaenid beetles may be especially important predators of armoured mites. In his investigations on prey preference and prey handling, Schmid found that different beetle genera were adapted to different types of armoured prey. Morphological adaptations, involving mandible shape, labial suckers and hairs on the tarsi of the front legs were

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Figure 1

Armoured mite consumption of individual Scydmaenidae sorted by genus. The length of the mites is plotted on the y-axis and predators are on the x-axis. Oppioidea were the most frequently eaten mites.

associated with specialisation at the generic-level on different types of armoured prey. The first aim of the present study was to determine if the Scydmaenidae from the soil-litter system in subtropical rainforest of southern Queensland feed on armoured mites. Moreover, we tested two hypothesis presented by Schmid (1988): (1) that scydmaenid genera are specialised on different armoured prey types, and (2) that scydmaenids are restricted to armoured mite prey. Armoured mite predation in other soil dwelling insects was tested by offering armoured mites to various species of Pselaphidae (Coleoptera) and Enicocephalidae (Hemiptera).

MATERIALS AND METHODS Leaf litter was collected from subtropical rainforest in Queensland, Australia, using a sieve to exclude larger branches, leaves and rocks from the sample. The beetles and mites were than extracted using simple Berlese-funnels with 40 Watt light-bulbs. Extraction containers with hydrated powdered charcoal-plaster (1:7 by weight) floors were used to collect live arthropods, and individual Scydmaenidae, Pselaphidae and Enicocephalidae were kept in similar vials. All experiments were carried out in plastic culture wells consisting of 24 round arenas (1.7 cm) with hydrated charcoal-plaster floors and sealed at the top with glass coverslips. Arthropods were transferred using a fine, wetted brush. As keys to the Australian species of Scydmaenidae and Pselaphidae were not available, we identified genera using Matthews (1992), O’Keefe (unpublished), and reference material at the Queensland Museum and the University of Queensland Insect Collection. Within genera, specimens were sorted into morphospecies. Mites attacked by predators or found dead after overnight

284

trials were mounted in Hoyer’s medium on glass microscope slides, and numbered for identification and assessment of damage using a single-blind technique (i.e. the source of the damage was unknown to the assessor). Prey were identified to superfamily, measured along the midline of the body, and scored for damage to legs and body openings (gnathosoma, genital valves, anal valves). Specimens were prepared for the JEOL JSM 820 scanning microscope by dehydration through an ethanol series followed by twice soaking in a drop of hexamethyldisilazane until dry (ca. 60 min.) and subsequently coated with gold or platinum. Feeding experiments

Each predator was placed in an arena and provided with microarthropods extracted from various litter collections. Predators were observed at least once every 15 minutes and feeding behaviour was recorded, occasionally with a video set-up. When a prey item was abandoned the remains were stored in glass vials in 80% ethanol for later identification. At the end of an observational session, predators were left in arenas overnight and the next day any dead mites were collected for identification and analysis. Two unarmoured mites from laboratory cultures, a relatively large mesostigmatan (Epicroseius sp., 750 µm) and immatures of a Galumna species, were used as alternative prey in a second experiment. Each arena contained a single mite and a single scydmaenid beetle; the experiment continued for several days at room temperature (25°C).

RESULTS AND DISCUSSION In total, 43 individual Scydmaenidae where observed, of which 32 (74%) ate a total of 130 armoured mites (Fig. 1). We identified 31 of 43 individuals to genus (morphospecies): Horaeomor-

NICHE SEGREGATION

Figure 2

AND CAN-OPENERS: SCYDMAENID

BEETLES AS PREDATORS OF ARMOURED MITES

Length of prey in relation to the length of scydmaenid beetles.

phus (1 sp., 1 individual), Euconnus (8 spp., 12 individuals, including a cluster of at least five sibling species), Microscydmus (1 spp., 2 individuals), Scydmaenus (6 spp., 11 individuals), and Stenichnus (5 spp., 5 individuals). The remainder (12), all belonging to the tribe Cyrtoscydmini (Newton and Thayer 1992), escaped during trials and were not identified further. In all of the genera tested, most individuals fed on armoured mites: Horaeomorphus (100%), Euconnus (92%), Microscydmus (100%), Scydmaenus (55%), and Stenichnus (60%). The degree of specialisation on armoured prey varied among species. For example, Horaeomorphus sp. preyed exclusively upon Oppioidea, which have smooth cuticles and long legs. Other beetles also may prefer Oppioidea, including Euconnus sp. 35 and two of the Stenichnus species. Schmid (1988) found that only smooth-skinned mites were eaten by beetles with labial suckers, as found in the tribe Cephenniini and the genus Stenichnus (Cyrtoscydmini). However, many of our beetles (tribes Scydmaenini and Cyrtoscydmini) were not limited to smooth mite prey. For example, Euconnus sp. 11 preyed upon mites of 9 different superfamilies (Fig. 1) including mites with smooth (27 individuals) and rough (5 individuals) cuticles. Although the Australian Scydmaenidae attack prey over a broad range of lengths (230–1000µm), a maximum and minimum prey size may apply (Fig. 2). The smallest beetle, Microscydmus sp.

(630 µm in length), only attacked mites under 300 µm. Larger beetles tended to attack larger prey; however, the overlap in prey size choice was extensive. Overall, beetle length explained less than 10% of the variance in prey length (R2 = 0.0982; P = 0.00077). This may not reflect the predation pattern in the field as larger mites may be more likely to escape from a predator, but cannot escape from the small arena. All the Scydmaenidae that were observed feeding on armoured mites first lifted the prey from the ground using the first pair of legs, which have a dense brush of spatulate setae on the inner margins of each tibia. The mites were rotated while the mandibles were used to cut off each leg near its base (Fig. 3). In the typical sequence of behaviour, after the legs were partially or fully removed, the beetle started probing the surface of the mite with its mandibles while turning the mite with its front legs. When the gnathosomal opening or a valve was located it was penetrated with a mandible and cut out. Typically, the first area opened was the gnathosoma, then the beetles proceeded to one or another of the ventral openings. When feeding on Uropodina, the gnathosoma was penetrated, but the minute anal valves were never attacked. When feeding on oribatid mites, the genital valves were usually penetrated (35%), but occasionally only the anal valves (6%) or both anal and genital valves were removed (27%). In the genus Euconnus (sp. 35), an exceptional feeding behaviour was

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Freerk Molleman et al.

Figure 3

286

Armoured mites eaten by scydmaenid beetles: a) Uropodidae, b) Galumnoidea, c) Hermanniella sp., d) Oppioidea. All had their legs removed before penetration through the gnathosoma. Additionally, the oribatid mites had the genital valves removed (and the anal valves in the oppioid). Scale bars = 110µm.

NICHE SEGREGATION

AND CAN-OPENERS: SCYDMAENID

recorded. While most other Scydmaenidae apparently opened the gnathosoma first and then proceeded to open other valves, 5 of 7 individuals from this group attacked only the genital valves when feeding on Oppioidea. The feeding behaviour we observed is similar to Schmid’s (1988) ‘cutting technique’ (schneidetechnik), except that he makes no mention of the pruning off legs or leg segments, except by a species of Neuraphus (Cyrtoscydmini) that attack long-legged Belboidea (neither of which occurred in our samples). In Queensland, beetles cut off the legs of mites irrespective of the lengths of the legs. Many mites that had been unsuccessfully attacked (i.e. no valves were penetrated) were missing legs. Only a few bodies were found with all their legs intact and only the gnathosoma or valves penetrated. Leg-cutting may be initiated by the struggles of the mites, and those with the legs not removed may have been passive or dead when eaten. One beetle (Euconnus sp. 11) was videotaped feeding on a Scheloribatidae with a smooth cuticle. As with many of the beetles we observed, this individual was capable of lifting the mite with one leg using its tibial suckers. After a few minutes the effectiveness of the suckers decreased and the legs began slipping over the smooth cuticle of the mite. The legs were then groomed extensively with the mouthparts, after which the suckers regained their effectiveness. Tibial grooming is a common behaviour, especially during feeding, and undoubtedly serves to maintain the suckers. The same individual also consumed rough-skinned Oribatida, indicating that the tarsal suckers do not limit the beetles to mites with a smooth cuticle. Many mites attempted to escape when attacked by Scydmaenidae, and oppioid oribatid mites were especially successful in escaping. Although the experiment was not designed for detailed observation of attacks, 13 oribatids were recorded escaping from the predator by running, 7 of which were oppioids. When an oppioid was caught, it struggled to free itself, often pushing the beetle away with its legs. Once free, the mites ran rapidly away from the beetles. Oppioidea have relatively long legs that are exposed to predators; however, these long legs also help the mite to escape predation. In our arenas, no definitive escape was possible and the Scydmaenidae had ample opportunity to catch the mites. In contrast to Oppioidea, mites that exhibit conglobation (rolling into a ball) do not run, but their armour may be highly effective against scydmaenid predation (we observed few successful attacks). Mites with tecta to protect the legs are possibly intermediate in this respect. Vermeij (1987) described the reduction of locomotion as a result of armouring as a general pattern in armoured animals. This hypothesis could be tested by comparing the walking speed and the effectiveness of armour in mites. Scydmaenid beetles were only observed attacking live mites; however, many would also feed on dead ants, beetles and collembolans of the family Onychiuridae. Of the 15 beetles observed scavenging on dead arthropods, ten also fed on armoured mites. Even Onychiuridae (Collembola), well known for the repelling excretions they produce (Eisenbeis and Wichard 1987), were scavenged. Some species of Scydmaenidae may be associated with ants and exhibit scavenging in this context (S. O’Keefe pers. comm.).

BEETLES AS PREDATORS OF ARMOURED MITES

Scydmaenids would not attack the large (750 µm) mesostigmatan (Epicroseius sp.) they were offered (12 tests). However, immature, unarmoured nymphs of a species of Galumna (Oribatida) were fed on by two species of Euconnus. The scavenging on dead arthropods and predation on unarmoured nymphs suggests that Scydmaenidae could be more opportunistic than Schmid (1988) suggested. He hypothesised a possible ecological limitation to armoured prey resulting from the beetles use of extra-intestinal digestion. However, many arthropods have extra-intestinal digestion and still feed on unarmoured prey. Perhaps, specialisation on slow-moving armoured prey is more a result of an inability to overcome the defences of other soil microarthropods, such as toxic secretions or jumping. Thirty-one specimens of 8 genera of Pselaphidae (Eupines [2 sp., 4 individuals], Eupinoda [10 spp. , 19 individuals], Pselaphaulax [1 sp., 1 individual], Pselaphophus [1 sp., 1 individual], Schaufussia [1 sp., 1 individual], Palimbolus [2 spp. , 2 individuals], Mesoplatus [1 sp., 1 individual], Euplectops [2 spp. , 2 individuals]) were tested with armoured mites, however, none preyed on the mites offered. On one occasion an individual made an attempt, turning the prey with the first four legs while trying to get grip with the mandibles, but the beetle gave up within five minutes. Park (1947) mentioned both collembolans and oribatids as prey for pselaphids. Engelmann (1956), however, found that the three species of pselaphids he investigated were specialised predators of collembolans that capture prey using spines on the front legs. These spines can be seen in many of the Pselaphids we collected, but some also have bristles on the inner side of the tarsi comparable with those found in Scydmaenidae. Enicocephalidae are limited to humid microhabitats in the tropics and subtropics, where they feed on larval and adult insects, but have not been reported to feed on armoured mites (Carayon 1951). However, of the six individual Enicocephalidae (Sphigmocephalus – 2 adults, each of different species, and 4 nymphs) tested, five fed on armoured mites. One large adult specimen fed on even the largest mites offered (Euphthiracarioidea, > 1000µm). The bugs clasped prey with their front legs and searched for a place to penetrate with their rostrum. Usually, penetration occurred through the gnathosoma. The largest adult had hairs on its front leg that possibly play a role in prey handling. All six Sphigmocephalus also preyed upon the mesostigmatan Epicroseius sp. Other soil-dwelling heteropterans have the potential for predation on armoured mites and should be investigated.

CONCLUSIONS Many Australian Scydmaenidae are predators of armoured mites, although the degree of specialisation on armoured prey varies among species. For example, Euconnus sp. 11 preyed upon 32 individual mites of 9 different superfamilies (Fig. 1) including mites with smooth and rough cuticle texture whereas Horaeomorphus sp. consumed only Oppioidea. Overall, most of the mites eaten in these experiments were Oppioidea; however, no choice tests were performed to determine what factors influenced this apparent preference. There is a positive relationship between the size of the scydmaenids and the size of their prey, although the

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range of the prey size per beetle is very broad, and beetle length accounts for less than 10% of the variation in prey length (Fig. 2). As was pointed out by Schmid (1988), many Scydmaenidae bear spatula-shaped hairs on their tibiae and femora, and these can be seen as white shiny patches on the inside of the prothoracic legs and act as tibial suckers. In the prey handling sequence, cutting of the legs is the first action. Typically, the first area opened was the gnathosoma, then the beetles proceed to one or another of the ventral openings. One distinctive pattern in prey-handling was observed in the Euconnus sp. 35. Of 13 mites eaten, 10 were Oppioidea and 70% of these had only their genital valves opened. In summary, Australian Scydmaenidae do not feed exclusively on armoured mites, but also scavenge on insects, collembolans and unarmoured nymphs of a Galumna species (Oribatida); however, attacks on live animals other than mites were never observed. Predation on armoured mites is not common among Pselaphidae in rainforest litter in south-eastern Queensland as none of the 31 specimen (21 species, 8 genera) attacked mites. Adults and nymphs of at least one species of Enicocephalidae also prey on armoured mites.

ACKNOWLEDGEMENTS

Carayon, J. (1951). Ecologie et régime alimentaire d’Hémiptères Hénicocéphalides Africains. Bulletin de la Socièté Entomologique de France 1, 39–44. Eisenbeis, G. and Wichard, W. (1987). ‘Atlas on the Biology of Soil Arthropods.’ (Springer-Verlag: Berlin.) Engelmann, M. D. (1956). Observations on the feeding behavior of several pselaphid beetles. Entomological News. 67, 19–24. Masuko, K. (1994). Specialised predation on oribatid mites by two species of the ant genus Myrmecina (Hymenoptera: Formicidae). Psyche 101, 159–171. Matthew, E. G. (1992). ‘A Guide to the Genera of Beetles of South Australia.’ (South Australian Museum: Adelaide.) Maiorana, V. C. (1978). Behaviour of an unobservable species: Diet selection by a salamander. Copeia 4, 664–672. Newton, A. F., and Thayer, M. K. 1962. Current classification and familygroup names in Staphyliniformia (Coleptera). Fieldiana Zoology (New Series) 67, 1–92. Norton, R. A., and Behan-Pelletier, V. (1991). Calcium carbonate and calcium oxalate as cuticular hardening agents in oribatid mites (Acari: Oribatida). Canadian Journal of Zoology 69, 1504–1511. Park, O. (1947). Observations on Batrisodes (Coleoptera: Pselaphidae), with particular reference to the American species east of the Rocky Mountains. Bulletin of the Chicago Academy of Sciences 8, 45–132. Pengilley, R. K. (1971). The food of some Australian anurans (Amphibia). Journal of Zoology 163, 93–103.

We would like to thank S. O’Keefe (University of California, Berkeley) for his help with the identification of the Scydmaenidae as well as G. Monteith and the Queensland Museum for making their collections available for study. Special thanks also to A. O’Toole and C. Meacham for help with the scanning electron microscopy. For useful insights and criticisms which aided the development of this work we thank R. A. Norton, A. F. Newton, and all the mite people of Dave’s mob.

Schmid, R. (1988). Morphologische Anpassungen in einem RäuberBeute-System: Ameisenkäfer (Scydmaenidae, Staphylinoidea) und gepanzerte Milben (Acari). Zoologisher Jahresbericht Abteilung Systematik Oekologie Geografie Tiere 115, 207–228.

REFERENCES

Schuster, R. (1966). Uber den Beutefang des Ameisenkäfers Cephennium austriacum Reiter. Die Naturwissenschaften 4, 113.

Cancela da Fonseca, J. P. 1975. Notes Oribatologiques. Acarologia 17, 320–330.

Vermeij, G. J. (1987). ‘Evolution and Escalation.’ (Princeton University Press: Princeton.)

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Riha, G. (1951). Zur ökologie der Oribatiden in kalksteinböden. Zoologisher Jahresbericht Abteilung Systematik Oekologie Geografie Tiere 80, 407–450.

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ACAROLOGY: PROCEEDINGS OF THE 10TH INTERNATIONAL CONGRESS

INTERACTIONS BETWEEN MITES AND PLANTS

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Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

THE FALSE SPIDER MITE, BREVIPALPUS OBOVATUS DONNADIEU (ACARI: TENUIPALPIDAE): HOST-RELATED BIOLOGY, SEASONAL ABUNDANCE, AND CONTROL

Department of Economic Entomology, Faculty of Agriculture, Elshatby, University of Alexandria, Alexandria, Egypt ([email protected])

....................................................................................................

Hussien A. Rezk

.................................................................................................................................................................................................................................................................

Abstract The false spider mite, Brevipalpus obovatus Donnadieu, is a major pest of fruit trees and ornamental plants in Egypt. This work was directed at studying the seasonal abundance, host related biology and field control of B. obovatus. Populations of B. obovatus on citrus trees were monitored for 12 months. Populations peaked in early spring and fall at an average of 0.71±0.02 and between 0.52±0.04 and 0.61±0.02 mites/leaf, respectively. B. obovatus was reared on citrus and mint leaves in the laboratory conditions (25±2-C and 65±5% RH) and the duration of developmental stages was measured. The mean incubation period was 3.07 and 4.16 days on citrus and mint, respectively. Hatch rate was 87.49% and 72.9% for the two hosts. The active larval, protonymphal and deutonymphal stages lasted an average of 2.76, 2.63 and 3.21 days on citrus, and 3.13, 3.23 and 4.53 days on mint. Female longevity averaged 34.26 and 41.16 days on citrus and mint, respectively. Fecundity was also observed for five generations. The effect of two acaricides, Ortus (fenpyroximate) and Neoron (bromopropylate), on B. obovatus were evaluated in citrus orchards in the Tahrir area, Egypt. The results indicated that Ortus reduced the mite population faster than Neoron.

INTRODUCTION False spider mites (Tenuipalpidae) are plant feeders infesting horticultural crops, weeds and wild plants world wide. They may cause serious problems, particularly when populations are large (Attiah 1956; Baker and Tuttle 1964). The genera Brevipalpus, Cenopalpus and Tenuipalpus are the most important, containing major fruit tree pests (Zaher and EL-Badry 1964; Rasmy 1966; Yousef 1967; Wafa et al .1969; Denmark 1984). The genus Brevipalpus was first recorded in Egypt by Attiah (1956). It includes several species (e.g. B. obovatus, B. californicus, B. phoenicis) that are cosmopolitan. Brevipalpus obovatus is a major pest of fruit trees and ornamental plants. The host range of this species includes fruit trees, house plants, medicinal plants and shrubs (Pritchard and Baker 1958). B. obovatus is an important pest of citrus trees, feeding on the underside of leaves, twigs and

fruits. Mite feeding sites turn rusty brown on fruits and appear as brownish/bronze-patches on leaves, which eventually fall (Zaher et al. 1970). In Egypt, biological aspects of B. obovatus were investigated by Wahab et al. (1974 ) and Shereef and Hanna (1981). The present work is aimed at studying the seasonal abundance and biology of the Brevipalpus obovatus on two of its major hosts, citrus and mint. In addition, field control of this mite on citrus trees using two acaricides was also studied.

MATERIALS AND METHODS 1. Mite population density on citrus trees

Brevipalpus obovatus was monitored on citrus trees (Citrus sinensis, Washington Navel Orange) for 12 months (Sept. 1995 to Aug. 1996) at the North Tahrir agriculture company, 40 km south of Alexandria. The total geographical area of the company is about 18,000 ha. Most of the land is calcareous loam with calcium

291

Hussien A. Rezk

Figure 1

The relationship between seasonal abundance (bold line) of Brevipalpus obovatus on citrus trees from September 1995 to August 1996 and temperature (regular line) at Tahrir.

carbonate. Samples of 30 leaves were randomly collected from different trees twice a month and carefully transported to the laboratory. Leaves were examined under a stereoscopic microscope and mites were counted (Rezk and Gadelhak 1996). Meteorological data were provided by the Alexandria Meteorological Station. 2. Biological studies

All experiments were carried out using descendants of twenty females taken from the field. Mites were raised under laboratory conditions (25±2ºC and 65±5% RH) on citrus (Citrus sinensis) and mint leaves (Mentha arvensis) according to the method described by Zaher et al. (1970). Newly hatched larvae were confined individually on leaves. Each was encircled by Vaseline and citronella oil and allowed to continue development. Observations were made twice a day. The duration of egg, larva, protonymph, deutonymph and adult stage were observed for five generations. Hatch rate, female longevity (as pre-, post- and oviposition periods) and female fecundity were also recorded. Measurements of the different developmental stages were taken for both the length and width of about 10 to 15 individuals of each stage. 3. Field control

The effect of two acaricides on B. obovatus was evaluated in citrus orchards. The acaricides were (1) Ortus (fenpyroximate) 5% SC at 50 ml/100 litre (tert-Butyl (E)-alpha-(1,3-dimethyl-5-phenoxypyrazol-4-methyleneaminoxy)-p-toluate (Nihon Nohyaku, Tokyo, Japan); (2) Neoron 500 (bromopropylate) at 100 ml/100 litre (isopropyl-4,4-di-bromobenzilate (Ciba-Geigy, Cairo, Egypt). Treatments were arranged in a complete randomised block design with three replicates plus a control. Each replicate was 6 × 7 metres, containing 8–10 orange trees. Sampling and counting were conducted as described by Rezk and Gadelhak (1996).

RESULTS AND DISCUSSION 1. Mite population density on citrus trees

The populations of Brevipalpus obovatus on citrus trees (Fig. 1) were generally limited throughout the year and the size of the population fluctuated throughout the seasons. Generally speaking, mite the population declines sharply at the end of summer (August) and increases during winter. Populations peak in early

292

spring (February) reaching an average of 21.23±0.8 mites/30 leaves, and autumn (September-November) ranging between 15.7±1.2 and 18.39±0.9 mites/30 leaves. This rise in mite population could be due to more favourable environmental conditions. The results revealed that the mite population was affected by temperature and relative humidity. This agrees with the findings of Rizk et al. (1978), Raizer et al. (1988), and Sadana and Kumari (1991). On the other hand, Rezk and Gadelhak (1996) found that B. obovatus is a major prey for predatory mites on citrus in the summer months. This rise in mite population could be due to more favourable conditions, changes in host plant conditions or natural enemies (e.g. Agistemus exsertus, Amblyseius spp. and Cheletogenes ornatus). 2. Biological studies

Field observations indicated that different stages of B. obovatus inhabit either leaves or buds, fruits and new flushes of citrus trees throughout the year. Females, which are parthenogenetic, deposit eggs in protected places like pits and concave areas around the mid rib and main veins. Eggs are laid individually but rather close to each other so that they may appear to be clustered. Eggs hatch into the six-legged larval stage that feeds for a short time and then enters the first quiescent stage. Protonymphs then emerge and resume feeding to enter the second quiescent period. Active deutonymphs repeat the same trend and reach the third quiescent stage, then adult females emerge. In the laboratory, B. obovatus was reared on both citrus and mint leaves for five generations. Newly deposited eggs were red in colour, and average egg dimensions were 83.2 ± 2.6 µm (length) and 58.2±3.4 µm (width). The average number of eggs/female was 9.67±0.47 and 7.06±0.96 on citrus and mint leaves, respectively. Morishita (1954) found that female B. inornatus ( = obovatus) laid an average of 26.8 eggs, ranging from 0.0 to 60 at 27°C. The egg stage lasted for 3.07±0.7 and 4.16±1.1 days for citrus and mint, respectively, while the hatch rate was 87.49±1.08 and 72.9±2.13% for the two hosts. Wahab et al. (1974) stated that the incubation period of B. obovatus lasted an average 6.3±0.8, 6.0±1.2 and 7.2±1.2 days on Ipomoea batatas, Adhatoda vasica and Myoporum pictum leaves, respectively, at 30°C and 54% RH.

THE FALSE SPIDER MITE BREVIPALPUS OBOVATUS DONNADIEU

Figure 2

Effects of Ortus and Neoron on populations of Brevipalpus obovatus in a citrus orchard. Values are number of mites ± SE.

The different hosts used and the higher rearing temperature plus lower RH could explain the discrepancy between the two sets of data. Shereef and Hanna (1981) also found an incubation period of 8.06 days at 25±1°C and 65±5% RH on peppermint. The larval stage was oval-shaped and 143±3.1 µm in length, 87.5±2.2 µm in width . The active larval stage lasted for 2.76±0.4 and 3.13±0.7 days, while the quiescent larvae required 1.9±0.6 and 2.0±0.5 days on citrus and mint, respectively. The protonymphal stage measured 175.4±1.6 µm in length and 105.5±2.4 µm in width and lasted for 2.63±1.3 and 3.23±0.7 days, while the quiescent stage lasted 1.93±0.6 and 2.13±0.3 days on citrus and mint, respectively. These findings agree with Shereef and Hanna (1981). The deutonymphal stage was about 225.6±3.1 µm in length and 115.2±2.8 µm in width and lasted for 3.21±0.2 and 4.53±0.3, while the quiescent lasted for an average of 1.46±0.5 and 2.63±0.8 days before becoming adults on citrus and mint, respectively. These data slightly differ from those of Wahab et al. (1974) and Shereef and Hanna (1981). The life span of B. obovatus (from egg to adult) lasted 17.0±2.1 and 21.83±2.8 days on citrus and mint, respectively. Wahab et al. (1974) reported the life span to be 27–30 days on different hosts and under different rearing conditions. The preoviposition, oviposition and postoviposition periods lasted an average of 2.96±1.1; 20.3±2.3 and 11.0±1.8 days on citrus and 3.06±0.9; 22.43±3.1 and 15.66±2.1 days on mint. This agrees with Wahab et al. (1974), Shereef and Hanna (1981). Female longevity averaged 34.26±3.7 and 41.16±3.4 days on citrus and mint. Analysis of variance showed that the longevity on mint is significantly longer than that on citrus. 3. Field control

The effect of fenpyroximate and bromopropylateon B. obovatus was tested in citrus orchards (Fig. 2). The data revealed that both acaricides gave good control of this mite for nearly seven days post-treatment. On the other hand, fenpyroximate (Ortus) had a

quicker effect. After 2 days, bromopropylate (Neoron) the percentage population reduction was 77.95% while, it was 91.05% for Fenpyroximate. Control of false spider mites has been discussed extensively by several authors (Frick 1961; Elmer and Jeppson 1957; Zohdi 1967; Guirguis et al. 1979). In Brazil, Oliveira et al. (1983), Geos et al. (1985), Nakano et al. (1987) and Raga et al. (1992) evaluated the efficacy of bromopropylate in comparison to carbamates and formamidines for control programs. They found that bromopropylate achieved best results and recommended it for the control of these mites. Others have used growth regulators (Raizer et al. 1988) but these were less effective in Brazil. The synthetic pyrethroid abamectin and fungicides have also been tested (Rocha-Santos et al. 1988; Childers 1994). In Egypt, Guirguis et al. (1979) found that dicofol and chlordimeform controlled the mite population on peppermint plants. Zohdi (1967) and Elmer and Jeppson (1967) indicated that kelthane-S proved to be effective. In conclusion, the false spider mite B. obovatus, peaks twice under field conditions, once in early spring and the other during fall. Laboratory rearing of this mite is best done using citrus leaves. Although mint seedlings are easier to handle, better biological parameters were achieved on citrus as a host. Control of the false spider mite under field conditions was achieved using both Ortus and Neoron acaricides. Ortus decreased the mite population faster than Neoron.

ACKNOWLEDGEMENTS The author wishes to thank Dr G. G. Gadelhak for critical review of the manuscript and valuable help.

REFERENCES Attiah, H. H. (1956). The genus Brevipalpus in Egypt (Acarina: Tenuipalpidae). Bulletin de la Societe Entomologique de Egypte 40, 433–448.

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Hussien A. Rezk Baker, E. W., and Tuttle, D. M. (1964). The false spider mites of Arizona (Acarina : Tenuipalpidae). University of Arizona Technical Bulletin 163, 1–80. Childers, C. C. (1994). Feeding injury to Robinson tangerine leaves by Brevipalpus mites (Acari: Tenuipalpidae) in Florida and evaluation of chemical control on citrus. Florida Entomologist 77, 265– 271. Denmark, H. A. (1984). Brevipalpus mites found on citrus (Acari: Tenuipalpidae). Entomology Circular, Division of Plant Industry, Florida Department of Agriculture and Consumer Services 69, 1–2. Elmer, H. S., and Jeppson, L. R. (1957). Biology and control of the citrus flat mite. Journal of Economic Entomology 50, 566–570. Frick, K. E. (1961). Control of insects and mites attacking mint in Washington. Journal of Economic Entomology 54, 466–649. Goes, A. de; Barros, J. C., and Alves, R. C. P. (1985). Citrus leprosis: The mite and its control. Comunicado Técnico, PESAGRO RIO 148, 1–2. Guirguis, M. W., Gomaa, E. A.; Yousef, A. A. and Abd El-Rahman, M. M. T. (1979). Effect of some pesticides on pepperiment and its infestation with mite Brevipalpus obovatus, (Donn.). Zagazig Journal of Agricultural Research 6, 1–13. Morishita, F. S. (1954). Biology and control of Brevipalpus inorntus (Banks). Journal of Economic Entomology 34, 449–456. Nakano, O., Aguilar-Sanches, G., and Ishida, A. K. (1987). Reduction of Brevipalpus phoenicis (Geijskes), infestations in citrus through the control of scab. Laranja 1, 19–33. Oliveira, C. A. de, Silva, J. R., and Rigotto, E. L. de (1983). Control of leprosis mite, Brevipalpus phoenicis (Geijskes) Acari: Tenuipalpidae with chemical products on citrus crops. Anais da Sociedade Entomologica do Brasil 12, 221–234. Pritchard, A. E., and Baker, E. W. (1958). The false spider mites (Acarina: Tenuipalpidae). University of California Publications in Entomology 14, 175– 274. Raga, A., Sato, M. E., Ceravolo, L. C., Rossi, A. C., and Scarpellini, J. R. (1992). Effect of acaricides on the leprosis mite Brevipalpus phoenicis (Geijskes), in a citrus orchard in Presidente prudente SP. Ecossistema 15, 98–103. Raizer, A. J., Motta, R., Sugahara, C. A., Silva, J. M., Arashiro, F. Y., and Marconi, F. A. M. (1988). Control of the leprosis mite Brevipalpus phoenicis (Geijskes) on citrus with chemical acaricides, including chitin synthesis inhibitors. Anais da Sociedade Entomologica do Brasil 12, 271–281.

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Rasmy, A. H. (1966). ‘Integrated Control of Citrus Mites.’ Ph. D. Thesis, Faculty of Agriculture, Cairo University, Egypt. Rezk, H. A., and Gadelhak, G. G. (1996). Relationship between phytophagous and predatory mites in citrus orchards and the effect of acaricides on their populations. Alexandria Journal of Agricultural Research, 41, 217– 224. Rizk, G. A., Karaman, G. A., and Ali, M. A. (1978). Population densities of phytophagous and predaceous mites on citrus trees in middle Egypt. Bulletin de la Societe Entomologique de Egypte, 62, 97–103. Rocha-Santos, V. V., Silva, de, A. L., Sanchez, S. E. M., and Rocha, M. R. da. (1988). Chemical control of the mite Brevipalpus phoenicis (Geijskes), Acari, Tenipalpidae: transmitter of leprosis in citrus. Anais das Escolas de Agronomia e Verterinaria (Goiânia)18, 141–149. Sadana, G. L., and Kumari, M. (1991). Effect of temperature And relative humidity on the development of Brevipalpus phoenicis (Geijskes) Acari: Tenuipalpidae. Journal of Insect Science 4, 157– 159. Shereef, G. M., and Hanna, M. A. (1981). Biological studies on two mite species injurios to Camphor, Rose and Pepperment, with first description of their prelarvae. Bulletin de la Societe Entomologique de Egypte 68, 49–55. Wafa, A. K.; Zaher, M. A. and Yousef, A. A. (1969). Survey of the Tenuipalpid mites in UAR. (Acarina : Tenuipalpidae). Bulletin de la Societe Zoologique de Egypte 22, 52–59. Wahab, A. E. A., Yousef, A. A., and Hemeda, H. M. (1974). Biological studies on the tenuipalpid mite Brevipalpus obovatus Donnadieu (Acarina : Tenuipalpidae). Bulletin de la Societe Entomologique de Egypte. 58, 317– 321. Yousef, A. A. (1967). ‘Ecological and biological studies on mites of family Tenuipalpidae in UAR.’ Ph. D. Thesis, Faculty of Agriculture, Cairo University, Egypt. Zaher, M. A., and EL-Badry, E. A. (1964). Survey and population studies on red false spider mites. Acarologia 9, 425–433. Zaher, M. A., Wafa, A. K., and Yousef, A. A. (1970). Biology of Brevipalpus phoenicis (Geijskes) in Egypt. Bulletin de la Societe Entomologique de Egypte. 54, 177–183. Zohdi, G. I. M. (1967). The chemical control of some tenuipalpid mites (Acarina: Tenuipalpidae). M. Sc. Thesis, Ain-Shams University, Cairo, Egypt.

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

ACAROLOGY

COMPARISON OF FEEDING DAMAGE BY REDLEGGED EARTH MITE HALOTYDEUS DESTRUCTOR (TUCKER) (ACARI: PENTHALEIDAE) TO DIFFERENT GRAIN LEGUME SPECIES AS AN INDICATOR OF POTENTIALLY

A. Liu1 and T. J. Ridsdill-Smith1,2 1

Cooperative Research Center for Legumes in Mediterranean Agriculture, The University of Western Australia, Nedlands, WA 6907, Australia 2 CSIRO Entomology, Private Bag, Wembley, WA 6014, Australia

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RESISTANT LINES

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Abstract Twenty two species of grain legumes from four genera that are important or potentially important to Australian agriculture were examined for their response to feeding by redlegged earth mite (Halotydeus destructor) under controlled conditions. Special attention was paid to differences among species within a genus. Plants were exposed to mites at the seedling stage and feeding damage scored one week and two weeks after mite application. The results showed that within the genus Lupinus, lines of yellow lupin (L. luteus) had the highest feeding scores, while mites fed less on lines from narrow-leafed lupin (L. angustifolius). Lines from albus lupin (L. albus) and rough seeded lupins (L. atlanticus, L. cosentini, L. pilosus) suffered minimal attack by mites. H. destructor feeding damage also differed between species from the genus Vicia. V. sativa was attacked most, while V. ervillia and V. articulata were fed on very little. Five species from Lathyrus differed in levels of H. destructor feeding damage. L. tingitanus and L. ochrus were fed on most. L. cicera and L. sativus were fed on very little. Species and subspecies from Pisum were readily damaged by H. destructor feeding, with no significant variation among them. It is unlikely that the same mechanisms cause resistance to H. destructor over such a range of species. Mite feeding was clearly affected by interspecific variation within genera. A better knowledge of the mechanisms involved will assist selection and breeding of crops showing resistance to this pest.

INTRODUCTION Redlegged earth mite, Halotydeus destructor (Tucker) (Acari: Penthaleidae) is a serious pest in Australian agriculture. It is mainly distributed through the southern parts of Australia with a Mediterranean type climate (Wallace and Mahon 1971). Its northern or inland distribution coincides with the 205 mm isohyet for the May–October growing season, and its eastern distribution with the 225 mm isohyet for the December–March growing season. Within its distribution region, it attacks a wide range of crop species (McDonald et al. 1994; Ridsdill-Smith 1997). Recently, as the area planted to grain legume crops in Australia has been expanding quickly (Gladstones 1994; Hamblin et al 1997; Siddique and Sykes 1997) and mostly within the regions

where H. destructor was distributed, attention has again been given to their susceptibility to H. destructor and the potential loss caused by this pest. Grain legume species vary in their susceptibility to H. destructor (Bailey 1952; Gladstones 1969a; McDonald et al 1994; Thackray et al 1997). New research has been started to investigate the susceptibility of a wider range of plant species and lines to study their relative susceptibility to H. destructor, with the aim of identifying resistant lines and incorporating resistance into breeding programs. This paper reports on the screening of a range of grain legume species that are of potential importance to Australian agriculture, and especially variation in susceptibility among species within a genus.

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A. Liu et al. Table 1

Observations of numbers of mites on foliage of plants of different Lupinus species 4 and 7 days after mite application (100 mites/plant). Mites per plant 4-day

7-day

Lines used

L. angustifolius

Species

13

10

3

L. luteus

17

13

2

L. albus

9

9

1

L. atlanticus

4

6

1

L. cosentini

3

5

1

L. pilosus

2

1

1

LSD 0.05

8

7

–

MATERIALS AND METHODS Screening was conducted over a range of genera and species for their relative susceptibility to redlegged earth mite. Most screenings were conducted in the growth rooms of Agriculture Western Australia, South Perth. The temperature of the growth rooms was maintained at 18°C /13°C in a 12/12 hr day/night cycle. The light intensity during the day was around 250 ME.M–2.S–1. Soil moisture was maintained by an auto reticulating system with occasional hand watering to the dry spots. Before sowing, seeds were soaked for one or more days in petri dishes in an incubator set at 20°C, until they germinated. Time of soaking and sowing were arranged in a way that lines from different species would emerge at a similar time. Seeds were inoculated with the recommended inoculum. Mites were collected from pasture plots or raised in the control rooms and introduced to plants 2 to 3 days after emergence at a density of about 100 mites per plant. A thin layer of sphagnum moss was spread on top of the soil surface in the pots to increase the humidity at the soil surface to reduce mite mortality (except Experiment 5 in the field). One week after the first mite introduction, another 100 mites per plant were applied to supplement the observed decrease in mite number. The damage scoring system was adopted from the method used by Gillespie (1993) on subclover, with 1 representing no visible damage and 9 all plant surface silvered or distorted. In addition observations were made in Experiment 1 on the number of mites on the upper surface of leaves on days 4 and 7 in every pot. Only about 10% of individuals in a H. destructor population are on the canopy feeding at any one time (Gaull and Ridsdill-Smith 1996), and the observations represent an index of mite feeding on the different lupin species. In Experiment 1, nine lines from six Lupinus species were screened. Germinated seeds were sown into each 150 mm pot filled with potting mix. Mite number on the plant were counted at four and seven days after the first mite application. Fourteen days after the mite application, the plants were taken out of the pots and the roots separated out by sieving. Plants were then dried in an oven at about 80°C and weighed. In Experiment 1, a splitplot experimental design was used with lines as the main plot and mite treatment (plus or minus mites) as the subplot. The minus mite treatment was used as a control to calculate the dry weight reduction after mite attack.

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In Experiment 2, 17 lines from five Lathyrus species and 16 lines from six Vicia species were screened. Two lines of field pea were also used as controls. In Experiment 3, a total of 48 lines from two Pisum species (one of the species covering eight subspecies) were screened. In Experiments 2 and 3, lines were arranged in an alpha design with three (four for Experiment 3) blocks of 12 lines each, replicated four times. Each block (12 lines) was sown to a tote box 40 cm long × 30 cm wide × 20 cm deep and filled with a soil mix. In Experiment 4, 12 lines from six legume species of five genera were compared for their relative susceptibility to redlegged earth mite under glasshouse conditions. In Experiment 5, one line from each of the six legume species used in Experiment 4 was sown under field conditions to test their relative susceptibility to H. destructor. In Experiments 4 and 5, lines were arranged in randomised block experimental designs. Data were analysed using Genstat 5.3.2 according to the relevant designs.

RESULTS Mite behaviour

After application, it was observed that mites were active on the soil surface and on plants. At days four and seven after mite application, more mites were observed on L. angustifolius and L. luteus than on other species (Table 1). Attack on cotyledons of lupin resulted in silvering of the surface. The mite not only attacks the upper surface of the cotyledons, it also can damage the underside and the hypocotyls of some species (such as L. angustifolius cv. Myallie). Attack on the true leaves may also involve both leaf surfaces and leaf edges, which can result in deformed leaves. The cotyledons of L. angustifolius also tended to drop off the plant after being severely damaged, while on L. luteus they were retained. The rough-seeded lupins (L. atlanticus, L. cosentini and L. pilosus) and L. albus have hairy leaves, and hypocotyls (except L. pilosus and L. albus). It was observed that it was difficult for mites to climb the stems of these plants and to move about on the leaves. Deformation of leaves after damage was most serious on pea plants and mites appeared to seek protection inside the deformation. Damage to Vicia faba plants and Vicia narbonensis resulted in browning of the leaves in the damaged areas resembling that of the fungal disease ‘chocolate spot’. Possibly there was a secondary fungal infection following mite attack. Under field conditions, little damage was observed on the upper surface of the Vicia faba leaves, but there were patches of silvering on the underside. The damage was less severe under field conditions than in the glasshouse . Mite damage

(a) Lupinus species Mite feeding damage on Lupinus varied considerably among species (Table 2). One week after application, mites attacked nearly 100% of the surface area of the cotyledons of the lines of L. angustifolius and L. luteus. No significant differences were found among lines within these species. The damage scores for L. angustifolius and L. luteus were higher than those for L. albus and rough-seeded lupins (L. atlanticus, L. cosentini and L. pilosus) (Table 2). Damage scores on the true leaves of L. luteus was highest, followed by that of L. angustifolius. L. albus and rough-seeded lupins had the

FEEDING DAMAGE BY HALOTYDEUS DESTRUCTOR

Table 2

TO GRAIN LEGUMES

Damage score of different Lupinus species 7 days and 14 days after mite application. Average damage score Cotyledon

Species

True leaf

Lines

Dry weight

number

% of control

7-day

14-day

7-day

14-day

L. angustifolius

8.8

8.9

4.3

4.4

3

32

L. luteus

9.0

9.3

6.9

9.3

2

43

L. albus

2.3

2.3

1.3

1.0

1

1

L. atlanticus

5.3

5.8

1.0

2.0

1

12

L. cosentini

2.7

2.0

2.7

2.0

1

8

L. pilosus

1.0

1.0

1.0

1.0

1

3

LSD 0.05

1.6

1.9

2.2

2.5

–

24

Table 3

Damage score of some Lathyrus and Vicia species screened against H. destructor. Average damage score

Range between lines

7-day

14-day

(14-day)

Number of lines used

Lathyrus cicera

1.7

1.5

1.0–2.0

5

L. clymenum

4.4

5.8

5.0–6.5

2

L. ochrus

5.2

5.8

5.0–6.5

L. sativus

1.4

1.4

1.0–1.5

L. tingitanus

8.5

8.8

Pisum sativum

4.8

5.4

Vicia articulata

1.1

1.8

V. benghalensis

4.5

V. ervillia V. narbonensis

Species

Table 4

14-day

Damage by H. destructor to various Pisum species and subspecies. Average damage score

Range between lines

7-day

14-day

(14-day)

Number of lines used

P. sativum

8.2

7.9

7.5–8.3

3

ssp. abyssinicum

8.9

8.9

7.9–9.3

7

3

ssp. syriacum

8.4

8.3

7.0–9.1

5

5

ssp. jomardii

8.5

8.5

8.5

1

8.8

2

ssp. elatius

8.4

8.6

8.0–9.0

7

5.2–5.8

2

ssp. nepalensis

8.1

7.4

7.4

1

1.5–2.0

2

ssp. thebicum

8.3

7.2

7.2

1

3.5

3.5

1

9.0

8.9

8.6–9.0

5

1.2

1.5

1.0–2.0

5

ssp. transcausicum

3.0

4.6

2.8–6.0

4

P. fulvum

9.1

9.3

9.0–9.6

18

LSD 0.05

0.89

0.72

–

–

V. sativa

7.8

7.6

7.5–7.8

4

V. villosa

5.6

5.8

5.8

1

LSD 0.05

1.2

1.2

–

–

lowest damage. Only a few small patches of damage occurred on cotyledons of L. atlanticus and L. cosentini. No damage was observed on the L. pilosus line indicating its possible immunity to H. destructor. Dry-weight of the damaged plants measured 14 days after mite application was significantly reduced on susceptible Lupinus species (Table 2). L. luteus suffered the most (43%), followed by L. angustifolius (32%). No significant reduction was found in other species tested. It was also observed that cotyledons of L. angustifolius were shed sooner than those of L. luteus when damaged under field conditions. (b) Lathyrus and Vicia species As variation among lines within the same species was small, the average and range of damage score for each species are presented in Table 3. Mite feeding varied considerably among Lathyrus species, with L. cicera and L. sativus being least attacked and L tingitanus the most. Among the Vicia species, V. articulata and V. ervillia were the most resistant, and V. villosa the most susceptible to mite feeding. One line of V. narbonensis had a lower damage score than other lines in the same genus.

Species or ssp.

(c) Pisum species Although there was some variation among lines from Pisum, all 48 lines were susceptible to mite feeding (Table 4). Since the damage scores to plants were so high no further scoring was conducted. Comparison of field and glasshouse data

Grain legume species from the five genera varied considerably in their susceptibility to redlegged earth mite. P. sativum and L. luteus were the most susceptible to mite feeding damage followed by V. faba and L. angustifolius (Table 5). Mites did not appear to feed on Cicer arietinum and there was little damage to Len culinaris. Results from the glasshouse generally agreed with those from the field.

DISCUSSION It has been observed that H. destructor not only attacked the upper surface of the cotyledons and the true leaves, but also their lower surface and even the surface of the hypocotyl of some lines, such as was observed on L. angustifolius cv. Myallie. The loss of cotyledons (L. angustifolius) and deformation of true leaves could result in reduced plant growth and root function as indicated by a dry weight reduction in these plants.

297

A. Liu et al. Table 5

Damage score of six legume species under glasshouse and field conditions 14 days after mite application. Damage scores for the two Lupinus species are the average between those for true leaves and cotyledons. Damage score Glasshouse (1996)

Species

Field (1997)

14-day

lines-used

14-day

lines used

P. sativum

7.1

2

7.3

1

Lupinus luteus

7.8

1

8.4

1

L. angustifolius

5.6

1

6.0

1

Vicia faba

3.6

2

2.4

1

Len culinaris

2.0

2

1.0

1

Cicer arietinum

1.0

4

1.0

1

LSD 0.05

1.3

–

0.13

–

However, variation among lines within the same species was small. Because only two lines from L. luteus were used and both are sweet selections (B. Buirchell, personal communication), it is too early to make any conclusions regarding variation in their susceptibility to H. destructor. Due to its high susceptibility to H. destructor and its potential for expanded planting in commercial production in Western Australia (Sweetingham et al. 1996), selection for resistance from a wide range of germplasms has commenced. Recent work has found some resistance in lines of this species (A. Liu, unpublished data). H. destructor feeding damage scores varied considerably among the six lupin species studied. The data reported here are in agreement with the comments provided by Gladstones (1969a) for the four species he mentioned (L. cosentini, L. luteus, L. angustifolius, L. albus). The variation among Lupinus species in response to feeding by H. destructor could be the result of a number of factors. Lupin species and lines contain a wide range of alkaloids, and breeding programs have placed great effort into reducing the alkaloid content of seed being used for animal feed (Gladstones 1969a). Most cultivars and advanced lines now have low levels of alkaloid content in their seed. For example, the alkaloid content in the seeds of L. angustifolius (0.01–0.04 µg/kg), L. albus (0.01–0.02) and L. luteus (0.01–0.10) is low, but in the seeds of rough-seeded lupins (L. atlanticus: 0.26–0.45, L. pilosus: 0.56–0.73) (Petterson et al 1997) and L. cosentini (Gladstones 1969b) it is high. Berlandier (1996) recorded a negative correlation between high alkaloid content in lines of L. angustifolius and aphid performance. A low level of alkaloid concentration in new cultivars could also make them more prone to mite attack. Leaf hairiness which may inhibit mite feeding could also be an important contributor to resistance to H. destructor in L. albus and rough-seeded lupins. Most lines of the rough-seeded types tested have hairs on the true leaves and hypocotyl. Variation in response to feeding by H. destructor among species of Lathyrus and Vicia was considerable, and ranged from nearly immune to highly susceptible. The chemical ODAP (b-N-oxalylL-a-b-diaminopropionic acid) produced by Lathyrus is a neuro-

298

toxin which can cause lathyrism, a paralysis of the lower limbs of humans, when a large amount is consumed over a considerable period. ODAP concentration appears to be inversely related to susceptibility to H. destructor. Siddique et al (1996) reported that the ODAP content of three Lathyrus species (seed) was L. ochrus > L. sativus > L. cicera, while the damage scores of the three species in this experiment were L. ochrus > L. sativus = L. cicero. ODAP concentration varies considerably among genotypes and can be affected by environmental conditions (Siddique et al 1996), and ODAP concentrations in the seedlings which mites attack may not be related to that in the seeds. Variation among Pisum species and sub-species was small and all lines tested were quite susceptible. Although considerable resistance to pea weevil (Bruchus pisorum) was found in P. fulvum (Hardie 1997), resistance to H. destructor was not found in this species. It appeared that low seedling vigour could be one of the reasons for the severe damage inflicted, especially to some of the wild types. One line of Pisum ssp. syriacum suffered the least damage, but even so, was severely affected. Observations suggest that this susceptibility may have been over-estimated due to its slow growth, so that when other plants in the screening box were heavily damaged, more mites turned their attention to it. A nonchoice experiment might clarify this. Also, more lines should be included in future screening to find potential resistant resources. In conclusion, considerable variations in susceptibility to H. destructor were found among species within the same genus, except for Pisum. The mechanisms of the resistance could involve different factors. Some factors that are desirable for mite resistance may be undesirable for the qualities of the plant seed as animal feed. Further information is required in order to be able to use the various resistance factor in plant breeding.

ACKNOWLEDGEMENTS We thank Drs B. Buirchell, M. Sweetingham, D. Enneking, D. Hardie and C. Hanbury for advice on various lines used in the screening and for supplying seeds. This research was supported by the Grains Research and Development Corporation.

REFERENCES Bailey, E. T. (1952). Agronomic studies of vetches and other large-seed legumes in southern Western Australia. CSIRO Division of Plant Industries Technical Paper 1, 3–21. Berlandier, F. A. (1996). Alkaloid level in narrow-leafed lupin, Lupinus angustifolius, influences green peach aphid reproductive performance. Entomologia Experimentalis et Applicata 79, 19–24. Gaull, K. R., and Ridsdill-Smith, T. J. (1996). The foraging behaviour of redlegged earth mite, Halotydeus destructor (Acarina: Penthaleidae), in an annual subterranean clover pasture. Bulletin of Entomological Research 86, 247–252. Gillespie, D. J. (1993). Redlegged earth mite (Halotydeus destructor) resistance in annual pasture legumes. In ‘Pests of Pastures: Weed, Invertebrate and Disease Pests of Australian Sheep Pastures’. (Ed. E. Delfosse.) pp. 211–213. (CSIRO: Melbourne.) Gladstones, J. S. (1969a). Lupins in Western Australia: 3. cultivation methods. Journal of the Department of Agriculture of Western Australia 10, 477–484.

FEEDING DAMAGE BY HALOTYDEUS DESTRUCTOR

Gladstones, J. S. (1969b). Lupins in Western Australia: 1. species and varieties. Journal of the Department of Agriculture of Western Australia 10, 318–324. Gladstones, J. S. (1994). An historical review of lupins in Australia. In ‘Proceedings of the First Australian Lupin Technical Symposium’. Perth. (Eds M. Dracup and J. Palta.) pp. 1–38. (Department of Agriculture, Western Australia: South Perth.) Hamblin, J., Hawthorne, W., and Perry, M. (1997). Pulses: An Australian success story. Australian Grain 7, 26–27. Hardie, D. C., Clement, S. L., Elberson, L. R., Collie, H.,and Byrne, O. M. (1997). Detection and comparison of pea weevil resistance in wild pea germplasm in Australia and USA. ‘Proceedings of the International Food Legume Research Conference III.’, p. 171. Adelaide, Australia. McDonald, G., Moritz, K., Merton, E., and Hoffmann, A. A. (1994). The biology and behaviour of redlegged earth mite and blue oat mite on crop plants. Plant Protection Quarterly 6, 168–169. Petterson, D. S., Sipsas, S., and Mackintosh, J. B. (1997). ‘The chemical composition and nutritive value of Australian pulses (2nd edition).’ (Grains Research and Development Corporation: Canberra.)

TO GRAIN LEGUMES

Ridsdill-Smith, T. J. (1997). Biology and control of Halotydeus destructor (Tucker) (Acarina: Penthaleidae): a review. Experimental and Applied Acarology 21, 195–224. Siddique, K. H. M., Loss, S. P., Herwig, S. P., and Wilson, J. M. (1996). Growth, yield and neurotoxin (ODAP) concentration of three Lathyrus species in Mediterranean-type environments of Western Australia. Australian Journal of Experimental Agriculture 36, 209–218. Siddique, K. H. M., and Sykes, J. (1997). Pulse production in Australia past, present and future. Australian Journal of Experimental Agriculture 37, 103–111. Sweetingham, M., French, M., Dracup, M., MacLeod, B., Carr, S., Davies, C., and Shea, G. (1996). Yellow lupins: a new grain crop for acid soils. Australian Grain 6, 6–8. Thackray, D., Ridsdill-Smith, T. J., and Gillespie, D. J. (1997). Susceptibility of grain legume species to redlegged earth mite (Halotydeus destructor Tucker) damage at the seedling stage. Plant Protection Quarterly 12, 141–144. Wallace, M. M. H., and Mahon, J. A. (1971). The distribution of Halotydeus destructor and Penthaleus major in Australia in relation to climate and land use. Australian Journal of Zoology 19, 65–76.

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ACAROLOGY

Acarology: Proceedings of the 10th International Congress. R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton and M. J. Colloff (eds). CSIRO Publishing, Melbourne, 2001

DENSITIES OF PANONYCHUS ULMI (ACARI: TETRANYCHIDAE) AND ACULUS SCHLECHTENDALI (ACARI: ERIOPHYIDAE) ON THREE APPLE CULTIVARS IN WESTERN NORWAY ....................................................................................................

Mofakhar S. Hossain1 and Torstein Solhøy Department of Animal Ecology, Institute of Zoology, University of Bergen, N-5007 Bergen, Norway. 1 Present address: Institute of Sustainable Irrigated Agriculture,Tatura Centre, Private Bag 1, Tatura, Victoria 3616, Australia

.................................................................................................................................................................................................................................................................

Abstract The overwintering populations of Panonychus ulmi and Aculus schlechtendali showed small variations in densities on three different cultivars of apple, Aroma, Summerred and Gravenstein. The summer population densities of P. ulmi and A. schlechtendali were significantly different on the different cultivars. Aroma had the highest number (21/leaf) of P. ulmi per leaf at the end of June. On the other hand, Summerred showed the highest (936/leaf) numbers of A. schlechtendali per leaf in the middle of August. There was a gradual increase in the density of A. schlechtendali during the study period.

INTRODUCTION Two phytophagous mites, the European red mite, Panonychus ulmi (Koch) and the apple rust mite, Aculus schlechtendali (Nalepa) are the most important acarine pests of apples in western Norway. During the last few years these two mites have become more abundant, often reaching damaging levels in conventionally sprayed orchards (K. Hesjedal, personal communication). The size of the overwintering population reflects, to a certain extent, the size of the mite population in the preceding season, and also indicates the potential for attack in the following year. Easterbrook and Fuller (1986) showed that the most sensitive period of russet damage caused by A. schlechtendali was shortly after the blossom period. They also suggested that the best method for assessment of damage risk was to estimate the overwintering population of mites and to apply a pre-blossom acaricide if necessary. Wardlow and Jackson (1984) reported that the threshold for potential crop damage may be as few as 10 rust mites per bud during winter. The time of the year at which mite populations attack trees is extremely important in determining the effect on production.

300

Chapman (1959) reported that a population of 67 spider mites per leaf in early July had no appreciable effect on the yield of apples, while Boulanger (1958) pointed out that it was the early season populations that were the most critical. Despite the widespread distribution of P. ulmi and A. schlechtendali on apples in western Norway, no aspects of their seasonal variations and variations in numbers on different cultivars have been studied. In this study, an attempt was taken to estimate the size and distribution of the overwintering population of both mites in 1988/89 and 1989/90. In 1989, the summer population densities of both mite species were also regularly monitored. The apple rust mite can play an important role in integrated pest management programs as an alternative food source for different predacious arthropods (e.g. bugs and mites) in the apple orchards when common prey items are depleted (Herbert and Sanford 1969; Hoyt 1969a; Croft 1975; Solhøy et al. 1991). It is therefore important to allow an increase in population density of A. schlechtendali in orchards in order to provide food for predators, but the density should not rise above that tolerable to the trees. Solhøy et al. (1991) reported that the Aroma cultivar in western Norway

DENSITIES OF PANONYCHUS ULMI AND ACULUS SCHLECHTENDALI

ON THREE APPLE CULTIVARS IN WESTERN

NORWAY

seemed to be resistant to high populations of rust mites, which may be valuable for integrated pest management.

MATERIALS AND METHODS Study area

The study was carried out in two apple orchards, Kvitavoll (0.63 ha) and Løeflaten (0.19 ha) at Ullensvang Research Station, Lofthus, western Norway, at an altitude of about 15 m.a.s.l. During the growing season (May-September) 1989, the average temperature was 12.3°C and the rainfall was 429 mm. The corresponding normal values are 13.0°C and 392 mm, respectively. The orchard at Kvitavoll contains three different apple cultivars, Aroma, Summerred, and Gravenstein, and is 14 years old. There were four rows of each cultivar, each consisting of about 35 trees. The Løeflaten orchard, eight years old, contained 16 rows, each of about 20 trees of the cultivar Aroma. Sampling of overwintering populations

Overwintering eggs of P. ulmi are oviposited in-groups, mostly on two or three year old spurs and branches (Hoyt 1969b). In January 1989 and 1990, two year old branches were collected from all cultivars of apples at Kvitavoll and from Aroma at Løeflaten. One hundred branches of each cultivar were collected and one oviposition site (mostly nodes of branches) from each branch were examined. The number of eggs at each site was graded as follows: 0, 1–50, 51–100, 101–150, 151–200, and >200. Aculus schlechtendali overwinter as deutogyne females (Easterbrook 1984). Fifteen long shoots were collected from each apple cultivar at Kvitavoll and from Aroma at Løeflaten. Ten buds from each shoot were dissected under a stereobinocular microscope at 25x magnification and the number of overwintering mites were graded into the following density classes: 0, 1–10, 11–50, and >50 mites per bud. Sampling of summer populations

Half of the Kvitavoll orchard (about 18 trees from each of the 12 rows) and ten trees from each of eight rows of trees at Løeflaten were sampled. Both orchards were completely unsprayed in the years 1988 and 1989. Thirty mature leaves from the shoots and rosettes (1–3 leaves from each tree) were collected from each row of apple trees. Motile P. ulmi and phytoseiids were collected by washing the leaves, and A. schlechtendali was collected by using a mite brushing machine (Henderson and McBurnie 1943). Leaves were collected separately for each method. Hossain (1992) describes both washing and brushing methods in greater detail. For identification, all phytoseiids were extracted from the alcohol samples and mounted in lactic acid. Sampling of mites was conducted from the middle of June to middle of August. Statistical analysis

The standard error (SE) and one-way analysis of variance (ANOVA) were calculated for all samples except for the overwintering population of P. ulmi and the phytoseiids. Due to the sampling procedure used in this study for P. ulmi, calculation of SE and ANOVA was not possible. The densities of phytoseiids were very low and for this reason no further statistical analysis was done.

Figure 1

Distribution of oviposition sites occupied by different numbers of P. ulmi winter eggs at Kvitavoll.

RESULTS Overwintering of P. ulmi

There was little difference in the number of potential oviposition sites occupied by eggs of P. ulmi on different apple cultivars at Kvitavoll during the winter 1988/89 (Fig. 1), except that on Aroma, only 5% of potential oviposition sites lacked eggs compared with about 11% and 13% on Summerred and Gravenstein respectively (Fig. 1). During the winter 1989/90, only small numbers of overwintering eggs were observed. About 85%, 42% and 33% of the potential oviposition sites on Aroma, Summerred and Gravenstein respectively, were without eggs. No oviposition sites on Aroma at Kvitavoll contained >50 eggs (Fig. 1). A few oviposition sites had a higher number (>100) of egg on Summerred but none had >100

301

Mofakhar S. Hossain et al.

Figure 2

Distribution of oviposition sites occupied by different numbers of P. ulmi winter eggs on Aroma at Kvitavoll and Løeflaten.

on Gravenstein (Fig. 1). Both in 1988/89 and 1989/90, a striking similarity in distribution of overwintering eggs of P. ulmi was observed on Aroma at both localities (Fig. 2). Overwintering of A. schlechtendali

During the winter periods 1988/89 and 1989/90, there were significant differences in the number of overwintering A. schlechtendali per shoot on the three cultivars at Kvitavoll. Significant differences among the three cultivars were observed in the density class- 1–10 and >50 in 1988/89 (P50 in 1989/90 (P