Soft Scale Insects their Biology, Natural Enemies and Control 0444893032, 9780444893031, 9780080541341

Table of contents :
Content:
Preface
Pages v-xi
Yair Ben-Dov, Chris J. Hodgson

Contributors to Volume 7A
Pages xxiii-xxiv

1.1.1 Diagnosis Original Research Article
Pages 3-4
Yair Ben-Dov

1.1.2.1 The adult female Original Research Article
Pages 5-21
Daniéle Matile-Ferrero

1.1.2.2 The adult male Original Research Article
Pages 23-30
Jan H. Giliomee

1.1.2.3 The immature stages Original Research Article
Pages 31-48
Michael L. Williams

1.1.2.4 The male test Original Research Article
Pages 49-54
Gary L. Miller, Michael L. Williams

1.1.2.5 Chemistry of the test cover Original Research Article
Pages 55-72
Yoshio Tamaki

1.1.2.6 Internal anatomy of the Adult Female Original Research Article
Pages 73-90
ImrÉ Foldi

1.1.2.7 Ultrastructure of integumentary glands Original Research Article
Pages 91-109
Imré Foldi

1.1.3.1 Taxonomic characters — adult female Original Research Article
Pages 111-137
Chris J. Hodgson

1.1.3.2 Taxonomic characters — adult male Original Research Article
Pages 139-142
Jan H. Giliomee

1.1.3.3 Taxonomic characters — nymphs Original Research Article
Pages 143-156
Michael L. Williams, Greg S. Hodges

1.1.3.4. Classification of the Coccidae and related Coccoid families Original Research Article
Pages 157-201
Chris J. Hodgson

1.1.3.5 Intraspecific variation of taxonomic characters Original Research Article
Pages 203-212
Evelyna M. Danzig

1.1.3.6 Zoogeographical considerations and status of knowledge of the family Original Research Article
Pages 213-228
Ferenc Kozár, Yair Ben-Dov

1.1.3.7 Phylogeny Original Research Article
Pages 229-250
Douglass R. Miller, Chris J. Hodgson

1.2.1.1 General life history Original Research Article
Pages 251-256
Salvatore Marotta

1.2.1.2 Embryonic development; oviparity and viviparity Original Research Article
Pages 257-260
Ermenegildo Tremblay

1.2.1.3 Endosymbionts Original Research Article
Pages 261-267
Ermenegildo Tremblay

1.2.2.1 Morphology and anatomy of honeydew eliminating organs Original Research Article
Pages 269-274
Chris P. Malumphy

1.2.2.2 Scooty moulds Original Research Article
Pages 275-290
Richard K. Mibey

1.2.3.1 Scale insect honeydew as forage for honey production Original Research Article
Pages 291-302
Hartwig Kunkel

1.2.3.2 The pela wax scale and commercial wax production Original Research Article
Pages 303-321
Ting-Kui Qin

1.3.1 Effects on host plant Original Research Article
Pages 323-336
John A. Vranjic

1.3.2 Gall formation Original Research Article
Pages 337-338
John W. Beardsley

1.3.3 Crawler behaviour and dispersal Original Research Article
Pages 339-342
David J. Greathead

1.3.4. Seasonal history; diapause Original Research Article
Pages 343-350
Salvatore Marotta, Antonio Tranfaglia

1.3.5 Relationships with ants Original Research Article
Pages 351-373
Penny J. Gullan

1.3.6 Encapsulation of parasitoids Original Research Article
Pages 375-387
Daniel Blumberg

1.4.1 Collecting and mounting Original Research Article
Pages 389-395
Yair Ben-Dov, Chris J. Hodgson

1.4.2 Laboratory and mass rearing Original Research Article
Pages 397-419
Mike Rose, Steve Stauffer

General Index
Pages 421-439

Index to Coccoidea Taxa
Pages 441-447

Index to Names of Parasitoids, Predators and Pathogens
Page 449

Index to Plant Names
Pages 451-452

Citation preview

World Crop Pests, 7A

SOFT SCALE INSECTS T H E I R BIOLOGY, NATURAL ENEMIES AND C O N T R O L

World Crop Pests Editor-in-Chief M.W. Sabelis University of Amsterdam Institute of Systematics and Population Biology Section Population Biology Kruislaan 320 1098 SM Amsterdam, The Netherlands

Volumes in the Series

1. Spider Mites. Their Biology, Natural Enemies and Control Edited by W. Helle and M.W. Sabelis A. ISBN 0-444-42372-9 B. ISBN 0-444-42374-5 2. Aphids. Their Biology, Natural Enemies and Control Edited by A.K. Minks and P. Harrewijn A. 1987 ISBN 0-444-42630-2 B. 1988 ISBN 0-444-42798-8 C. 1989 ISBN 0-444-42799-6 3. Fruit Flies. Their Biology, Natural Enemies and Control Edited by A.S. Robinson and G. Hooper A. ISBN 0-444-42763-5 B. ISBN 0-444-42750-3 4. Armored Scale Insects. Their Biology, Natural Enemies and Control Edited by D. Rosen A. ISBN 0-444-42854-2 B. ISBN 0-444-42902-6 5. Tortricid Pests. Their Biology, Natural Enemies and Control Edited by L.P.S. van der Geest and H.H. Evenhuis ISBN 0-444-88000-3 6. Eriophyoid Mites. Their Biology, Natural Enemies and Control Edited by E.E. Lindquist, M.W. Sabelis and J. Bruin ISBN 0-444-88628-1 7. Soft Scale Insects. Their Biology, Natural Enemies and Control Edited by Y. Ben-Dov and C.J. Hodgson A. ISBN 0-444-89303-2 B. ISBN 0-444-82843-5

W o r l d Crop Pests, 7A

SOFT SCALE INSECTS T H E I R BIOLOGY, NATURAL ENEMIE S AND CONTROL V o l u m e 7A

Edited by

YAIR BEN-DOV

Department of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel CHRIS J. HODGSON

Department of Biological Sciences, Wye College, University of London, Wye, Ashford, Kent, UK

1997 ELSEVIER Amsterdam

- Lausanne - New York-

Oxford - Shannon - Singapore - Tokyo

ELSEVIER SCIENCE B.V. Sara Burgerhartstraat 25 P.O. Box 211, 1000 AE Amsterdam, The Netherlands

ISBN: 0-444-89303-2 91997 Elsevier Science B.V. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior written permission of the publisher, Elsevier Science B.V., Copyright & Permissions Department, P.O. Box 521, 1000 AM Amsterdam, The Netherlands. Special regulations for readers in the USA. This publication has been registered with the Copyright Clearance Center Inc. (CCC), 222 Rosewood Drive Danvers, MA 01923. Information can be obtained from the CCC about conditions under which photocopies of parts of this publication may be made in the USA. All other copyright questions, including photocopying outside of the USA, should be referred to the copyright owner, Elsevier Science B.V., unless otherwise specified. No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. This book is printed on acid-free paper. Printed in The Netherlands

Preface Even four or five decades ago, entomologists embarking on a study on soft scale insects would have encountered a scarcity of general text books or comprehensive treatese of the family, as a starting point for their research. At this time, the available knowledge and data were either scattered among numerous articles or regional monographs or were in obsolete books such as those of M.E. Fernald (1903) A Catalogue ofthe Coccidae ofthe Worm and A.D. MacGillivray (1921) The Coccidae. Since then, the availability and comprehensiveness of data on soft scale insects has been greatly increased by a number of valuable publications, including bibliographies covering all the Coccoidea, such as those of Morrison and Renk (1957), Morrison and Morrison (1965), Russell et al. (1974) and Kosztarab and Kosztarab (1988), while several regional monographs have also become available, such as those for the former USSR (Borchsenius, 1957); Central Europe (Kosztarab and Kozrr, 1988); Tropical South Pacific (Williams and Watson, 1990); Florida (Hamon and Williams, 1984) and California (Gill, 1988). The present volumes are intended to be a further step towards providing comprehensive information on soft scale insects. Together with the recently-published monographs, Ben-Dov (1993) A systematic Catalogue of the Soft Scale Insects of the Worm and Hodgson (1994) The Scale Insect Family Coccidae: an Identification Manual to Genera, it is hoped that these volumes will cover almost the entire spectrum of the knowledge on the soft scale insect family, Coccidae. For technical reasons this work has been published in two Volumes, Volumes 7A (comprising Sections 1.1.1 to 1.4.2)and Volume 7B (comprising Sections 2.1 to 3.3.18). This needs to be borne in mind when looking up cross references. In these volumes we have followed the pattern of previous books in the Elsevier' series of 'Worm Crop Pests' and so the information is divided into three parts: Part 1. The So~ Scale Insects presents a comprehensive account of the morphology, systematics, phylogeny, biology, physiology, ecology and techniques for their scientific study. The majority of soft scale species are pests of agricultural crops, although several species are ranked as beneficial insects, thus this aspect is also treated here. Part 2. The Natural Enemies covers the pathogens, predators and parasitoids. Part 3. Damage and Control opens with an account on the major soft scale pests of agricultural crops in the world. Because of the hazardous environmental effects of synthetic pesticides, these have not been treated here but a Section on Insect Development and Reproduction Disrupters is included. This Part concludes with a series of eighteen Sections on the coccid pests of the major crops in the world. Many of the contributing authors to these volumes have also reviewed various sections of the book and we are extremely grateful for their help. We are also very grateful to other colleagues who kindly consented and reviewed sections at our request, these are:

vi

Prefa c e

Dr. Israel Ben-Zeev (Ministry of Agriculture, Bet Dagan, Israel); Dr. Ezra Dunkelblum (The Volcani Center, Bet Dagan, Israel); Dr. Isaac lshaaya (The Volcani Center, Bet Dagan, Israel); Dr. Robert Minckley (Department of Entomology, Auburn University, Alabama, USA); Dr. John S. Noyes (The Natural History Museum, London, England); Dr. James Pakaluk (Systematic Entomology Laboratory, USDA, Washington, D.C., USA); Dr. Andrew Polaczek (International Institute of Entomology, London); Dr. Michael Schauff(Systematic Entomology Laboratory, USDA, Washington, D.C., USA); Dr. Zvi Solel (The Volcani Center, Bet Dagan, Israel); Dr. Gillian W. Watson (International Institute of Entomology, London) and Dr. Douglas J. Williams (International Institute of Entomology, London, England). We are extremely grateful to the following for permission to use their photographs on the covers and on pages vii-xi: Alfredo D'Ascoli, Facultad de Agronomia, Universidad Central de Venezuela (through Michael Kosztarab, Virginia Polytechnic Institute, Blacksburg, Virginia) (B, C); T. Eisner (through Michael Kosztarab) (A); Avas Hamon, Florida Department of Agriculture and Consumer Services, Gainesville, Florida (cover: centre and fight, & D, E, J, L); Rosa Henderson, Landcare Research, Auckland, New Zealand (P, Q, R, S, T, U, V, W, X, Y, Z, AE); Birgit E. Rhode, Landcare Research, Auckland, New Zealand (F, G, H); A.C. Stewart, The Australian National University, Canberra, Australia (I); S. Wadlington, Department of Plant Industry, Gainesville, Florida (through Avas Hamon) (cover: left, and K), and J. Windsor, Department of Plant Industry, Gainesville, Florida (through Avas Hamon) (M). Special thanks are due to the British Council for a grant towards travel expenses for the final editing of these volumes. Thanks are due to our colleague Mme. Dani/~le Matile-Ferrero (Musrum National d'Histoire Naturelle, Paris) who kindly checked and corrected the spelling of most of the references in French, but any errors still present are our responsibility. We are grateful to our Institutes for the time that we have been allowed to give to this project. CH would particularly like to thank Professor Dennis Baker for allowing free access to the Departmental facilities and Dr Mike Copland, Mrs Sue Briant and Mrs Margaret Critchley for their help in various ways. Lastly, we would like to thank our respective wives, Yehudith Ben-Dov and Charlotte Hodgson, for their patience, support and understanding. We hope you will find this book helpful.

Yair Ben-Dov

Chris J. Hodgson

Cover photographs. Left: Coccus viridis (Green) (Coccinae: Coccini), dorsal view, adult female. Flat and pale green in life. Note small, black simple eyes at anterior (pointed) end, black U-shaped dotted line on dorsum (marking position of alimentary canal) and the two pale radiating lines on right side caused by the white wax in the stigmatic grooves beneath venter. Middle: Inglisia vitrea Cockerell (Cardiococcinae), dorsal view, adult female. Reddish-brown in life. Note glassy test, in two halves separated by a distinct longitudinal suture; marginal setae and white wax in stigmatic grooves clearly visible. Right: Ceroplastes dugesii Lichtenstein (Ceroplastinae), dorso-lateral view, adult female. Note thick test composed mainly of whitish "wet" wax, but with small areas of whiter "dry" wax medially on dorsum and associated with each stigmatic area; anal plates hidden on right side of plate.

Photographs

vii

A: adult female Toumeyella lignumvitae Williams (Myzolecaniinae) attended by two ants (Camponotusfloridanus). The ants collect the honeydew eliminated by the scale insect (thus reducing damage by sooty moulds) but the presence of the ants will deter parasitoids and predators from attacking the scales, thus disrupting their biological control. B: a mass of wax tests of adult female Ceroplastes caesalpiniae Reyne (Ceroplastinae). Numerous individuals are present (see Plate C) and their fused tests form a wax 'candle' similar to that formed by Gascardia madagascariensis Targioni Tozzetti. Each dark indentation in the wax shows the position of a pair of anal plates, which emerge through the "wet" wax to allow the elimination of honeydew, while the rays of very white wax are composed of spiracular "dry" wax secreted by the spiracular disc-pores; these rays extend from the spiracles to the exterior to allow diffusion of respiratory gases through the "wet" wax.

oo~

VIII

SEM micrographs and photographs

C: section through the mass of wax tests of Ceroplastcs caesalpiniae Reyne (Ceroplastinae), showing a predatory pyralid caterpillar which has been feeding on the scale insects. Note the rather elongate, adult female Ceroplastes within the mass of "wet" wax, the very white rays of spiracular "dry" wax arising from the spiracles and extending to the exterior to allow diffusion of respiratory gases through the wet wax; also a pair of anal platcs ~merging from the mass of wax. D: a young tree (probably Podocarpus sp.) heavily infested with Ceroplastes ceriferus (Fabricius) (Ceroplastinae). Plants with such a heavy infestation can become black with sooty moulds and may show die-back. E: Ceroplastes dugesii Lichtenstein (Ceroplastinae) on Coccoloba uvifera, showing the smaller tests of the 2nd- and 3rd-instar nymphs as well as those of the adult female. For other details, see caption to cover photo of C. dugesii.

Photographs

ix

F: SEM micrograph of the glassy wax test of a 2nd-instar male Ctenochiton piperis Maskell (Cardiococcinae), showing the distribution of the wax plates and sutures and also the marginal fringe of flat wax plates, probably secreted by the marginal setae. The anal plates would emerge through the small hole to the right of the test. G, H: as F above, but showing details of the structure of the test. It is clear that each plate consists of numerous layers of wax and that the earliest (outside) layers were much smaller than the later (inner) layers, suggesting that the area of each plate expands as the insect beneath grows. I: scanning EM of Torarchus endocanthium Gullan & Stewart (Myzolecaniinae), an unusual soft scale known only from inside ant domatia (hollow, swollen stems) in Canthium sp., in which it lives as a trophobiont, attended by ants belonging to the genus Podomyrma. The ants obtain their nutrition largely from honeydew from the coccid, while the scale insects may be dependent on the ants for the removal of the honeydew and also possibly for dispersal. J: Inglisia vitrea Cockerell (Cardiococcinae), with exit holes through the glassy test made by emerging hymenopterous parasitoids. K: a shelter constructed by ants to protect honeydew producing coccoids from parasitoids and predators; they may also produce an improved environment. In coccoid colonies composed of more than one species, these shelters may be built only over one species, possibly indicating a closer relationship between the ants and the protected species than with the unprotected species.

SEM micrographs and photographs

L: adult female Milviscutulus mangiferae (Green) (Coccinae: Pulvinariini). Flat and yellowish-green in life; cosmopolitan, primarily a pest of mangoes. Note pyriform shape of body, small black eyes-pots at anterior (pointed) end, white lines marking stigmatic areas, deep anal cleft with elongate anal plates placed almost centrally. M: adult female Toumeyella liriodendri (Gmelin) 0Vlyzolecaniinae). Highly convex, colour varying from greyish-green to pinky-orange to brown or black. A pest of magnolias and the tuliptree, as well as other ornamentals. N: adult female and late nymphs of Saissetia coffeae (Walker) (Coccinae: Saissetiini). Adult females hemispherical, oval, convex when mature, with a smooth dorsum; H-shaped ridges most pronounced in nymphs and young adults; pale to dark brown but may be pinkish as nymphs. Major cosmopolitan pest. Note short, white stigmatic wax projections at each stigmatic cleft. O: adult female Protopulvinaria pyriformis (Cockerell). An important cosmopolitan pest on a wide range of plants. Flat, light greenish-brown to brown, slightly darker along margins, with a narrow marginal, white ovisac. Characters otherwise similar to L. Other members of the Pulvinariini can have a more pronounced ovisac, up to many times as long as the body. P: adult female of the Ctenochiton viridis Maskell complex (Cardiococcinae). Flat and bright green in life. Note pyriform shape and reticulate pattern over dorsum; also numerous crawlers. Q: two adult females of an undescribed species of Ctenochiton. Rather convex and pale green with reticulate pattern in dark green. Note several crawlers. R: adult female Ctenochiton viridis Maskell. Note reticulate pattern of markings on thin glassy test and absence of distinct eyespots. Also note lst-instar crawler. S: adult male coccoid. Note single pair of rather broad wings with only two veins, a pair of long white tail-streamers, body divided into distinct head, thorax and abdomen, and ten-segmented antennae.

Photograph~

xi

T: two 2nd-instar male tests of an undescribed species of Ctenochiton (Cardiococcinae) off Vitex lucens from New Zealand. The glassy tests have a marginal fringe of fiat plates of similar glassy wax. The white U-shaped line at the posterior (right-hand) end of each test marks the juncture between the main test and the posterior plate, which lifts up when the adult male emerges baclc~,ards from the test. The hole through which the anal plates of the 2nd-instar male emerge can be seen in the centre of the posterior plate. The left-hand test contains a prepupa and the fight-hand test an adult male, whose tail-streamers can be seen emerging posteriorly. U: 2nd-instar male test of a Ctenochiton sp. on Hedycarya arborea containing a pupa showing similar characters to T. V: test of an undescribed species of Ctenochiton, showing the glassy plates and sutures; the anal plates would emerge through the hole at the posterior (fight-hand) end. W: test of an adult female Inglisia ornata Maskell (Cardiococcinae) on Vitex lucens. Note the distinctive shape, the shape of the plates and sutures and the marginal fringe of wax plates. X, Y and Z: tests of adult females of two undescribed species of Inglisia and of Inglisia leptospermi Maskell respectively, all on Kunzea ericoides. Compare with that of I. ornata. Note the variation in test shape, etc. /E: dorsal view of an adult female of a n. gen., n. sp. off Blechnum f r a s e r / f r o m New Zealand. It is covered in a clear waxy test, divided into a series of plates by narrow sutures. Also visible are short, white protrusions of stigmatic wax from each stigmatic area. Note that the female has withdrawn from the posterior (fight-hand) end of the test in preparation for oviposition (and so withdrawn her anal plates - presumably she stops feeding (and therefore the elimination of honeydew) when she starts ovipositing).

This Page Intentionally Left Blank

xiii

Contents

Contents of Volume 7A Preface

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

v

P h o t o g r a p h s and S E M m i c r o g r a p h s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C o n t r i b u t o r s to this V o l u m e

PART 1 CHAPTER 1.1.1

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

vii xxiii

THE SOFT SCALE INSECTS 1.1 M O R P H O L O G Y ,

SYSTEMATICS AND PHYLOGENY

D i a g n o s i s , b y Y. B e n - D o v

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

3

1.1.2 Morphology 1.1.2.1

T h e A d u l t F e m a l e , b y D. M a l i l e - F e r r e r o . . . . . . . . . . . . . . . . . . . . . . . . . . . .

5

Introduction

5

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

G e n e r a l structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Margin

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

V e n t r a l surface

10

Setae

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

13

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

13

Ducts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

13

Anal plates Anal ring

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

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

14 15 15

Setae

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

15 16

Pores

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

18

Setae and g l a n d u l a r structures

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

Ducts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

19

G l a n d u l a r tubercles

19

References

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

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

20

The Adult Male, by J . H . Giliomee . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

23

Introduction

23

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

General appearance Head

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

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

Thorax

24

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

Mesothorax

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

Metathorax

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

Wings Legs

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

Chaetotaxy

24 25 25 28

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

Abdomen

23 23

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

Prothorax

1.1.2.3

8

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

Pores

D o r s a l surface

1.1.2.2

7

28

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

28 29

O t h e r cuticular structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

29

References ................................................

30

T h e I m m a t u r e S t a g e s , by M . L . W i l l i a m s ........................... Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

31 31

D e v e l o p m e n t in soft scale insects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

31

G e n e r a l characteristics

31

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

First-instar male and female General appearance

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

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

Characteristics o f slide-mounted specimens

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

S e c o n d - i n s t a r female and second-instar male . . . . . . . . . . . . . . . . . . . . . . . . . . .

32 32 32 35

xiv

Contents General appearance

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

Characteristics of slide-mounted specimens Third-instar female

39

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

41

F o u r t h instar m a l e (pupa) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References ................................................

43 46

The M a l e T e s t , by G . L . M i l l e r a n d M . L . W i l l i a m s

49

Introduction

1.1.2.5

37

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

T h i r d instar m a l e ( p r e p u p a )

1.1.2.4

36

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

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

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

49

A p p e a r a n c e o f the m a l e test . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

49

References ................................................

54

C h e m i s t r y of the T e s t C o v e r , by Y. T a m a k i ......................... Introduction ...............................................

55 55

R e l a t i v e w e i g h t o f the test or c o v e r . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C o m p o s i t i o n o f the w a x y materials in the c o v e r ........................

55 56

1. W a x e s

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

2. H y d r o c a r b o n s

56

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

58

3. R e s i n o u s materials or t e r p e n o i d s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. P i g m e n t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

58 62

5. O t h e r c o m p o n e n t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C o m p o s i t i o n o f b o d y lipids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

63 63

C o m p o s i t i o n o f the a q u e o u s materials in the test c o v e r s . . . . . . . . . . . . . . . . . . . .

66

1. T h e t w o kinds o f " h o n e y d e w " in scale insects . . . . . . . . . . . . . . . . . . . . . . .

66

2. A m i n o acid c o m p o s i t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. C a r b o h y d r a t e c o m p o s i t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

66 66

4. Possible function o f "interior h o n e y d e w " . . . . . . . . . . . . . . . . . . . . . . . . . . M o d e o f secretion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

67 67

1. C h a n g e s in the c o m p o s i t i o n o f the c o v e r d u r i n g g r o w t h . . . . . . . . . . . . . . . . . 2. S e c r e t i o n and c o n s t r u c t i o n o f the c o v e r . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion ...............................................

67 68 69

Acknowledgements

69

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

References ................................................

1.1.2.6

1.1.2.7

69

I n t e r n a l A n a t o m y of the A d u l t F e m a l e , by I. F o i d i Introduction ...............................................

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

73 73

D i g e s t i v e s y s t e m and associated structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . Head capsule . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

73 74

M o u t h p a r t s and f e e d i n g strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stylets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

74 75

T e n t o r i u m and stylet levers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Salivary pump ............................................. Filter c h a m b e r . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Respiratory system ........................................... Excretory system ............................................ Nervous system ............................................

76 77 78 80 83 83

Female reproductive system ..................................... Male reproductive system ......................................

84 87

Anal apparatus . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References ................................................

87 89

Uitrastructure Introduction

of Integumentary

G l a n d s , by I. F o l d i

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

91

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

91

T h e i m p o r t a n c e o f w a x g l a n d structure in the classification o f the C o c c i d a e I m p o r t a n c e o f the cuticular structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D e s c r i p t i o n and t e r m i n o l o g y ................................... a. Pores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . b. D u c t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . c. D u c t u l e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C u t i c u l a r structures associated with the w a x g l a n d s i. S i m p l e p o r e s

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

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

.......

93 93 93 93 97 97 97 97

ii. D o r s a l m i c r o d u c t u l e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

98

iii. S p i r a c u l a r d i s c - p o r e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . iv. M u l t i l o c u l a r d i s c - p o r e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

99 99

v. V e n t r a l m i c r o d u c t s

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

99

vi. P r e o p e r c u l a r p o r e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

99

vii. T u b u l a r ducts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

99

Contents

XV

viii. D o r s a l tubercles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix. C r i b r i f o r m plates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

99 99

W a x g l a n d s associated with the spiracles and spiracular f u r r o w s 1. T h e s p i r a c u l a r setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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

2. T h e 5-1ocular w a x g l a n d s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . i. C u t i c u l a r structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

100 100

ii. G e n e r a l structure and cytological c h a r a c t e r s . . . . . . . . . . . . . . . . . . . . . . iii. M i c r o m o r p h o l o g y and function o f the secretion . . . . . . . . . . . . . . . . . . . . V e n t r a l w a x g l a n d s associated with sites o f r e p r o d u c t i o n . . . . . . . . . . . . . . . . . . 1. T h e t u b u l a r duct w a x g l a n d s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . i. C u t i c u l a r structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ii. G e n e r a l o r g a n i s a t i o n and cytological characteristics . . . . . . . . . . . . . . . . . . iii. M i c r o m o r p h o l o g y and function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. M u l t i l o c u l a r disc-pore g l a n d s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Dorsal microductule glands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . i. C u t i c u l a r structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

104 104 105 105

ii. G e n e r a l o r g a n i s a t i o n and cytological characteristics . . . . . . . . . . . . . . . . . . iii. M i c r o m o r p h o l o g y and function o f the secretion . . . . . . . . . . . . . . . . . . . . ...............................

105 105 107

Ceroplastes-type g l a n d s D o r s a l tubercles

100 103 103 103 103 103 104 104

W a x g l a n d s associated with h o n e y d e w excretion . . . . . . . . . . . . . . . . . . . . . . . W a x g l a n d s associated with defence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

T h e ventral m i c r o d u c t w a x glands

99 100

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

107 107

I n t e g u m e n t a r y g l a n d s o f u n k n o w n function . . . . . . . . . . . . . . . . . . . . . . . . . . Preopercular glands ........................................ D o r s a l simple pore g l a n d s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References ...............................................

108 108 108 109

1.1.3. Systematics 1.1.3.1

T a x o n o m i c C h a r a c t e r s - A d u l t F e m a l e , by C . J H o d g s o n Introduction ..............................................

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

111 11 1

External a p p e a r a n c e o f u n m o u n t e d insects . . . . . . . . . . . . . . . . . . . . . . . . . . . T e s t and ovisac . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I 11 111

Size, shape and c o l o u r . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T h e m o u n t e d insect; structures on the d o r s u m . . . . . . . . . . . . . . . . . . . . . . . . . Derm ................................................. Segmentation ............................................ Dorsal setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D o r s a l pores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . i. Dorsal m i c r o d u c t u l e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ii. Simple pores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

114 115 115

iii.Preopercular pores

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

iv. M u l t i l o c u l a r disc-pores

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

116 118 118 118 118 120 120

v. F i g u r e - o f - e i g h t p o r e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vi. F l o w e r - s h a p e d p o r e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

120 120

vii. Ceroplastes-type p o r e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . viii. Bilocular pores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

120

121

ix. O t h e r pore types . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C r i b r i f o r m plates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

121 121

M i c r o t u b u l a r ducts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T u b u l a r ducts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D o r s a l tubercles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pocket-like sclerotisations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Anal plates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A n o - g e n i t a l fold . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

123 123 124 124 1225

Anal ring

121

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

12:5

S t r u c t u r e s associated with the m a r g i n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Margin ................................................ Stigmatic clefts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M a r g i n a l setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stigmatic spines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Eyespots ...............................................

126

S t r u c t u r e s on the v e n t e r

128

Derm

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

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

D e r m a l spinules Segmentation

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

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

126 126 126 127 127 128 128 128

Contents

xvi

Ventral pores

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

128

i. D i s c - p o r e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

128

a. P r e g e n i t a l d i s c - p o r e s

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

129

b. S p i r a c u l a r d i s c - p o r e s

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

129

ii. V e n t r a l m i c r o d u c t s

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

130

iii. P r e - a n t e n n a l p o r e s

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

130

iv. O t h e r v e n t r a l p o r e s ..................................... Ventral tubular ducts ....................................... Ventral setae Spiracles Legs

131 131

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

131

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

132

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

Antennae

132

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

Mouthparts

135

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

135

Vulva .................................................

1.1.3.2

References

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

Taxonomic

Characters

Introduction Head

- Adult Male, by J.H. Giliomee

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

139

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

139

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

Thorax

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

Wings

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

Legs

139 140 140

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

Abdomen

140

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

Dermal structures

1.1.3.3

136 136

References

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

Taxonomic

Characters

Introduction Taxonomic

141

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

- Nymphs,

141 142

by M.L.

Williams and G.S. Hodges

.......

.............................................. characters of first-instar nymphs

Dorsal structures

143

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

143

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

143

Dorsal setae

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

143

Dorsal pores

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

143

Dorsal tubular ducts

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

Dorsal microductules Anal plates Anal ring

145

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

145

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

145

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

146

Marginal structures ......................................... Eyespots ..............................................

147 147

M a r g i n a l setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

147

S p i r a c u l a r ( s t i g m a t i c ) setae

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

148

S p i r a c u l a r ( s t i g m a t i c ) clefts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

149

Ventral structures

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

149

Ventral setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

149

Ventral pores

149

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

Ventral microducts

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

149

Ventral tubular ducts .......................................

149

Antennae

149

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

Mouthparts Spiracles Legs

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

149

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

149

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

Conclusions

151

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

151

References ............................................... 1.1.3.4

143

Classification of the Coccidae and Related Coccoid Families, by C.J. Introduction

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

A c l e r d i d a e - Flat G r a s s S c a l e s

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

A s t e r o l e c a n i i d a e - Pit S c a l e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C e r o c o c c i d a e - O r n a t e Pit S c a l e s

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

Cryptococcidae - Bark-crevice Scales Dactylopiidae - Cochineal Scales

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

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

Eriococcidae - Felted Scales .................................... Kermesidae - Gall-like Scales

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

L e c a n o d i a s p i d i d a e - O r n a t e Pit S c a l e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Micrococcidae

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

T a c h a r d i i d a e - Lac i n s e c t s C o c c i d a e - Soft S c a l e s

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

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

C l a s s i f i c a t i o n o f the C o c c i d a e

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

156 Hodgson

. . 157 157 158

167 168 170

170 173 176 178 181 183 185 185

Contents

xvii

1.1.3.5

Cardiococcinae ............................................ Ceroplastinae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cissococcinae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Coccinae ................................................ Coccini . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Paralecaniini . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pulvinariini . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Saissetiini . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cyphococcinae ............................................ Eulecaniinae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Eriopeltinae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Filippiinae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Myzolecaniinae ............................................ Pseudopulvinariinae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

187 187 190 190 190 190 193 193 193 193 196 196 196 196

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

198

I n t r a s p e c i f i c V a r i a t i o n of Taxonomic C h a r a c t e r s , by E . M . D a n z i g . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

203 203

Intraspecific variability in populations o f the E u r o p e a n fruit scale Parthenolecanium corni (Bouch~) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Variability o f morphological characters . . . . . . . . . . . . . . . . . . . . . . . . . . . . Variability o f biological characters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Reproduction ...........................................

203 203 204 204

Seasonal d e v e l o p m e n t . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Intraspecific differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Intraspecific variability in populations o f the cottony vine scale Pulvinaria vitis (Linnaeus) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . lntraspecific variability in other coccid species . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1.1.3.6

1.1.3.7

204 205 207 207 210

Zoogeographical Considerations and Status of Knowledge of the Family, by F . K o z d r a n d Y. B e n - D o v . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Z o o g e o g r a p h y o f the Coccidae o f the World . . . . . . . . . . . . . . . . . . . . . . . . . Characterization o f the Z o o g e o g r a p h i c a l Regions . . . . . . . . . . . . . . . . . . . . . . . a. Palaearctic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . b. Nearctic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . c. Neotropics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . d. Ethiopian . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . e. Oriental . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . f. Australian . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . g. Pacific . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . h. N e w Zealand . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . i. M a d a g a s i a n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . j. Austro-Oriental . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

213 213 215 218 218 218 220 222 222 222 222 222 222 223

C o n n e c t i o n s b e t w e e n regions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Centres o f diversification o f large cosmopolitan genera . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

223 225 227

P h y l o g e n y , by D . R . M i l l e r a n d C . J . H o d g s o n ....................... Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methodology ............................................. Results and Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements ......................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A p p e n d i x 1 . 1 . 3 . 7 , A : sources o f characters and character-states . . . . . . . . . . . . . . A p p e n d i x 1 . 1 . 3 . 7 , B : list o f characters and character-states used . . . . . . . . . . . . . A p p e n d i x 1 . 1 . 3 . 7 , C : character-state matrix . . . . . . . . . . . . . . . . . . . . . . . . . . A p p e n d i x 1 . 1 . 3 . 7 , D : character-state changes . . . . . . . . . . . . . . . . . . . . . . . . .

229 229 229 230 238 242 242 244 246 :248 250

Contents

XVIII

CHAPTER

1.2 B I O L O G Y

1.2.1 Biology 1.2.1.1

G e n e r a l Life H i s t o r y , by S. M a r o t t a . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . First-instar n y m p h or crawler . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Subsequent immature instars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Adult female . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Egg . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1.2.1.2

E m b r y o n i c D e v e l o p m e n t ; O v i p a r i t y a n d V i v i p a r i t y , by E. T r e m b l a y Embryonic development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Oviparity and viviparity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1.2.1.3

E n d o s y m b i o n t s , by E. T r e m b l a y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M o r p h o l o g y of the symbionts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The nature of the symbionts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Localization of symbionts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hereditary transmission of symbionts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Host regulation of symbiont growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The significance of symbiosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

251 251 251 252 254 255 255 ........

257 257 259 260 261 261 261 263 264 265 265 266 266

1.2.2 Honeydew 1.2.2.1

1.2.2.2

M o r p h o l o g y a n d A n a t o m y of H o n e y d e w E l i m i n a t i n g O r g a n s , by C . P . M a l u m g h y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Definition o f h o n e y d e w . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Harmful effects of h o n e y d e w . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Disposal of h o n e y d e w . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M o r p h o l o g y and anatomy of the anal apparatus of Coccidae . . . . . . . . . . . . . . . . Anal cleft . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Anal plates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Anal plate and associated setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ano-genital fold and associated setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Anal-tube . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Anal-ring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Elimination m e c h a n i s m of the anal apparatus of Coccidae . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

269 269 269 270 270 272 272 272 272 273 273 274 274

Sooty M o u l d s , by R . K . M i b e y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Taxonomy ............................................... Antennularielliaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Capnodiaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chaetothyriaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Euantennariaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Metacapnodiaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Occurrence and Distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Early Observations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Host Plant - Sooty Mould Interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Insect - Sooty Mould Interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Effects o f Sooty Mould on Host Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Glossary of the mycological terminology used in this Section . . . . . . . . . . . . . . .

275 275 275 276 276 277 277 278 278 279 279 280 284 285 285 285 289

Contents

xix

1.2.3

Soft S c a l e s as B e n e f i c i a l Insects

1.2.3.1

Scale Insect H o n e y d e w as F o r a g e for H o n e y Production, by H. K u n k e l . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Distribution and diversity of species visited by honey-bees . . . . . . . . . . . . . . . . . Regions where honey-bee is endemic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Areas where N o r w a y spruce is endemic . . . . . . . . . . . . . . . . . . . . . . . . . . . Southern Europe, especially Greece . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Regions w h e r e the honey-bee has been introduced . . . . . . . . . . . . . . . . . . . . . . T h e United States of America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T h e southern hemisphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . N e w Zealand . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . South America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Some aspects of the ecology of h o n e y d e w and honey-bees . . . . . . . . . . . . . . . . . T h e attractiveness of the h o n e y d e w . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A m o u n t s of h o n e y d e w . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Factors affecting the build-up of scale insect populations . . . . . . . . . . . . . . . . . . Effects of waterstress in the host plant on population growth . . . . . . . . . . . . . . Effects of changes in soil fertility on population growth of coccids . . . . . . . . . . . The role of apiculturists . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

291 291 291 291 291 293 294 294 295 295 295 295 296 296 297 297 297 298 299

1.2.3.2

T h e Pela W a x Scale a n d C o m m e r c i a l W a x Production, by T . K . Q i n . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . History and study of pela wax scale . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biology of pela w a x scale . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Geographical distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C o m m e r c i a l w a x production regions in China . . . . . . . . . . . . . . . . . . . . . . . . Life cycle of pela wax scale . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . General biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . i. egg laying and hatching . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ii. first-instar n y m p h . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . iii. second-instar n y m p h s and subsequent stages . . . . . . . . . . . . . . . . . . . . . . iv. overwintering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . v. sex ratio . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vi. host plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Natural enemies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . a. Natural enemies of Ericerus pela . . . . . . . . . . . . . . . . . . . . . . . . . . . . . b. Natural enemies of the host plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . W a x secretion and w a x glands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. W a x secretion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. N u m b e r and structure of the wax glands in the male . . . . . . . . . . . . . . . . . 3. W a x secretion periods in the second-instar male . . . . . . . . . . . . . . . . . . . . Production of pela w a x scale and its wax . . . . . . . . . . . . . . . . . . . . . . . . . . . . Seed production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . W a x production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Release of male n y m p h s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Post-release m a n a g e m e n t . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Harvesting w a x flower . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chemical and physical properties of the wax . . . . . . . . . . . . . . . . . . . . . . . . . Chemical characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Physical and chemical characteristics of refined wax . . . . . . . . . . . . . . . . . . . C o m m e r c i a l products of China wax . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Semifinished w a x . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Refined w a x . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Uses of China w a x . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Yield of China w a x . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . W a x production of species of Ceroplastes . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements ......................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

303 303 303 304 304 305 305 306 306 306 307 307 307 307 307 307 309 309 309 310 310 312 312 312 312 313 313 314 314 315 315 315 316 317 318

318 318 319 319

xx

Contents

C H A P T E R 1.3 1.3.1

1.3.2

ECOLOGY Effects on Host P l a n t , by J . A . V r a n j i c . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . H o w scale insects affect plant growth: direct effects . . . . . . . . . . . . . . . . . . . . . 1. Feeding damage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Resource removal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Galls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

323 323 323 323 324 325

H o w scale insects affect plant growth: indirect effects . . . . . . . . . . . . . . . . . . . 1. Contamination with h o n e y d e w and sooty moulds . . . . . . . . . . . . . . . . . . . . 2. Associations with plant pathogens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Impact on plant physiological processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Photosynthesis and gas exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Water relations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Nutrient content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Impact on plant growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Shoot growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Root growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Flower and fruit production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Architecture and allocation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Factors affecting plant responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Host plant condition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Insect population density . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Ant attendance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

325 325 326 326 326 328 328 328 328 329 330 330 331 331 332 333

S u m m a r y and recommendations for future research . . . . . . . . . . . . . . . . . . . . . Acknowledgements ......................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

333 334 334

G a l l F o r m a t i o n , by J . W . Beardsley . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

337 337 337 338

Cissococcus fulleri

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

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1.3.3

C r a w l e r B e h a v i o u r a n d Dispersal, by D . J . G r e a t h e a d Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C r a w l e r behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dispersal by air currents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1.3.4

S e a s o n a l H i s t o r y ; D i a p a u s e , by S. M a r o t t a a n d A. T r a n f a g l i a . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Voltinism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Diapause . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

343 343 343 347 348

1.3.5

R e l a t i o n s h i p s w i t h Ants, by P . J . G u U a n . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Benefits of ants to coccids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T h e effect of ant exclusion on coccids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Coccid protection and ant aggression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Benefits of coccids to ants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Coccids, ants and ant-plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S u m m a r y and suggestions for future research . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements ......................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

351 351 353 356 361 363 364 370 370 371

1.3.6

E n c a p s u l a t i o n of P a r a s i t o i d s , by D. B l u m b e r g . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Factors affecting encapsulation incidence by soft scale insects . . . . . . . . . . . . . . . T h e host insect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Effect of host age . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Effect of host strain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Effect of the host's physiological condition . . . . . . . . . . . . . . . . . . . . . . . . 4. Effect of superparasitism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Effect of the rearing temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T h e host plant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

375 375 377 377 377 379 381 382 382 383

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

339 339 340 340 341 342

Contents

xxi References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

384

C H A P T E R 1.4 T E C H N I Q U E S 1.4.1

Collecting a n d M o u n t i n g , by Y. Ben-Doe a n d C . J . H o d g s o n Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Collection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1.4.2

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

389 389 389

Preservation and storage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Wet preservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dry preservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Slide preparation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Procedure for preparation of permanent microscope slides . . . . . . . . . . . . . . . . Alternative methods and procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . R e m o u n t i n g old slides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . M o u n t i n g and staining of adult males . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

390 390 390 391 391 392 394 394 395

L a b o r a t o r y a n d M a s s R e a r i n g , by M . Rose a n d S. S t a u f f e r Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

397 397

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

Rearing methods and environmental conditions . . . . . . . . . . . . . . . . . . . . . . . .

Saissetia oleae (Olivier) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Coccus hesperidum L . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ceroplastes floridensis Comstock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Philephedra tuberculosa Nakahara and Gill . . . . . . . . . . . . . . . . . . . . . . . . . . Summary ............................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

399 406

410 413 415 416 416

General Index .......................................................

421

I n d e x to C o c c o i d e a T a x a . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

441

I n d e x to N a m e s of P a t h o g e n s , P r e d a t o r s a n d P a r a s i t o i d s . . . . . . . . . . . . . . . . . . . . . . . . . . .

449

I n d e x to N a m e s of P l a n t s

451

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

Contents of Volume 7B PART 2 THE NATURAL ENEMIES

Chapter 2.1 Chapter 2.2 Chapter 2.3 PART 3

Pathogens Predawrs Parasitoids

DAMAGE AND CONTROL

Chapter 3.1 Chapter 3.2 Chapter 3.3

Pest Status of Soft Scale Insects Control Coccid Pests of lmportant Crops

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xxiii

Contributors to Volume 7 A

JOHN W. BEARDSLEY Professor Emeritus, University of Hawaii, 1026 Oakdale Lane, Arcadia, California 91006, U.S.A. YAIR BEN-DOV Department of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan 50 250, Israel DANIEL BLUMBERG Department of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan 50 250, Israel EVELYNA M. DANZIG Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. St Petersburg 199034, Russia

1,

IMRI~ FOLDI Laboratoire d'Entomologie, Mus6um National d'Histoire Naturelle, 45 rue Buffon, 75005 Paris, France JAN H. GILIOMEE Department of Entomology and Nematology, University of Stellenbosch, 7600 Stellenbosch, South Africa PENNY J. GULLAN Department of Botany and Zoology, Australian National University, GPO Box 4, Canberra, ACT 2601, Australia GREG S. HODGES Department of Entomology, Auburn University, Auburn, Alabama 36830, U.S.A. CHRIS J. HODGSON Department of Biological Sciences, Wye College, University of London, Wye, Ashford, Kent, TN25 5AH, UK FERENC KOZAR Research Institute for Plant Protection, P.O. Box 102, Budapest H-1525, Hungary HARTWlG KUNKEL Institut tiir Angewandte Zoologic der Universit~t, An der Immenburg 1, D-5300 Bonn 1, Germany CHRISTOPHER P. MALUMPHY Central Science Laboratory, Ministry of Agriculture, Fisheries and Food, Sand Hutton, York, YO4 16Z, UK

rodv

Contributors

SALVATORE MAROTTA Universittt degli Studi della Basilicata, Dipartimento di Biologia Difesa e Biotecnologie Agro-Forestali, Via Nazario Sauro 85, 85100 Potenza, Italy DANII~LE MATILE-FERRERO Laboratoire d'Entomologie, Museum National d'Histoire Naturelle, 45 rue Buffon, 75005 Paris, France RICHARD K. MIBEY Department of Botany, University of Nairobi, Nairobi, Kenya

Chiromo,

P.O.

Box 30197,

DOUGLASS R. MILLER Systematic Entomology Laboratory, Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland 20705, U.S.A. GARY L. MILLER Systematic Entomology Laboratory, Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland 20705, U.S.A. TING-KUI QIN Systematics Group, Manna~i Whenua- Landcare Research, Private Bag 92170, Auckland, New Zealand. Formerly: Department of Botany and Zoology, Australian National University, GPO Box 4, Canberra, ACT 2601, Australia MIKE ROSE Biological Control/Entomology, 59717, U.S.A.

Montana State University, Bozeman, Montana

STEVE STAUFFER Biological Control Laboratories, Department of Entomology, Texas A&M University, College Station, Texas 77843-2475, U.S.A. YOSHIO TAMAKI Insect Science & Bioregulation, Tohoku University, Tsutsumidori-Amamiyamachi 1-1, Sendai, 981 Japan

Faculty of Agriculture,

ANTONIO TRANFAGLIA Universit~ degli Studi della Basilicata, Dipartimento di Biologia Difesa e Biotecnologie Agro-Forestali, Via Nazario Sauro 85, 85100 Potenza, Italy ERMENEGILDO TREMBLAY Dipartimento di Entomologia e Zoologia Agraria, Facolta di Agraria, Via UniversitY, 100, 80055 Portici, Italy JOHN A. VRANJIC The Cooperative Research Centre for Weed Management Systems, c/-CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia MICHAEL L. WILLIAMS Department of Entomology, Auburn University, Auburn, Alabama 36830, U.S.A.

PART 1

THE SOFT SCALE INSECTS

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Soft Scale Insects - Their Biology, Natural Enemies and Control

Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.

Chapter 1.1 Morphology, Systematics and Phylogeny 1.1.1 Diagnosis YAIR BEN-DOV

The soft scale insects (lnsecta: Homoptera: Coccoidea: Coccidae), which are n a m e d c o c h e n i l l e s c o c c i n e s (in F r e n c h ) , Schildlaus (in G e r m a n ) , ]71:37 ]71 r3~ ] :3 (in Hebrew), coccini (in Italian), r t: ~ t ~ff ~ r k (in Japanese), 3Io>~aom,rtTomcrt (in Russian) and coccidos (in Spanish) - constitute a family among the 21 families of scale insects, Coccoidea. While scale insects are generally classified as the superfamily Coccoidea, other taxonomists of the group rank the latter as the suborder Coccinea. Within the Coccoidea, the Coccidae are assembled among the 18 families of the advanced coccoids (also erroneously termed as the Neococcoidea). This group is distinguished from the Margaroid scale insects (also erroneously termed Archeococcoidea) mainly in that all instars possess only two pairs of thoracic spiracles, and that the adult male have only simple unicorneal eyes, while in the Margaroids there are also abdominal spiracles and the male has compound eyes (see Sections 1.1.3.1, 1.1.3.2). The Coccidae are placed among the lecanoid families of Coccoidea, showing great affinity with the Aclerdidae, Kermesidae and the Lecanodiaspididae (see Sections 1.1.3.4 and 1.1.3.7). The soft scales are plant-feeding insects which develop mainly on perennial, but occasionally on annual plants. Members of this family, about 1100 described species, are distributed in all zoogeographical regions extending to the north and south latitudes 60-65 o (see Section 1.1.3.6). The family, like other families of the Coccoidea, is characterized by a very distinct sexual dimorphism. The adult female is always neotenic and wingless, and exhibits complete fusion of the head, thorax and abdomen into a flattened or globular, sac-like body (see Section 1.1.2.1). The male is usually a winged insect, with a clear division of the body into head, thorax and abdomen; the latter bears a long, heavily sclerotized genital organ (see Section 1.1.2.2). Attributes of sexual dimorphism may be present also in the first and second instars, although the differences are observable only in slide-mounted specimens (see Section 1.1.2.3). The life cycle of the females contains two or three nymphal instars and the adult female. The male develops through two nymphal instars plus a prepupa and a pupa before emerging as the winged adult male. The dorsum of all stages is always covered by a soft, waxy covering, which varies considerably, in both texture and structure, between the various subfamilies. In species of the Coccinae it is very thin, whereas both the nymphs and adults of the Ceroplastinae (the wax scales) are covered by a voluminous waxy test (see Sections 1.1.2.1, 1.1.2.5 and 1.1.2.7). Soft scale insects feed on almost any live organ of the host plant, including the roots, although most species develop on the leaves or twigs or the trunk. Actual takeup of nutrients is from the phloem vessels and thus all species of Coccidae produce honeydew.

Diagnosis

The Coccidae are noxious pests (see Sections on Coccid Pests of Important Crops), causing direct injury by depleting the host plant of nutrients and damaging tissues (see Section 1.3.1), and indirectly through honeydew secretion which accumulates on crops. The consequent cover of sticky honeydew and the development of black sooty mold on crops reduces significantly their market value (Section 1.2.2.2). The control of soft scale populations in crops was based to a great extent on synthetic insecticides. However, the development of resistance to the latter in populations of the coccids, combined with increased awareness to the hazardous impact of these chemicals on the environment, created a beneficial shift to the application of IPM management, based on natural enemies (see Sections on Natural Enemies) and on more selective insecticides (see Section 3.2.1). Moreover, several coccid pests have been the targets and successful results of biological control projects (see Sections 2.3.1, 2.3.2 and 2.3.3). Although most species of soft scales are noxious plant pests, others are ranked as beneficial insects. Thus, the honeydew of various species is foraged by the honeybee, and of great benefit to apiculture (see Section 1.2.3.1). The voluminous waxy tests of several species are harvested in some countries and are processed into commercial products (see Section 1.2.3.2). These insects are usually sessile in their life habit, i.e. the complete life cycle of the adult female or male takes place at the settling site of the first nymph or crawler. However, the majority of species possess functional legs in all instars. Consequently, several species exhibit a considerable mobility between various organs of the host plant in the course of their annual development (see Section 1.2.1.1 and 1.3.4). Because of the sedentary life habit of the nymphs and adult females, the Coccidae are subject to several ecological difficulties. These pressures have been 'solved' in various ways. Thus: 1. the continuous pressure of living in a harsh environment is minimized by means of the waxy test cover (see Section 1.1.2.5); 2. the buildup of honeydew droplets around and above the insects is partly evaded through (a) the activity of honeydew-harvesting ants (see Section 1.3.5) and (b) by infesting the lower leaf surfaces of the host, thus avoiding the honeydew droplets are ejected away from the host plant and the coccid; 3. a successful symbiosis has evolved between species of Coccidae and ants which is effective in deterring the activity of natural enemies (see Section 1.3.5). An additional mechanism is their ability potency to encapsulate the eggs or larvae of parasitoids (see Section 1.3.6). Two modes of reproduction have been recorded among species of soft scales, sexual and parthenogenetic. It is premature to state which system is more common, since, for most described species, this parameter has not been recorded. However, it should be indicated that some of the cosmopolitan, widely-distributed species, e.g., Coccus hesperidum L., Saissetia oleae (Olivier) and Parasaissetia nigra (Nietner), are known to reproduce parthenogenetically throughout the range of their distribution. Two chromosome systems have been recorded in species of this family. The Comstockiella system, in which reproduction is sexual, and diploid arrhenotoky, which is a type of facultative parthenogenesis.

Soft Scale Insects - Their Biology, Natural Enemies and Control Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.

1.1.2 Morphology 1.1.2.1

The Adult Female

DANI]~LE MATILE-FERRERO

INTRODUCTION Most current classifications of the genera and species of Coccidae are based almost exclusively on the external features of the adult female (Steinweden, 1929; Borchsenius, 1957). However, the characters of the adult male are more useful than those of the female for a phylogenetic approach on higher taxa and Hodgson (1994) used both male and female characters for his classification. The Coccidae seem to be an homogeneous group, except for some atypical adult females, mainly in the genus Physokermes Targioni Tozzetti. Unlike adult females in other coccoid families, those of the Coccidae are often difficult to study, mainly because of the strong distention and thickness of the body at full maturity, which may become swollen, strongly convex, heavily sclerotized, hard and brittle. Young adult females can be studied satisfactorily, but unfortunately young adults, particularly in univoltine species, may occur for only a few days each year. Young and old females, however, can be most often recognizeA as Coccidae (like the immature stages) by the presence of a pair of anal plates (Figs 1.1.2.1.5,L; 1.1.2.1.7,B). Unlike males, which have prepupal and pupal instars, adult females emerge directly from the 2nd-or 3rd-instar nymphs (according to species) and continue to grow slightly or considerably, changing significantly in shape and colour (Kawai, 1980; Gill, 1988). Each young adult female may grow from two to eight times the size of its previous instar. Adult females of many species become swollen and heavily sclerotized (e.g., Toumeyella sp., Fig. 1.1.2.1.1,F). Several other species secrete a thick waxy test (e.g., Ceroplastes spp. Fig. 1.1.2.1.1,C), others a thin glassy test (e.g., Inglisia spp.). Many remain naked (e.g., Coccus spp.) but, in several genera related to Pulvinaria, a more or less elongate cottony ovisac is secreted, which is usually fairly short and slightly carinate, as with Pulvinaria spp., or ring-like as with Takahashia japonica Cockerell (Fig. 1.1.2.1.1,A,B) or deeply carinate, short and broad, as with Ceronema africana Macfie (Fig. 1.1.2.1.1,G,H); others are flattish, resembling bird droppings, such as those of Mametia louisieae Matile-Ferrero (Fig. 1.1.2.1.8,A). The ovisacs of Pulvinarisca serpentina (Balachowsky) can be very long, up to 30 mm. The size of the adult females of Coccidae with the wax removed, ranges from a little over 1.0 mm to about 18 mm in length at maturity. Vinsonia stellifera (Westwood), one of the smallest species, reaching only about 1.5 mm long, while Toumeyella sp. grows up to about 14 mm long (Fig. 1.1.2.1.1 ,F) and Eulecanium giganteum (Shinji) to about 18 mm long. The form of the adult female in life may vary considerably, depending on whether it feeds on leaves, stems or twigs. Host-induced morphological variation can also be observed (cf. below and Section 1.1.3.5).

Section 1.1.2.1 references, p. 20

6

Morphology

External morphology of the adultfemale The whole dorsal cuticle may become hard and glossy and variously coloured, either plain, spotted or brightly coloured. The colour may vary within a population, usually according to age. Toumeyella liriodendri (Gmelin), for example, varies from grayishgreen to pink-orange or dark brown (Hamon & Williams, 1984). While the ventral cuticle hardly changes after the last moult, the dorsal cuticle becomes thick and sclerotized. The cuticle of swollen, spherical and fully-grown females (sometimes therefore referred to as "hard scales") change considerably during the teneral period. For example, the cuticle of the dorsum of fully grown female Saissetia coffeae (Walker) is about four times thicker than immediately after the final moult, and more than ten times thicker than the ventral cuticle (Koteja et al., 1976). These changes are much less pronounced in the dorsal cuticle of females that produce an ovisac, in which the derm remains fiat and soft, hence the vernacular name "soft scales". The dorsum remains membranous on females which are entirely enclosed within an ovisac, such as with species of Eriopeltis (Fig. 1.1.2.1.1 ,D), while the dorsal cuticle of females not enclosed within an ovisac may become slightly sclerotized, as with Pulvinaria spp. Important external features of young adult female Coccidae are discussed below. As new species are discovered, some morphological features may become of increased significance, so that the following descriptions should not be treated as definitive. The characters discussed here are based on properly stained specimens, using light microscopy with a magnification up to 2000X.

GENERAL STRUCTURE The general appearance of the young female is very similar to that of the second- or third-instar female and therefore is usually termed neotenic, as compared with the adult male. The shape of slide-mounted specimens is narrow to broadly oval, subcircular or sometimes pyriform, and dorso-ventrally flattened. Adult females have well-developed legs and antennae, except in a few genera where these appendages are reduced or vestigial. Only a few species, such as Houardia troglodytes Marchal, are legless. The head, thorax and abdomen are fused. Members of the Coccidae are provided with two anal plates located at the base of an anal cleft. The anal cleft may be very deep, parallel-sided or strongly divergent. The margin of the anal cleft is usually devoid of setae but a few species possess an anal cleft with marginal or submarginal setae, which may be slender as on species of Physokermes and Filippia or spine-like as on Metaceronema sp. The anal cleft may be fused along its whole length, as with some species of Etiennea (Fig. 1.1.2.1.5,A). The antennae, eyes and mouthparts indicate the head, while legs and spiracles mark the thoracic segments.

L

Fig. 1.1.2.1.1. General appearance of fully-grown, adult females. A - Takahashia japonica Cockerell, cottony ring-like ovisacs of aggregated females on a twig, Japan. B - Takahashiajaponica, naked adult female (7 mm long) with its cottony ring-like ovisac. C - Wax test of Ceroplastes sinensis Del Guercio, France, on C/trus sp. (4.5 mm long). D - Felted ovisac enclosing the female of Eriopeltisfestucae (Fonscolombe), Hungary, on grass (10 mm long). E- Saissetia oleae (Olivier), France, on Nerium oleander, note the dorsal H-shaped ridges (2.5 mm long). F - Toumeyella sp., Mexico, on Erythrina sp. (14 mm long). G, H Ceronema africana MacFie, adult female, Senegal, on Vigna unguiculata: G - Frontal view of three adult females and their ovisacs; H - Lateral view of 2 ovisacs (5 mm high). (A,B from Kawai, 1972; C-H, photographs by J. Boudinot, MNHN, Paris).

Morphology

The abdominal segmentation of most species is usually conspicuous only on the midregion on the ventral surface and can usually be detected by the arrangement of the ventral body setae. It is generally agreed that the ventral abdominal segments I and II are fused together. The anal opening is on the Xlth abdominal segment. On the Xth segment are the anal ring and anal fold, the IXth is composed of the anal plates, while the VIIIth segment bears the vulva. The cuticle is sparsely covered with setae and pitted by openings of secretory glands pores, ducts and glandular dorsal tubercles - which are described below. The cuticular secretory glands of the adult female are sometimes also found in other instars of both sexes, while others are restricted to the adult female, especially the ventral multilocular disc-pores associated with the vulva, the dorsal and ventral tubular ducts and the dorsal preopercular pores (see below). For many species, the morphology is quite constant. However, host-induced variation of morphological characters occurs on some Coccidae (see Section 1.1.3.5) and has been recorded for two world-wide pests, Coccus hesperidum (L.) in Rhodesia (Hodgson, 1967) and Parasaissetia nigra (Nietner) on a world basis (Ben-Dov, 1978).

B

Fig. 1.1.2.1.2. Paralecanium carolinensis Beardsley, adult female, Caroline Is., on Pandanus sp. A - Details of the stigmatic cleR, stigmatic setae and marginal fan-shaped setae. B - a fan-shaped seta. (Modified from Beardsley, 1966).

MARGIN The junction of the dorsal and ventral surface of the body is usually marked by a fringe of setae, the marginal setae. Physokermes species are atypical in being devoid of marginal setae. Marginal setae are usually arranged in a single row, varying from only a few to numerous. They may be stout or slender, spine-like, straight or curved, conical, cylindrical, deeply frayed or fimbriate, bifid, chisel-shaped, or fan-shaped (as on Paralecanium (Fig. 1.1.2.1.2)). The marginal setae on a given species are generally of the same shape and size, but sometimes they may be variously shaped. At the posterior end of the abdomen, the marginal row of setae sometimes terminates in one to several longer setae. The number of marginal setae between each anterior cleft or laterally between the anterior and posterior clefts is sometimes of taxonomic value. The row of marginal setae is often interrupted on the thorax by four groups of stigmatic setae, also called spiracular setae, located laterally to the stigmatic furrow (cf. ventral surface below). The stigmatic setae are usually well differentiated from the

External morphology of the adultfemale m a r g i n a l setae, o f v a r i a b l e shape and located in a slight or deep d e p r e s s i o n k n o w n as the stigmatic or spiracular cleft. T h e y are s o m e t i m e s displaced onto the dorsal surface (Fig. 1 . 1 . 2 . 1 . 9 , A ) . On m o s t species, each g r o u p o f stigmatic setae is c o m p o s e d o f three setae, the m e d i a n stigmatic seta usually being the larger, the two lateral setae u s u a l l y s m a l l e r and o f equal length to each other (Fig. 1 . 1 . 2 . 1 . 3 , C ) . Several species p o s s e s s

Fig. 1.1.2.1.3. Etienneaferox (Newstead), adult female, Ivory Coast, on Xylopia sp. A - Dorsum and venter. B-G: ventral structures. B - Minute duct. C - Area of stigmatic furrow, with three stigmatic setae and marginal setae. D - Quinquelocular disc-pore. E- Hind tibia, tarsus, tarsal digitules, claw and claw digitules. F - Tubular duct. G - Multilocular disc-pore. H-N: dorsal structures. H - Preopercular pore. J - Derm of mid-dorsal area showing pattern of cell-like areolations. K - Body seta. L - Submarginal glandular tubercle. M - Minute duct. N - Derm of submarginal area showing pattern of cell-like areolations. (From Matile-Ferrero and Le Ruyet, 1985).

Section 1.1.2.1 references, p. 20

10

Morphology only one stigmatic seta, while others have more than three (Figs 1.1.2.1.2,A; 1.1.2.1.4,C). Houardia mozambiquensis Hodgson can have 120-140 per cleft, where they cover the inner margin of a deep sclerotize~ stigmatic cleft (Hodgson, 1990), while some species of Ceroplastes have up to 300 stigmatic setae lateral to each stigmatic furrow (Gimpel et al., 1974). The shape, size, number and location of the stigmatic setae are of taxonomic importance and are often used at the genetic level. Differentiated stigmatic setae are sometimes absent, as on species of Eriopeltis, Physokermes, Vittacoccus, some Toumeyella and on Etiennea villiersi Matile-Ferrero (Fig. 1.1.2.1.5,C).

VENTRAL SURFACE The ventral surface usually remains membranous throughout the life of the insect. The antennae of most Coccidae are long and slender and are five to nine-segmented, the third segment being the longest (Fig. 1.1.2.1.8,C). Several sensory organs are present, such as fleshy and slender setae and basiconic and campaniform sensillae (Koteja, 1980; Rosciszewska, 1989). Each apical segment bears three fleshy setae, several slender setae and one basiconic sensilla. Each of the two subapical segments possess one fleshy seta. The second segment has a campaniform sensilla. Antennae are variable in size within the family. They can be fully developed, long or short and reduced to one segment, such as on species of Houardia (Hodgson, 1990) and on Inglisia vitreae Cockerell. Eyes are present on most species but are not always easy to detect. They are reduced to a small eyespot placed dorsally near or on the margin, anterior to each antenna (Fig. 1.1.2.1.9,A). Sometimes they are present on the submedian dorsal area of the head, as on many Paralecaniini. The mouthparts are located between the bases of the anterior legs. They are composed of three main parts: the internal frame or tentorium, the piercing-sucking stylets and the labium. Externally, only the clypeolabral shield, which covers the internal frame, and the labium are visible. The moderately sclerotized clypeolabral shield bears two labral setae and two marginal setae (Koteja, 1976). The labium is short, one- or indistinctly two-segmented, usually hemispherical or conical, with a rounded apex, with five pairs of setae always present throughout the family (Koteja, 1974). Legs are well developed on most Coccidae, each composed of five segments, the tarsus bearing an apical tarsal claw. The median and posterior pairs of legs are usually of the same size, the anterior pair sometimes shorter. The legs are long on most species, greatly reduced on some, vestigial on a few, such as on Cribrolecanium andersoni (Newstead), Eumashona msasae (Hall) and several Toumeyella species; rarely, they may be entirely absent, as on Inglisia vitreae and most Cryptostigma species. Throughout the family, the trochanter possesses one pair of sensory pores on each side. The tibia and tarsus may articulate by means of an articulatory sclerosis (Fig. 1.1.2.1.8,J), or they may be fused without a sclerosis (Fig. 1.1.2.1.3,E). Each tarsus and claw bears a pair of long digitules. The tarsal digitules are slender, slightly knobbed apically and are usually equal in size. The claw digitules are paired and usually thick, broadly knobbed apically, often of the same size but sometimes they are disparate, as on most immature specimens (Fig. 1.1.2.1.8,J). The claw may bear an inner denticle. In contrast to many Eriococcidae and Pseudococcidae, no translucent pores have been found on the hind legs of the Coccidae. There are two pairs of spiracles situated lateroventrally on the thorax and these are of the same structure (Fig. 1.1.2.1.3,A). They are sometimes displaced towards the margin, as on some species of Cryptostigma. The anterior pair, which is sometimes smaller, is believed to mark the border between the prothorax and the mesothorax. The posterior pair lie between the mesothorax and the metathorax

External morphology of the adult female

(Hamon & Williams, 1984). The spiracles are short and stout, composed of a peritreme, an atrium and an arm or apodeme, variable in size and thickness, sometimes surrounded by a sclerotic plate. The peritreme and atrium are devoid of pores throughout the family. Abdominal spiracles are absent in the Coccidae.

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1.1.2.1.4. Richardiella taiensis Matile-Fermro and I.r Ruyet, adult female, Ivory Coast, on Gilber~iodendron splendidum. A - Dorsum and renter. B-H: ventral structures. B - Minute duct. C - Area

Fig.

o f stigmatic furrow with numerous stigmatic setae and marginal setae. D - Quinquelocuh, r disc-pore. E - Seta o f submarginal row. F - Tubular duct. G - Body scta. H - Multilocular disc-pore. J - Anal plates, dorsal and ventral. K-N: dorsal structures. K - Large cribriform pore. L - Minute duct. M - Body seta. N - Hairlike seta. (From Matile-Ferrero and I..r Ruyet, 1985).

Section 1.1.2.1 references, p. 20

12

Morphology

The genital opening, or vulva, is not clearly discernible in the Coccidae, in contrast to the conspicuous vulva of the Diaspididae, Pseudococcidae and many other families. It opens on the VIIIth segment and its position can be detected only by the presence of clustered multilocular disc-pores.

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A - D o r s a l a s p e c t (left side)

C - Head, ventral view.

G - 10th s e g m e n t o f left a n t e n n a , ventral v i e w .

F - 3rd

J - Claw of foreleg.

27

The adult male

Abbreviations used in Fig. 1.1.2.2.2 aas ab ads

aed al ams amss an anp

apar as asc ase

astnls at atp ax 1

axz ax3 bra bas bma bs c ca

cb CCX ce

el CX

dhs dmcr dos dps dse dss eprrh epm3 eps: eps3 eps3s f fm

fp fs g gls gP gs gts h hs ior lmcr lpl lpns lse mc mdr med mo

mpns nlr mt8 o ocs

pa per:

ante-anal setae antennal bristles abdominal dorsal setae aedeagus alar lobe antemetaspiracular setae anterior metasternal setae anus anterior notal wing process anterior postalar ridge abdominal sternite additional sclerite apical seta anteprosternal seta abdominal tergite anterior tentorial pit first axillary wing sclerite second axillary wing sclerite third axillary wing sclerite basal rod of aedeagus basalare basal membranous area sensilla basiconica cicatrix cranial apophysis coxal bristle(s) costal complex of wing veins caudal extension claw coxa dorsal head setae dorsomedial part of midcranial ridge dorsal ocular setae dorsopleural setae dorsal simple eye dorsospiracular setae mesepimeron metepimeron mesepisternum metepisternum postmetaspiracular setae furca segments of flagellum, 3rd to 10th femur furcal pit fleshy seta gena seta of glandular pouch glandular pouch genal setae setae of genital segment haltere hair-like seta interocular ridge lateral branch of midcranial ridge lateropleurite lateral pronotal setae lateral simple eye median crest median ridge media mouth opening medial pronotal setae marginal ridge metatergal setae ocellus ocular sclerite postalare precoxal ridge of mesothorax

pcq pdc pepcv plat plaz pla3 plr~ plr2 plrs pms pmss pth pn3 pna pnp pnr pocr ppar pra prn prnr procr pror prsc ps pscr pscs pt pta ptp ptr2 ptr3 pts pwp2 pwp3 rad sa set.scla scl self scls scp set sctse ser

sp2 sP3 spl ss stn 1

stn2 stn3 stnls stn2s t

tar tdgt teg tegs tib tibs tp tr udgt vhs vmcr vps vs vse

vestigial precoxal ridge of metathorax pedicel proepisternum + cervical sclerite propleural apophysis mesopleural apophysis vestigial metapleural apophysis propleural ridge mesopleural ridge metapleural ridge postmesospiracular setae posterior metasternal setae mesopostnotum metapostnotum postnotal apophysis posterior notal wing process pronotal ridge postocular ridge posterior postalar ridge prealare lateral pronotal sclerite pronotal ridge preocular ridge preoral ridge prescutum penial sheath prescutal ridge prescutal suture posttergite posterior tentorial arm posterior tentorial pit peritreme of mesothoracic spiracle peritreme of metathoracic spiracle posttergital setae mesopleural wing process vestigial metapleural wing process radius subalare subapical seta scutellum scutellar foramen scutellar setae scape scutum scutal setae subepisternal ridge mesothoracic spiracle metathoracic spiracle sensillum placodeum suspensorial sclerite prosternum basisternum of mesosternum metasternum prosternal setae basisternal setae tendon-like apodeme tarsus tarsal digitule tegula tegular setae tibia tibial spur triangular plate trochanter ungual digitule ventral head setae ventral part of midcranial ridge ventropleural setae ventral sclerite ventral simple eye

Morphology

28

Anterior to the epistemum, the metathoracic spiracle (spa) and its supporting peritreme (ptr3) are located. Ventrally a median plate or irregular sclerotization represents the metasternum (Stna).

Wings The semitransparent fore-wings are about as long as the body (excluding the genital segment) and two to three times longer than wide. They have a narrow base and a broadly rounded apex. When halteres are present, a small alar lobe (ai) is found near the base on the hind-margin of the wing; the apical setae of the haltere hook onto an invagination of the lobe. Two distinct wing veins are present, the radius (rad) and media (reed), while an elongate sclerite near the anterior margin of the wing forms the costal complex of wing veins (ccx) which articulates with the anterior notal wing process. Other sclerites involved in the articulation of the wing are the tegula (teg), three axillary sclerites (axl, ax2 and ax a) the additional sclerite (asc). The hind wings are either absent or reduced to halteres (h), also called hamulohalteres. They usually bear one hooked seta, but in some species there may be three or four.

Legs All three pairs of legs are usually long and slender. The eoxa (cx) is short and broad, and articulates distally with the short trochanter (tr) which is narrow basally and broad distally, and is separated from the femur (fro) by a narrow strip of membrane. The femur is long and broad, the tibia (tib) long and slender. The elongate tarsus (tar) is one-segmented and articulates with a single claw (el).

ABDOMEN The abdomen is composed of eight pregenital segments and a 9th or genital segment; the first segment is not developed ventrally. The segmentation is indicated by shallow transverse grooves. Most of the abdomen is membranous, but tergal and sternal plates may be present in some species. Where present, the abdominal tergites (at) are usually situated laterally in the more anterior segments and medially in the posterior segments. The abdominal sternites (as) are large, transverse plates which may be absent or medially interrupted in the intermediate segments. Pleural sclerotization may be present on the caudal extensions of segment VII and VIII and occasionally more anteriorly. Caudal extensions (ce) are found on the VII and VIII segments of many species. Their shape and size vary interspecifically. Those of the VII segment are usually lobiform, but they may be tapering and finger-like. On the VIII segment, they may be lobiform, cylindrical, mammillate or various other shapes. In the Coccus-group of species, a circular, membranous, weakly-reticulated cicatrix (c) is found on the distal part of caudal extension VIII. Near the posterior rim of the VIII segment, a funnel-shaped glandular pouch (gp) with two long setae is usually present on each side. These setae give support to the waxy filament produced by the multilocular pores in the pouch. The filaments are very conspicuous in the living males but their function is uncertain. The pouch and pores are absent in some species. The IX or genital segment is elongate and forms a long, tubular style which is comprised of the penial sheath (ps) and the aedeagus (aed). The penial sheath is composed of sternum IX and sclerotized laterally. Anteroventrally, a basal membranous area (bma) is found and, posterior to this, a narrow median ridge represents the basal rod (bra). The latter supports the tubular aedeagus which is situated in a slit of the penial sheath. Dorsally, a small anus (an) is present in the membrane at the base of the segment. Anterior to this a small 9th tergite (atg) can sometimes be seen.

The adult male

29

CHAETOTAXY The two basic types of setae of male Coccidae are the fleshy setae (fs) and hair-like (hs) setae. The former are more thick-set, with a blunt apex and the setal membrane is not surrounded by a distinct basal ring; the latter have an acute apex and a distinct basal ring. Bristles, larger than the fleshy setae, are present on the distal segments of the antennae and on the front coxae. The setae of the head can be divided into four groups, i.e. dorsal head setae (dhs), dorsal ocular setae (dos), ventral head setae (vhs) and genal setae (gs), the latter being only present in some groups of species. When the setae are predominantly of the fleshy type, as in C. hesperidum, the head appears distinctly hairy. The antennae also appear hairy, carrying numerous fleshy and a few hair-like setae. Large antennal bristles (ab) are present on the distal segments. On the terminal segment, long, capitate subapical setae (set. scla) are found. The latter are usually three in number, but may vary from zero to six. On the prothorax, several groups of fleshy and hair-like setae are found, i.e. the lateral pronotal setae (lpns), medial pronotal setae (mpns), posttergital setae (pts), anteprosternal setae (astnis) and prosternai setae (stnis). However, the full complement is only present on some species. On the mesothorax, one may find scutai setae (sctse), scutellar setae, (scls), tegular setae (tegs), postmesospiracular setae (pms) and basisternal setae (stn=,s). Metathoracic setae that may be present are the metatergai setae (mts), dorsospiracular setae (dss), antemetaspiracular setae (ams), postmetaspiracular setae (eps~s), anterior metasternal setae (amss) and posterior metasternal setae (press). The wing surface is covered with microtrichia and, in addition, a small number of hair-like alar setae (als) may be present on the anterior part of the base of the wing. On the legs, fleshy and hair-like setae occur abundantly on all the segments except the claw. In some species, the anterior coxae also carry long coxal bristles (cb) which are sometimes capitate. Ventrally, near the apex of the coxa and the trochanter, one or two long, hair-like apical setae (ase) are found, while an apical spur (tibs) occurs in this position on the tibia. A minute seta occurs anteriorly and posteriorly in the articular membrane between the coxa and trochanter. A pair of capitate tarsal digitules (tdgt) are present near the dorsal apex of the tarsus and a pair of claw or ungual digitules (udgt) occur on the claw. The abdomen usually has a single pair of hair-like dorsal setae (ads) on segments IV to VII, but in some species they are present on all segments; dorsal fleshy setae are present on some species. Pleural setae occur in groups of dorsopleural setae (dps) and ventropleural setae (vps) which sometimes coalesce, while ventral setae (avs) occur medially on the segments. The position and number of the hair-like setae are more constant than those of the fleshy setae. In addition to these setae, three hair-like setae and occasionally a fleshy seta occur lateral to the glandular pouch on the posterior margin of the VIII segment. In the region anterior to the anus, two long, two short and a few fleshy ante-anal setae (aas) may be present. On the penial sheath a number of small, scattered genital setae (gts), which are probably tactile receptors, can be seen. Fleshy setae are found on the penial sheath of Ceroplastes ceriferus (Fabricius) (Miller, 1991).

OTHER CUTICuLAR STRUCTURES Sensilla and pores occur on various parts of the body. Some of the sensilla are very constant in position and occur in the same position on all the species studied. Examples are the sensillum placodeum (spi), which occurs distally on the dorsolateral surface of the pedicel, the two sensilla basiconica (bs) on the ventral surface of the terminal antennal segment and the ring of six (sometimes eight) oval, campaniform sensilla in the

Section 1.1.2.2 references, p. 30

30

Morphology

basal half of the trochanter. A variable number of sensilla basiconica may occur on the 3rd antennal segment and what are possibly campaniform sensilla on the apex of the style. Very few pores are found on the body. In addition to the multilocular disc-pores of the glandular pouch on the VIII abdominal segment, a variable number of circular pores that resemble seta sockets, from which the seta was detached, occur dorsally behind the pronotal ridge in some species. Minute dermal denticulations are present on the dorsal and ventral surfaces of the median part of each abdominal segment.

REFERENCES Bodenheimer, F.S., 1953. The Coccoidea of Turkey. III. Revue de la Facult6 des Sciences de l'Universit6 d'instanbul (Series B), 18: 91-164. Borchsenius, N.S., 1957. Sucking Insects, Vol. IX, Suborder mealybugs and scale insects (Coccoidea). Family cushion and false scale insects (Coccidae). Fauna SSSR. Zoologicheskii Institut Academii Nauk SSSR, Novaya seriya, 66: 1-493. (In Russian). Farrel, G.S., 1990. Redescription of Cryptes baccatus (Maskell) (Coccoidea: Coccidae), an Australian species of soft scale. Memoirs of the Museum of Victoria, 51: 65-82. Giliomee, J.H., 1967. Morphology and taxonomy of adult males of the family Coccidae (Homoptera: Coccidae). Bulletin of the British Museum (Natural History), Entomology Supplement 7: 1-168. Gimpel, W.F., Miller, D.R. and Davidson, J.A., 1974. A systematic revision of the wax scales, genus Ceroplastes, in the United States (Homoptera: Coccoidea: Coccidae). Miscellaneous Publication Agricultural Experiment Station, University of Maryland, 841 : 1-85. Hodgson, C. J., 1991. A redescription of Pseudopulvinaria silda'mensis Atkinson (Homoptera, Coccoidea), with a discussion of its affinities. Journal of Natural History, 25:1513-1529. Hodgson, C. J., 1993. The immature instars and adult male of Etiennea (Homoptera: Coccidae) with a discussion of its affinities. Journal of African Zoology, 107: 193-215. Hodgson, C. J., 1994. The Scale Insect Family Coccidae: an Identification Manual to Genera. CAB International, Wallingford, UK, 639 pp. Manawadu, D., 1986. A new species ofEriopeltis Signoret (Homoptera: Coccidae) from Britain. Systematic Entomology, 11 : 317-326. Miller, G.L., 1991. Morphology and Systematics of the Male Tests and Adult Males of the Family Coccidae (Homoptera: Coccoidea) from America North of Mexico. Ph.D. Thesis, Auburn University, Auburn, USA. Ray, C.H. and Williams, M.L., 1980. Description of the immature stages and adult male of Pseudophilippia quaintancii (Homoptera: Coccoidea: Coccidae). Annals of the Entomological Society of America, 73: 437-447. Ray, C.H. and Williams, M.L., 1983. Description of the immature stages and adult male of Neolecanium cornuparvum (Homoptera: Coccidae). Proceedings of the Entomological Society of Washington, 85: 161-173. Tang, Fang-teh, 1991. The Coccidae of China. Shanxi United Universities Press, China, 377 pp. (In Chinese, English summary). Tang, Fang-teh, Hao, J., Xie, Y. and Tang, Y., 1990. Family group classification of Asiatic Coccidae (Homoptera, Coccoidea, Coccidae). Proceedings of the Vlth International Symposium of Scale Insect Studies, Cracow, August 6-12th, 1990. Part II: 75-77. Theron, J.G., 1958. Comparative studies on the morphology of male scale insects (Hemiptera: Coccoidea). Annals of the University of Stellenbosch, 34(A): 1-71.

Soft Scale Insects - Their Bio!ogy, Natural Enemies and Control

Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.

1.1.2.3

31

The Immature Stages

MICHAEL L. WILLIAMS

INTRODUCTION The classification of taxa in the family Coccidae has been based primarily on morphological characteristics of the adult female. More recently characters of the adult male have also been used (see Section 1.1.2.2). Little work has been done on the immatures. Of the immature stages, the first instar or "crawler" stage has been studied most but, even so, first instars of less than 5 % of the known species have been adequately described. Miller (1991) published a key and illustrations, diagnoses and discussions on relationships of first instars in sixteen families of the Coccoidea, including the Coccidae, but information on the other immature stages is practically non-existent. Most published keys to and descriptions of immature scale insects cover only a single species. Table 1.1.2.3.1 presents a summary of publications which contain descriptions and/or illustrations of immature stages for 118 species of soft scales. Scientific names presented herein follow the classification of Ben-Dov (1993), with a few changes from Hodgson (1994).

DEVELOPMENT IN SOFT SCALE INSECTS In the Coccidae, the female generally goes through four developmental stages, while the male has five. For some species, however, it appears that the third instar female is the adult stage and there are only two immature stages in the female (Hodgson, 1994). There are always five stages of development in the male, with the third instar being called the "prepupa" and the fourth instar the "pupa". The fifth instar is the adult male. The third, fourth and adult male stages all develop within the wax cover or test produced by the second stage male. When the male matures, it ecloses from the test by backing out from beneath it.

GENERAL CHARACTERISTICS The following is a summary of the general morphology of the immature stages in male and female Coccidae. For diagnostic purposes, the characters discussed for each of the developmental stages present the usual features as they are most commonly seen in the instar being described. Both general appearance and characteristics of slide mounted specimens are discussed for the first and second instars. For the third and fourth instars, only a discussion of the general morphology is presented, as descriptive information is available in only a few species for these developmental stages. Study of the immature stages is in its infancy, and one should keep in mind that, while some exceptions are noted below, variations to other character states are likely to exist. For a more complete coverage of the variation of characters in the first instar, refer to Section 1.1.3.3 Taxonomic Characters - Nymphs. The terminology used primarily follows that of

Section 1.1.2.3 references, p. 46

Morphology

32

Williams and Kosztarab (1972) and Ray and Williams (1980). Where these terms differ from those used in Section 1.1.3.1, alternatives are included in parenthesis. The illustrations presented here of the bisexual woolly pine scale, Pseudophilippia quaintancii Cockerell, and of the parthenogenetic pyriform scale, Protopulvinaria pyriformis (Cockerell), are provided as representing two patterns of development, i.e. P. quaintancii in which there is a reduction in the size of both the antennae and legs as the nymphs develop, whereas in Pr. pyriformis these appendages remain well developed throughout metamorphosis.

FIRST-INSTAR MALE AND FEMALE (Figs 1.1.2.3.1; 1.1.2.3.2) GENERAL APPEARANCE The first instar or "crawler" is the dispersal stage and is generally the most active developmental stage in the soft scales. In this stage the sexes are indistinguishable and share the following characteristics: eyes present; anal plates present, each plate generally with a long apical seta; legs well developed and five-segmented; each tarsus with a pair of knobbed digitules except on the prothoracic legs which have one of tarsal digitules setiform; each antenna well developed and five-or six-segmented; spiracular setae usually differentiated from marginal setae; anal ring well developed, with six setae; multilocular disc-pores and tubular ducts absent from abdominal region. CHARACTERISTICS OF SLIDE-MOUNTED SPECIMENS

Body: oval to elongate oval. Derm membranous throughout, usually smooth but on occasion rugose or papillate. Appendages, mouthparts, spiracles, anal plates, setae, pores and microducts sclerotised. Segmentation: head, thorax and abdominal segments closely fused. Segmentation not readily apparent, usually best defined in the mid-abdominal regions. Antennae, eyes and mouthparts delineate the head region. Legs, spiracular furrows, spiracular setae and spiracles located on thoracic region. Dermal folds on abdomen indicate abdominal segmentation. Usually with a pair of ventral body setae present submedially on each abdominal segment. Generally, marginal setae present on all segments. Antennae: well developed on all specimens, usually 6-segmented, but 5-segmented in some genera (e.g., Toumeyella sp.). The third segment and the terminal segment generally longest and roughly the same length in most species. Hairlike setae usually on all antennal segments, but sometimes absent from segment 4 of 6-segmented antennae. Enlarged sensory setae present on segments 4, 5, and 6. A simple sensory pore present on segment 2 of all species studied. Eyes: located on lateral margin of head, just anterior to or level with antennal scape, reduced to a single facet. Mouthparts: mouthparts lie between prothoracic coxae, consisting of a clypeolabral shield, 1-segmented labium and stylet loop. Labium generally with 6-8 setae. Legs: well developed, without tibio-tarsal sclerotisation or free articulation. Two sensory pores present on each face of trochanters. Various hairlike setae present on each segment. Each trochanter generally with one long hair-like seta, occasionally 2. Knobbed digitules in pairs on both tarsus and claw except for the prothoracic leg where 1 tarsal digitule is setiform. Microctenidia on tibial apex present or absent. Tarsal claw simple or with a denticle. Denticle may be pronounced or only slightly evident.

The immature stages

33

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Spiracles: one pair on each meso- and metathorax. Each spiracular furrow with 3-4 pores, usually tri-, quadri-, quinque- or multilocular disc-pores. Sometimes these discpores clustered near peritreme of spiracle. Spiracular setae: generally differing in shape from the marginal setae; usually with 3 stout setae with blunt apices, positioned at the marginal end of each spiracular furrow, with the median seta of each group usually twice as long as the 2 lateral setae, rarely subequal. Occasionally spiracular setae undifferentiated from marginal setae (e.g., Toumeyella parvicornis (Cockerell)). Stigmatic sclerotisations occasionally present.

Section 1.1.2.3 references, p. 46

34

Morphology

'G

\

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.

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Fig. 1.1.2.3.2. Protopulvinaria pyriformis (Cockerell), 1st instar (From Ray and Williams, 1982).

Anal plates: two anal plates present, well developed, triangular with rounded angles.

In Paralecanopsis formicarum (Newstead), the anal plates are fused along the midline, giving it the appearance of only having a single, arched and bilobed, anal plate. Dorsum of each plate often with areolations or shingle-like reticulations, which can be important for identification at the species level (Sheffer and Williams, 1990). Generally with 3 or 4 setae present on dorsum of each anal plate, with 3 apically and 1 on mesal margin. Apical seta on each plate generally long, approximately 1/3 to 1/2 as long as total body length, but rarely short. When present, the long median apical seta is a good diagnostic character for separating first instars from other stages. One ventral subapical seta present per plate.

The immaturestages

35

Anal ring" subcircular, circular to hexagonal in shape with 6 long, stout hairs and 10-14 irregularly-shaped pores, located at the end of a short anal tube. Pores: generally pore groupings on the dorsum are located in rows submarginally, submedially and/or medially. Pore groupings consisting of simple disc pores (simple pores), bilocular pores (dorsal microductules) or with a pair of pores (consisting of 1 bilocular and 1 disc pore). Bilocular pores are categorized as small (1-2 #) to large (5-8 #). A dorsal trilocular pore present near the anterior margin on each side of the head. In some species, special pore types particular to the species are present on the dorsum (e.g., Toumeyella parvicornis, which has bilocular pore clusters submarginally on the dorsum). Multilocular disc-pores with 3 to 5 loculi occur in each spiracular furrow or may be clustered near or in the peritreme of the spiracles (e.g., Paralecanopsis

formicarum). Ducts: ventral microducts present in a submarginal row between each of the pairs of ventral body setae on abdomen, one on each side between anterior and posterior spiracular furrows and one on each side of the head just below level of the antennal scape. A dorsal microduct (dorsal microductule) is occasionally present on each side of body laterad of the level of the antennal scape and generally 2 located submarginally between anterior and posterior spiracular setae. Body setae: marginal setae slender, hair-like to stout and lobate, generally distributed as follows: 8 anteriorly between eyes, 2 on each side between eyes and anterior spiracular setae, 2 on each side between anterior and posterior spiracular setae and 8 on each side of abdomen. A few species may have many more marginal setae, (e.g., lnglisia patella Maskell, which has 120). Dorsal body setae slender and bristle-like, generally with 4 pairs in medial rows running between clypeo-labral shield and metathoracic legs. Ventral body setae short and bristle-like, generally with 1 on each side near anterior margin of head, 1 on each side between anterior and posterior spiracular regions and 7 pairs on each side of posterior abdominal segments. Two long interantennal setae present mesad of antennal scapes. Generally with three pairs of long ventral submedian setae on pregenital segments of abdomen (pregenital setae), with the most posterior pair being the longest. Dermal microspines: generally present on venter in median area of posterior abdominal segments.

SECOND-INSTAR FEMALE (Figs 1.1.2.3.3, 1.1.2.3.4) AND SECOND-INSTAR MALE (Fig. 1.1.2.3.5) Sexual dimorphism first becomes apparent in the second instar for, although the male and female nymphs of this stage are very similar morphologically, the female lacks the tubular ducts which are present dorsally in the male (Fig. 1.1.2.3.5). These tubular ducts are generally found marginally around the anterior two-thirds of the body and often occur in a transverse band on the dorsum at about segment four of the abdomen. Sometimes these tubular ducts are arranged in a pattern corresponding to the suture pattern seen in the male test. See Section 1.1.2.4 for discussions on the plates and sutures of the male test. An exception to this can be found in the second-instar female of the parthenogenetic Eulecanium cerasorum (Cockerell), which has tubular ducts on the dorsum around the margin of the body.

Section 1.1.2.3 references, p. 46

36

Morphology

C

___

Fig. 1.1.2.3.3. Pseudophilippia quaintancii Cockerell, 2nd-instar 9.

GENERAL APPEARANCE The shape of the body in the male is elongate oval, while that of the female is usually oval to round. Besides these features, the male and female are very similar and share the following characteristics: eyes present; anal plates present, without a long apical seta; anal cleft developed; five-segmented legs well developed or reduced; tarsi each with a pair of knobbed digitules; antennae well developed or reduced, usually six-segmented, but may have from five to seven segments; spiracular setae usually differentiated from marginal setae; anal ring well developed, with six setae; multilocular disc-pores and tubular ducts absent from ventral abdominal region; preopercular and discoidal pores absent.

37

The immature stages

9 [

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Fig. 1.1.2.3.4. Protopulvinaria pyriformis (Cockerell), 2nd-instar 9 (FromRay and Williams, 1982). CHARACTERISTICS OF SLIDE-MOUNTED SPECIMENS to elongate oval, round or pyriform. Derm membranous throughout. Segmentation more obscure than in first instar, occasionally visible on venter of abdomen. Anal cleft developed. Spiracular clefts not usually developed.

Body: oval

Antennae: well developed in most species, but may be reduced in some. Usually 6segmented, but ranges from 5 to 7 segments. Hairlike setae usually present on most segments and fleshy setae on last 3 segments. A simple sensory pore present on segment 2. Eyes: present on lateral margin of head.

Section 1.1.2.3 references, p. 46

38

Morphology

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Fig. 1.1.3.1.2. Schematic diagram of an adult female soft scale, left side showing dorsal structures and right side ventral structures. Where: ac = anal cleft; acs = crescentic sclerotisation around anal plates; ag = antennal groove; a g f = ano-genital fold; ans = anterior spiracle; ant = antenna; ap = anal plates; cls = clypeolabral shield; c r p = cribriform plate; d a m = dermal areolation with dorsal microductule; des = dermal sclerotisation; dot = dorsal tubercle; ds = dorsal setae; ~ = deep stigmatic cleft; dtd = dorsal tubular duct; eye = eyespot; ias = inter-antennal setae; la = labium; msl = mesothoracic leg; mfl = metathoracic leg; p a p = preantcnnal pore; pdp = pregenital disc-pores; ~ = pregenital sctae; pis = pocket-like sclerotisation; p o p = preopercular pores; pos = posterior spiracle; prl = prothoracic leg; sdp = spiracular disc-pores; ssc = shallow stigmatic cleft; ssp = stigmatic spine; sta = stigmatic area; stg = stigmatic groove; sts = stigmatic sclerotisation; sus = submarginal sctae and vtd = ventral tubular duct. In addition, II-VI = visible abdominal segments.

Taxonomic characters - adult female

117

V E N T R A L SETAE

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Fig. 1.1.3.1.3. Taxonomic characters of adult female soft scales: dorsal setae: D1 = setose or flagellate; D2 - sharply spinose; D3 -- bluntly spinose; D4 - clavate; D5 - spatulate; D6 - bluntly conical (as in Mallococcus spp.); D7 = very short (as in Ceroplastes spp.) and D8 = very short (as in Saccharolecanium spp.). Where bbs = broad basal socket and nbs = narrow basal socket. Ventral setae: V = generally finely setose. M a r g i n a l setae: M1 = setose" M2 = sharply spinose; M3 = bluntly spinose; M 4 = fimbriate; M_5 = bent and clavate; M6 = bent and bluntly spinose; M7 = digitate; M8 = spinose with open, divided apex; M 9 = short, stout, spinose, with open apex and M10 = fan-like (as in Paralecanium spp.). Where bbs = broad basal socket; nbs = narrow basal socket and ix) = pores in basal socket (as in Megapulvinaria maxima). Stigmatic spines" S1 = group of three unequal spines all with broad basal sockets; 82 = group of three unequal spines with dissimilar basal sockets; $3 = conical stigmatic spines (as in Ceroplastes spp.). Where bbs = broad basal socket and nbs = narrow basal socket. Dorsal microductules: E l - E 5 = side view under the light microscope, showing various shapes of sclerotised pore; E6 = dorsal views, showing variety of apparent structure as seen under the light microscope, depending on depth of focus. Where id = inner ductule; od = outer ductule and tp = true pore opening. Ventral microducts: G1 = side view of typical form of microduct; G2 = ventral view of typical microduct; G3 = microduct with differently-shaped inner ductule (as in Cryptes spp.) and G4 - ventral view of cruciform ventral microduct (as in Ceroplastes spp.). Where id - inner ductule and od - outer ductule.

118

Systematics Dorsal setae (Fig. 1.1.3.1.3) These are almost invariably present, except in the Cardiococcinae in which their absence is a key character. Dorsal setae are highly variable in form, i.e. flagellate (f'mely setose), sharply or finely spinose or they may have a swollen (clavate) apex, as in Kilifia. In Eriopeltis, MaUococcus and Metaceronema, these setae have become highly modified and conical, while in a few other genera, such as Maacoccus and Saccharolecanium, the setae are extremely short, even shorter than the width of their basal sockets. In most species, dorsal setae are randomly distributed but they have a distinct distribution pattern in a few genera, such as Tillancoccus and in the Cyphococcinae. Most setae are 4-10#m long but exceptionally they may be over 100#m long, as in Didesmococcus, Richardiella and Trijuba. A few genera have more than one type of dorsal seta, e.g., Parthenolecanium and Trijuba. In the Cyphococcinae, the setae form a distinct sinuous line separating the median area of the dorsum, which is covered by the glassy test, from the marginal area where pores and setae are frequent. Each dorsal seta has a basal socket in which it articulates. These sockets are usually rather uniform in structure but can be distinctive, as in Cajalecanium, Udinia and

Umwinsia. Dorsal pores As indicated above, the waxy tests produced by most Coccidae are secreted through the pores and ducts in the derm from underlying glands. The most widespread pores on the dorsum belong to three main categories, which are here referred to as (i) dorsal microductules, (ii) simple pores and (iii) preopercular pores. In most genera, the first two types are distributed more or less randomly throughout the dorsum, but in a few genera, such as Alecanochiton, Ctenochiton and Stictolecanium, they occur in a distinctly polygonal pattern.

i. Dorsal microductules (Figs 1.1.3.1.3,E 1-6). These were referred to as dorsal microducts by Hodgson (1994a). However, Foldi (in Section 1.1.2.7 of this volume) shows that the structure of the glands secreting through these pores is different from those of the ventral microducts and has introduced the term microductule for these structures. This has been followed here. These have frequently been referred to as bilocular pores by earlier authors and as filamentous ducts by Qin and Gullan (1992). Each is round to oval in shape and is located at the base of a short membranous duct. The pore opening is centrally placed and is round to slit-like. Most are minute, 2-3/xm in diameter, but a few are much larger, as in Didesmococcus, Eumashona and Ctenochiton. When viewed from above, these pores can appear to be bilocular, but this is an optical illusion due to the structure of the pore, the bilocular appearance being caused by two lateral, oval areas of thinner sclerotisation associated with two lateral 'closed' pores; the true structure is best seen from the side. The outer duct of each microductule is usually quite short - about the width of the sclerotised pore - but rarely may be much longer, as in Kozaricoccus. Arising internally from each pore is an inner, non-staining, membranous filament, which may be quite long and characteristically shaped in some species (e.g., in Kozaricoccus and Megapulvinaria maskelli (Olliff)). Because this filament is non-staining, it can be difficult to detect in some preparations. Dorsal microductules are typical of most Coccidae, but appear to be absent in the Ceroplastinae, Cissococcinae and some Cardiococcinae. Their structure is discussed in more detail by Foldi (Section 1.1.2.7). ii. Simple pores (Figs 1.1.3.1.4). These have been referred to by previous authors as 'dark-rimmed', 'discoidal' or 'disc' pores. They are small to minute pores but lack the inner filament of the dorsal microductules and only very rarely have an outer duct. There are at least two types (see Foldi, Section 1.1.2.7), namely 'open' and 'closed', although this distinction may be difficult to ascertain under the light microscope. Open

Taxonomic characters

-

adult female

119

SIMPLE PORES

PREOI)ERCULAR PORES

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Fig. 1.1.3.1.4. Taxonomic characters of adult female sol~ scales" simple pores: SI-$4 = surface and side views of variously shaped 'closed' pores (note surface usually apparently granulate, with no obvious pore opening under the light microscope, and lacking an inner ductule); $5 = 'open' pore (note the distinctpore aperture and lack of inner ductule). Preopercular pores: P1 = surface and side view of conical pore; P2-P4 = side views showing various shapes (note: all those pores are 'closed',with no obvious pore aperture, no inner ductulr and usually with a granulate surface). F'~,ure-of-eightpore: E - surface and side views (as in MaUococcus spp. Note: appears bilocular but true pore found centrally). Where id = inner ductulr and tp = true pore aperture. Flower-shaped pore: F = surface and side view (as in Anthococcus spp.), where id = inner ductule. Ceroplastes-type pores: restricted to the Ceroplastinae: C1-C3 = dorsal and side views of 'simple' pores and C4 and C5 = dorsal and side views of 'modified' pores; where id = inner ductulr with typically deeply divided apex; m p = main central pore and sp = satellite pores. C r i b r i f o r m plates: R1 and I{2 = surface views of plate, showing two forms, R1 being the generalised basic structure and R2 as in Eutaxia; where IX) = actual pores. Bilocular pore: B = typical pore as in Tectopulvinaria spp. Dorsal tubercles: T1 = side and dorsal view of 'normal' tubercle (as in Coccus and Saissetia); T2 = side view of intermediate type of tubercle (as in Couturierina); 1"3 side and dorsal view of most complex type of tubercle (as in Anopulvinaria); T4 and T5 = 'inverted' tubercles cr4 = Alichtensia attenuata and T5 = Lagosinia strachanQ; where cd = central duct; id = inner ductule and sd = satellite ducts. Pocket-like sclerotisation: L = dorsal and side view, where pi = pocket-like invagination.

120

Systemarics

pores have a distinct pore opening and are flat, whereas closed pores have no apparent aperture under the light microscope, and are generally slightly convex with a granular surface. Both types of pore are small (2-4#m in diameter), round to slightly oval and have slightly thicker margins so that they can appear 'dark-rimmed'. They are randomly distributed throughout the dorsum and their taxonomic significance is uncertain. iii. Preopercular pores (Figs 1.1.3.1.4, P 1-4). These pores have also been referred to as 'discoidal pores' and 'paraopercular pores' by earlier authors. In most species, they occur in a loose but distinct group just anterior to the anal plates. However, they may be much more widespread in some genera and species - as in Paralecanopsis turcica Bodenheimer - whilst in a few species (e.g., in Alecanochiton marquesi Hempel, Pulvinaria rhois Ehrhorn and more particularly in Didesmococcus spp.) they also occur in a small group medially on the head. In Palaeolecanium and most Cardiococcinae, preopercular pores occur in a distinct mid-dorsal line, while in many Paralecaniini they form two divergent lines. Preopercular pores are all closed pores (see Foldi, Section 1.1.2.7) and are rather variable in shape. They may be fiat, quite small (typically 35/,m in diameter), round to oval, and relatively unsclerotised with (under the light microscope) a slightly granular surface, as in Coccus hesperidum, when they look rather like slightly larger simple pores. In other genera, they may be large, strongly convex, heavily sclerotised and also generally have a rough or granular surface when viewed under the light microscope (these granulations relate to the minute microtubular pores through which the wax is secreted - see Foldi, Section 1.1.2.7); they can have quite deep vertical margins and so they may appear 'dark-rimmed' when viewed from above. The number, shape and distribution are important characters at the species and genetic level. Their function is unknown. Other pore types, which have a more restricted distribution, are as follows: iv. Multilocular disc-pores (Fig. 1.1.3.1.5). These are rare on the dorsum but are present in a submarginal band in Vittacoccus and densely throughout the dorsum in Pseudopulvinaria (although these might be better referred to as cribriform plates). Occasionally the spiracular disc-pores extend onto the dorsum (e.g., in Akermes and Lecanopsis) whilst in Myzolecanium the pregenital disc-pores occur along the margins of the anal cleft.

v. Figure-of-eight pores (Fig. 1.1.3.1.4). The structure of these pores in the Coccidae is similar to that found in the Asterolecaniidae, Cerococcidae and Lecanodiaspididae but, in the Coccidae, they are restricted to the genera Mallococcus and Bodenheimera. These are probably very large dorsal microductules and, like them, figure-of-eight pores can appear bilocular under the light microscope but again the actual open pore is a slit-like opening which occurs centrally and usually has a distinct, non-staining, membranous inner filament. These pores are 5-9#m wide at their widest point, oval in shape and slightly sunken. They are of considerable taxonomic significance. vi. Flower-shaped pores (Fig. 1.1.3.1.4). These are currently only known in Anthococcus and it is likely that they are merely dorsal microductules in which the outer rim has become ornate. Each pore is about 3-5/zm in diameter and has a long, flattened inner filament. vii. Ceroplastes-type pores (Fig. 1.1.3.1.4). These are restricted to the Ceroplastinae, where they are by far the most abundant pores, occurring throughout the dorsum except on the lateral lobes or clear areas. Each pore opening is 2-5~tm wide, heavily sclerotised, generally with a large central pore and 0-4 smaller (satellite) pores. Those with no satellite pores may be different and might represent what Williams and

Taxonomic characters - adultfemale

121

Kosztarab (1972)refer to as filamentous ducts. Ceroplastes-type pores generally have a long inner filament arising from the base of the central pore; these filaments are much branched or divided distally and so these pores were referred to as dendritic pores by De Lotto (1971). They almost certainly secrete the thick, soft waxy test typical of the Ceroplastinae. The structure of the associated gland system is discussed in Section 1.1.2.7. viii. Bilocular pores (Fig. 1.1.3.1.4). As indicated above, most of the pores referred to as bilocular by previous authors have only one central pore opening. 'True' bilocular pores, with a clear partition between the two loculi when viewed in side-view, are rather scarce in the Coccidae and are only known in a few genera, mainly from Central and South America (e.g., Pendularia, Pseudophilippia and Tectopulvinaria). They are 510#m wide and occur throughout the dorsum. ix. Other pore types. A variety of other pore types are known, but they are probably modifications of those describe~ above. Thus, in Anthococcus, Filippia, Myzolecanium and Physokermes, sclerotised convex pores are present throughout much of the dorsum; as preopercular pores are absent in these genera, these pores may merely represent widely distributed preopercular pores. Small pores, rather similar to ventral microducts but lacking the inner skirt-like gland, are also found in a number of genera (e.g., Cyphococcus, Cribrolecanium, Filippia, Halococcus and Metaceronema). In the Cardiococcinae, the wax joining the sutures between the plates of the glassy test is probably secreted by the pores which generally occur either in lines along the margin and longitudinally down the centre of the dorsum or in a reticulate pattern; these pores may have a rather specialised structure, as in Antandroya and Dicyphococcus.

Cribriform plates (Figs 1.1.3.1.4) This term is used for groups of similar pores enclosed in a sclerotised plate. Such plates are typical of a number of genera from diverse subfamilies and are, therefore, unlikely to all be homologous. Their function is unclear but they are thought to secrete the woolly test in Eutaxia and Stictolecanium. In the Myzolecaniinae, typical cribriform plates are present in several genera, whilst in others (e.g., in Houardia) there are loose groups of pores without any associated sclerotisation and these could be incipient cribriform plates. Cribriform plates can vary considerably in size, even within the same individual (as in Halococcusformicarii Takahashi) and a more complex terminology has been used by Qin and Gullan (1989) to describe their range in structure.

Microtubular ducts (Fig. 1.1.3.1.5) Within the Coccidae, these ducts are restricted to the Cyphococcinae. It is here considered that it is unlikely that they are homologous with the microtubular ducts in the Eriococcidae, although they have a similar basic structure. Each duct has a long, membranous outer ductule, 10-20#m long, which tends to be oval in cross-section, and which has a sclerotised base, constricted across the narrow part, even making it 8shaped. From this basal area a short, thin inner filament arises. The dorsum of the Cyphococcinae is divided into a median area, which has only very few minute pores and no ducts and setae, and a lateral area in which these structures are frequent. Microtubular ducts are restricted to the lateral areas but are most abundant in the sinuous line of pores and setae separating the lateral areas from the median area covered by the glassy test. It is likely that this test is secreted by the microtubular ducts.

Section 1.1.3.1 references, p. 136

Systematics

122

MICROTUBULAR

TUBULAR DUCTS T3

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M2

~

:~' 5 = 0; 4 or 5 = 1; 3 = 2; 2 or less = 3 21. Labial seta: n u m b e r (pairs): > 9 = 0; 6 to 8 = 1; 4 or 5 = 2; 3 or less = 3 Adult female: 22. Instars: number: 4 = 0; 3 = 1 23. Ovisac/test: dorsal woolly cover = 0; woolly test ventral only = 1; waxy = 2; glassy = 3; absent = 4 24. Dorsal derm: m e m b r a n o u s = 0; partially or completely sclerotised = 1 25. Dorsal tubular ducts: absent = 0; present = 1 26. Microtubular ducts: absent = 0; present = 1 27. Eyespots: near base of antenna = 0; far from antenna on venter = 1 ; far from antenna on margin = 2; far from antenna on dorsum = 3; absent = 4 28. Anal tieR: absent = 0; present = 1 29. N u m b e r o f anal plates derived from anal lobes: 0 = 0; 1 = 1; 2 = 2 30. Anal lobes: small, m e m b r a n o u s = 0; absent = 1; distinctly protruding, m e m b r a n o u s = 2; distinctly protruding, sclerotised = 3; withdrawn as anal plates = 4 31. Anal lobe setae: present including those on anal plates = 0; absent = 1 32. M e d i a n plate (arch plate): absent = 0; present = 1 33. Marginal setae: without clearly differentiated marginal setae = 0; differentiated = 1 34. Stigmatic spines: absent = 0; present = 1 35. Spiracular disc-pore rows: absent = 0; in or very near peritreme only = 1; incomplete, forming group rather than row = 2; complete and distinct = 3 36. Multilocular disc-pore distribution: dorsal and ventral surfaces = 0; absent = 1; ventral surface = 2 37. Ventral pregenital disc-pores: head, thorax and abdomen = 0; thorax and a b d o m e n = 1; a b d o m e n = 2; absent = 3 38. Ventral microducts: absent = 0; eriococcid-like bilocular (cruciform) = 1; coccid-like sunken = 2 39. T u b u l a r ducts: without invagination = 0; absent = 1; invaginated = 2 40. Legs: well developed = 0; reduced or absent = 1 41. Tibio-tarsal articulation: present, no sclerosis = 0; absent = 1; present, with sclerosis = 2 42. Claw digitules: finely knobbed = 0; dissimilar = 1; broadly knobbed = 2 43. N u m b e r o f antennal segments: 7 or more = 0; 5-6 = 1; 3-4 = 2; 0-2 = 3 44. Antennal fleshy setae: present on more than terminal segment = 0; differentiated on terminal segment only = 1 45. Body segmentation: distinct dorsally and ventrally = 0; distinct ventrally on abdomen only = 1; absent = 2 46. Translucent pores on hind legs: present = 0; absent = 1 Adult male: 47. Body: size large, > 2 3 0 0 m # = 0; intermediate = 1; small, ( < 1620m#) = 2 48. Head in lateral view: rounded = 0; dorsoventrally elongated = 1; flattened = 2 49. Head with anterodorsal bulge: absent = 0; present = 1. 50. Postoccipital ridge/suture: present = 0; absent = 1 51. Median crest: no reticulations = 0; polygonal reticulations = 1

Phylogeny

247 52. 53. 54. 55.

Interocular ridge: absent = 0; present = 1 Postocular ridge: dorsally weak = 0; intermediate = 1; strong = 2 Midcranial ridge ventrally; laterally sclerotised = 0; reticulated and sclerotised = 1; reticulated = 2 Preocular ridge: ventrally short not attaining midcranial ridge = 0; intermediate = 1; ventrally reaching or nearly reaching midcranial ridge = 2 56. Ocular sclerite dorsally: sclerotised throughout = 0; only sclerotised around eye = 1 57. Ocelli/larval eyes: present = 0; absent = 1 58. Cranial apophysis: s h o r t = 0 ; intermediate = 1; long = 2 65. Genae: unsclerotised = 0; sclerotised and reticulated = 1; sclerotised = 2 60. Dorsal head fleshy setae: present = 0; absent = 1 61. Dorsal ocular setae: absent = 0; present = 1 62. Ventral head fleshy setae: present = 0; absent = 1 63. Ventral setae present between or behind ventral eyes: present = 0; absent = 1 64. Genal setae: present = 0; absent = 1 65. Antennae: 3rd segment longer than apical segment = 0; 3rd segment equal to or shorter than apical segment = 1 66. Antennae: terminal segment cylindrical = 0; barrel shaped = 1; apically constricted = 2 67. Antennae: number of setae on pedicel: abundant ( > 7) = 0; few ( < 7 ) = 1 68. Posttergital setae: present = 0; absent = 1 69. Poststernal fleshy setae: present = 0; not fleshy = 1 70. Prescutum reticulation: absent or very weak = 0; distinct = 1 71. Scutum membranous area: absent = 0; present = 1 72. Scutum: length o f membranous area: less than twice width of membranous area = 0; twice width o f membranous area = 1 73. Scutellum: rectangular without foramen = 0; rectangular with foramen = 1; tubular = 2 74. Metathoracic furca: short (not reaching point where precoxal and marginal ridge meet) = 0; long = 1 75. Basalarr joining pleural wing process to metepisternum = 0; not so = 1 76. Basistcrnum: length in relation to length of membranous area of scutum: less than 2x as long = 0; more than 2x as long = 1 77. Basisternum median ridge: absent = 0; present = 1 78. Metasternal apophysis: present = 0; absent = 1 79. Scutal setae: number of hair-like setae: 5-30 = 0; 1-4 = 1; absent = 2 80. Suspensorial sclerite: present = 0; absent = 1 81. Metapleural ridge: not reduced = 0; reduced = 1 82. Dorsospiracular fleshy setae: absent = 0; present = 1 83. Antemetaspiracular setae: absent = 0; present = 1 84. Posterior metasternal setae: fleshy setae < 4 = 0; > 4 = 1 85. F o r e w i n g alar setae: present = 0; absent = 1 86. Hindwings: present = 0; absent = 1 87. Tibial apical spurs: 2 = 0; 1 = 1; absent = 2 88. Claw denticle: absent = 0; present = 1 89. Tergites between segments I and II: separate sclerites on each side = 0; continuous from side to side = 1; absent = 2 90. Pleurites: absent = 0; on segments IV-VII = 1: on segment VII only = 2 91. VIIlth abdominal sternite: small or absent = 0; two large plates = 1; one large plate = 2 92. Caudal extension of segment VIII: small = 0; prominent and pointed = 1 93. Cicatrix on segment VIII: absent = 0; present = 1 94. Glandular pouch on segment VIII: two separate areas laterally = 0; present as one area medially = 1; absent = 2 95. Glandular pouch setae length: > 4x internal part = 0; without internal part = 1; 3-4x internal part = 2; < 3 x internal part = 3 96. Ante-anal setae: fleshy setae usually absent = 0; fleshy setae present = 1 97. Ante-anal setae: long hair-like setae absent = 0; present = 1 98. Abdominal pleural setae: fleshy setae on segment HI: absent = 0; present = 1 99. Abdominal ventral setae: subequal or fewer than dorsal setae = 0; more numerous than dorsal setae = 1 100. Abdominal ventral setae: fleshy setae: present = 0; absent = 1 101. Apex o f penial sheath: not membranously extended = 0; membranously extended = 1 102. Ratio o f width to length o f p e n i a l sheath: slender ( > 1:4) = 0; thick ( < 1 : 3 ) = 1 103. Penial sheath length to length of body" short, body 5.5x or longer = 0; intermediate, 4.5-5.5x = 1; long, 4.5x or shorter = 2 104. Aedeagus: length to length o f p e n i a l sheath: long, penial sheath < 2 . 8 x longer = 0; short, penial sheath > 3 x longer = 1 105. Aedeagus lateral view: curved = 0; straight = 1

Systematics

248

Appendix 1.1.3.7,C Data matrix for the 24 tam used in the analysis. The numbers indicate the state of each character (see Appendix 1.1.3.7,B); missing or unbknown data are shown as a dash.

C h a r a c t e r no.

10 20 30 1234 56789 01234 56789 01234 56789 01234

Pseudococcidae Cerococcidae Eriococcidae Eriochitonini Lecanodiaspid. Kermesidae Stictococcidae Asterolecaniidae Tachardiidae Aclerdidae Micrococcidae Cardiococcinae Ceroplastinae Cissococcinae Paralecaniini Pulvinariini Coccini Saissetiini Cyphococcinae Eulecaniinae Eriopeltinae Filippiinae Myzolecaniinae Pseudopulvinar.

0000 1100 0100 1201 1102 1210 1111 1102 1101 1112 1102 1212 1212 1112 1102 1202 1202 1112 1212 1102 1202 1212 1212 1112

00000 01003 00002 01002 01003 01002 10010 00001 01001 00111 00112 10113 10103 01113 10113 10113 10113 01103 11103 11113 01103 01103 10103 01101

C h a r a c t e r no.

56789

40 50 60 01234 56789 01234 56789 01234 56789

Pseudococcidae Cerococcidae Eriococcidae Eriochitonini Lecanodiaspid. Kermesidae Stictococcidae Asterolecaniidae Tachardiidae Aclerdidae Micrococcidae Cardiococcinae Ceroplastinae Cissococcinae Paralecaniini Pulvinariini Coccini Saissetiini Cyphococcinae Eulecaniinae Eriopeltinae Filippiinae Myzolecaniinae Pseudopulvinar.

00000 30112 22112 22012 32112 21012 11011 32212 11022 22322 11312 12222 32222 ~2021 32222 32122 32222 32122 32022 32022 32222 32222 30321 10122

00000 00000 00000 20100 21010 11100 30100 10101 11100 42000 10101 11100 30101 21010 22000 30100 10001 11041 10010 10010 21141 00000 21011 33130 31000 20011 32141 21100 20010 22040 32000 20010 220-42011 20010 32-31 42001 20010 32121 42000 1 0 0 - - - 2 - 4 0 4 2 0 0 1 - 0 0 1 0 32-41 42001 20010 32-11 42001 20010 32141 42001 20000 12141 42001 20010 22-30 42001 20010 22-41 40000 20010 32-00 30000 21010 32000 42001 20010 32041 32000 20010 32001

00000 1--03 00010 00000 00000 0--20 00120 1--31 1--21 1--31 01021 01210 02200 110300200 02200 02200 02200 11020 00010 10000 02200 10010 00210

00000 00410 11010 01112 10400 00400 014000400 00401 11411 00202 00212 00312 00402 00312 10212 10212 00212 01412 10212 10412 10-12 00412 00412

00000 20110 20110 40110 00100 20000 11010 00100 41000 40010 40000 40011 40011 40000 40011 40011 40011 40011 40011 40011 40010 40011 40011 40010

00000 00000 00000 00000 00000 10-00 01010 00100 10111 11111 00000 00012 10000 10110 01011 100-0 1 0 0 1 - 0 0 0 - 0 10111 01111 01000 00010 01100 10111 01111 21100 00012 21002 10111 01011 21--0 0--10 0 0 0 - 0 - 0 - 0 0 02100 1-000 10012 01110 10111 01011 21000 01021 20011 10111 10111 1-000 10002 00020 10111 00111 011 . . . . . . . . . . . . . . . . . . . . . . 11110 11001 10012 01000 00010 11010 11022 00011 01000 12010 11-1--101--0-10 101-1--0-0 1 1 2 - - - 1 - 0 1 00--1 00000 020-0 11111 11022 00021 01000 10000 11011 11022 00021 01000 12000 11111 11012 00011 01000 12010 1101--101-20-00 1-011 1--111210 11002 00001 10111 00111 11020 11121 21012 01110 10010 11110 10012 11011 10111 10011 110-- 11022 00021 00000 11010 1121- 10012 200-0 01000 10111

249

Phylogeny

Appendix 1.1.3.7,C (continued)

Character

no.

Pseudococcidae Cerococcidae Eriococcidae Eriochitonini Lecanodiaspid. Kermesidae Stictococcidae Asterolecaniidae Tachardiidae Aclerdidae Micrococcidae Cardiococcinae Ceroplastinae Cissococcinae Paralecaniini Pulvinariini Coccini Saissetiini Cyphococcinae Eulecaniinae Eriopeltinae Filippiinae Myzolecaniinae Pseudopulvinar.

70 80 90 100 01234 56789 01234 56789 01234 56789 01234 5

00000 00000 00000 00000 00000 00000 00000 0 01001 01101 1 1 0 0 0 - 1 1 1 2 02002 -0000 10100 0 00-11 0-001 00000 00200 01000 00000 10100 0 0 0 - 1 1 - 0 1 0 2 00000 00210 02001 00000 1 0 1 0 0 01010 00010 11100 10112 02000 10000 10020 1 01010 00002 00001 10211 12000 00001 10100 0 1 1 - 2 1 - 0 0 0 0 111-1 11001 00000 00000 1 0 0 2 0 0 1 0 1 0 - 0 0 1 2 01000 11202 02002 10000 11000 0 11101 01111 00000 01011 02000 00001 10020 0 01011-0102-1000 11101 00002 10000 10100 1 .................................... 01010 00010 11111 11110 12002 00001 00010 1 11020 11110 11111 11110 22112 21011 01021 1 01011-0002-00-1-011--20-0-0-01-00-0 1 01000 -01-1 1-001 -110- --001 ---0- 011-1 1 11120 11110 11111 11110 22112 31111 01011 1 11120 11110 11111 11110 22112 00111 01011 1 11121 11110 11111 11110 22112 31111 00021 1 11011 -01-2 11000 11-1- 02000 --00- 0 0 0 2 - 01011 01112 00000 00110 02002 30111 10020 1 01021 00112 11011 11110 02002 01001 00011 1 11121 01110 00010 10110 02002 30111 10000 1 1 1 0 2 0 - 0 1 1 0 11001 11112 02002 10101 0 - 0 0 - 0 1 1 2 1 - 1 1 1 2 11101 10112 02000 00001 00020 1

Systematics

250 APPENDIX 1.1.3.7,D. Character state changes

Internode 46 Character 2: change from 0-1; 10: 0-3; 15: 0-1; 20: 0-1; 21: 0-1; 35: 0-2; 38: 0-1; 39: 0-2; 53: 0-1; 55: 0-2; 60: 0-1; 62: 0-1; 63: 0-1; 68: 0-1; 69: 0-1; 73: 0-1; 79: 0-2; 91: 0-2; 101: 0-1. Internode 45 9: 0-2; 17: 0-1; 19: 0-1; 22: 0-1; 26: 0-1; 28: 0-1; 32: 0-1; 33: 0-1; 36: 0-2; 66: 0-1; 74: 0-1; 87: 0-2; 102: 0-1. Internode 44 1: 0-1; 23: 0-4; 24: 0-1; 27: 0-4; 36: 0-1; 43: 0-2; 45: 0-2; 46: 0-1; 71: 0-1; 85: 0-1; 89: 0-1. Internode 43 4: 0-1; 18: 0-1; 20: 1-2; 22: 0-1; 35: 2-1; 67: 0-1; 74: 0-1; 86: 0-1. Internode 42 9: 0-1; 15: 1-2; 21: 1-2; 30: 2-4; 40: 0-1; 44: 0-1; 58: 0-1; 64: 0-1; 78: 0-1. Internode 41 4: 1-2; 24: 1-0; 81: 0-1; 87: 0-1. Internode 40 7: 0-1; 8: 0-1; 11: 0-2; 22: 1-0; 29; 0-2. Internode 39 3: 0-1; 28: 0-1; 33: 0-1; 36: 1-2; 38: 1-2; 45: 0-1; 50: 0-1; 77: 0-1; 105: 0-1. Internode 38 6: 0-1; 9: 1-3; 10: 3-4; 35: 1-3; 44: 1-3; 48: 0-1; 51: 0-I; 88: 0-1; 89: 1-0; 99: 0-1. Internode 37 81: 1-0; 86: 1-0. Internode 36 25: 0-1; 34: 0-1; 40: 1-0; 59: 0-1; 76: 0-1; 94: 0-2; 95: 0-3; 97: 0-1; 98: 0-1. Internode 35 8: 1-0; 55: 0-2; 62: 1-0; 65: 0-1; 80: 0-1; 100: 1-0; 103: 0-2. Internode 34 20: 2-3; 60: 1-0; 61: 0-1; 64: 1-0; 73: 1-2; 84: 0-1. Internode 33 2: 1-2; 37: 0-2; 53: 1-2; 67: 1-0; 69: 1-0; 94: 0-2; 104: 0-2. Internode 32 5: 0-1; 6: 1-0; 14: 0-1; 24: 0-1; 34: 0-1; 55: 2-0; 59: 0-1; 63: 1-0; 74: 1-0; 79: 2-0. Internode 31 40: 1-0; 42: 0-1. Internode 30 22: 0-1; 41: 0-2; 66: 0-2; 70: 0-1; 75: 0-1; 76: 0-1; 82: 0-1; 83: 0-1; 90: 0-2; 92: 0-1; 93: 0-1; 96: 0-1; 98: 0-1. Internode 29 27: 2-4; 49: 0-1; 72: 0-1; 97: 0-1. Internode 28 3: 1-0; 8: 0-1; 25: 0-1; 58: 1-2; 68: 1-0; I01: 0-1; 103: 1-0. Internode 27 8: 0-1; 53: 2-0; 54: 2-1; 65: 1-0. Intemode 26 16: 0-1; 30: 4-0; 32: 0-1; 35: 1-3; 36: 1-2; 43: 2-3; 57: 0-1; 66: 0-1; 89: 1-2; 95: 0-1. Internode 25 6: 0-1; 9: 1-3; 12: 0-1; 37: 0-1; 54: 2-0; 58: 1-0; 80: 0-1; 88: 0-1.

Soft Scale Insects Their Biology, Natural Enemies and Control Y. Ben-Dov and C.J. Hodgson (Editors) 1997 Elsevier Science B.V. -

251

Chapter 1.2 Biology 1.2.1.1 General Life History SALVATORE MAROTTA

INTRODUCTION The adult females of all soft scales, as in all other families of Coccoidea, are neotenic, reaching the adult stage after two or three moults, through metamorphosis of the heterometabola - paurametabola type. On the other hand, the postembryonic development of the male is essentially similar to the complete metamorphosis of the holometabolous insect orders (Bodenheimer and Harpaz, 1951) and is classified within the neometabola type. The adult male generally develops through two nymphal instars, followed by sessile prepupa and pupa stages and then, after moulting for the fourth time, becomes an active adult. However, extra nymphal instars have been recorded for the male of Ceroplastes sinensis Del Guercio (Snowball, 1970), Filippiafollicularis Targioni Tozzetti (Quaglia and Raspi, 1982a, 1982b) and for Lichtensia viburni Signoret (Pellizzari Scaltriti, 1982). Although these latter observations need further investigation, it is not impossible that extra instars may be discovered in other species. The terms used here (Fig. 1.2.1.1.1) to define the developmental stages of the female are: lst-instar nymph or crawler, 2nd- and 3rd-instar nymph (where the latter are present) and adult; whilst for the males: lst-instar nymph or crawler, 2nd-instar nymph, prepupa, pupa and adult. The term larva, although often utilized for the young stages, appears incorrect because it refers to insects with holometabolic postembryonic growth.

FIRST-INSTAR NYMPH OR CRAWLER The crawlers of soft scales do not appear to be sexually differentiated morphologically. This is generally the most active stage and is responsible for both active and passive dispersal and ultimately for the selection of the feeding site on the appropriate host plant (see Section 1.3.3). However, even within the short time usually spent as a crawler, different periods of behaviour can be differentiated. Upon hatching, the crawler remains motionless for a short time under the body of the adult female or in the ovisac. The duration of this torpid period is affected by environmental conditions, mainly temperature, and may last from only a few minutes to several hours or even days. Once the crawlers emerge from beneath the parental 'brood chamber' or from the ovisac, they are very active. This activity is affected by at least three groups of factors: (i) innate behaviour patterns which initiate wandering; (ii) the availability of suitable settling sites, and (iii) the ambient environmental conditions, such as illumination, temperature, relative humidity and wind velocity (Hoelscher, 1967; Beardsley and Gonzalez, 1975; Washburn and Washburn, 1984). This dispersal phase may last from

Section 1.2.1.1 references, p. 255

252

Biology

several hours to several days, but settling generally occurs within about a metre from the mother. This dispersal is influenced mainly by temperature; crawlers are most active between 21 and 32~ with a lower threshold of about 10-13~ and an upper lethal threshold of about 42 oC. However, other dominant cues for dispersal involve phototaxic and geotaxic responses (Beardsley and Gonz~les, 1975) which facilitate location of feeding sites over host surfaces (see Section 1.3.3). Selection of an appropriate feeding site is critical for subsequent development. Mortality is generally highest during the 1st instar and failure to settle is considered to be one of the major mortality factors for many species (Beardsley and Gonzdles, 1975; Podoler et al., 1979; Washburn and Washburn, 1984). Once settled, the nymph inserts its stylets into the plant tissue and commences feeding from the phloem. Although the lst-instar nymph does not usually move again once it has settled, subsequent instars may wander and select different feeding sites (see below). Once it is fully grown, the crawler stops feeding and undergoes its first moult. According to Annecke (1966), two phases are observable in the moulting process: (i) an initial change in body colour, particularly around the body margins, followed by (ii) contractile motions and the gradual extrusion of the exuviae. Crawlers appear to lack a waxy cover or test and are, therefore, the stage most susceptible to such environmental factors as high temperature, low humidity, wind, rainfall or combinations of these, and these are the main causes of high mortality at the crawler stage. In addition, this is also the most susceptible stage to the lethal effect of chemical insecticides.

SUBSEQUENT IMMATURE INSTARS Metamorphosis is significantly different in males and females. In females, the body of the 2nd instar increases in size and fmally undergoes a second moult. In those species which have only two nymphal instars, this moult gives rise to the adult and certain features appear, namely the genital aperture and a modified integumentary secretory system. When a third nymphal instar is present, it is generally very similar to the adult female but smaller and lacks the above two adult characters. In univoltine species which overwinter as the 2nd instar but spend the summer on the hosts' leaves, the 2nd-instar nymphs migrate to the woody parts of the plant prior to leaf fall in the autumn. The number of moults in the female life cycle has only been studied in rather few species. Even so, there are conflicting observations. Thus, for Sphaerolecanium prunastri (Fonscolombe), Silvestri (1939) considered there were only two instars whereas Ben-Dov (1968) found three; with Coccus hesperidum Linnaeus, Saakyan-Baranova (1964) and Annecke (1966) found there were two, whereas Y. Ben-Dov (unpublished observations) studied mounted material of C. hesperidum and C. capparidis (both in Israel) and found three nymphal instars. Bodenheimer (1935) found only two instars for Ceroplastesfloridensis Comstock, whereas Amitai (1969) and Ben-Dov (1970) recorded three. The duration of the third instar is usually very short (two to four days) and its occurrence seems likely to have been overlooked in some species. The 2nd instars of males are often gregarious and congregate in large clusters on the branches or twigs where they secrete a test or cover which encloses all the subsequent instars, i.e. the third (prepupal) and fourth (pupal) instars and the adult stage. This test or cover is glued to the surface of the plant and is composed of thin glassy wax, which is often rather fiat and translucent and is frequently divided into central and lateral plates by sutures (see Section 1.1.2.4). The 2nd-instar nymphs of males do not grow nearly as much as those of the female and are usually easily distinguished morphologically. Towards the end of the 2nd instar, the nymphs become elongated and show the beginnings of eye pigmentation. The second moult in males gives the prepupa, which has the first signs of dorsal and ventral eyes, wing-buds (in species with winged males) and a short penial sheath. They also have

General life history

253

rather short legs and antennae and lack functional mouthparts. No further feeMing takes place in the prepupa.

B

A

B1

A1 " [ ~ ~ ,

/

J

',, .

. /9

r r

1

/

#

.

.

'~

"

"z.:

As

B

~'~

A6

A7

Fig. 1.2.1.1.1. Diagram showing the life-stages of A. Parthenolecanium corni and B. Ceroplastes japonicus, where Az - 1st instar nymph, A 2 - 2nd instar female nymph, A 3 - adult female, A4 - 2nd-instar male nymph, A s - prepupa, A~ - pupa and A 7 - adult male; B ! - 1st instar nymph, 132 - 2nd instar female nymph, B a - 3rd-instar female nymph, B4 - adult female. AI,A2 after Kawecki (1958), A3 after Williams and Kosztarab (1972); A,, A, and A 7 after Danzig (1980); B t, B 2 and B~ after Camporese and Pellizzari (1994) and B4 after Pellizzari and Camporese (1994); A4 is modified from A2.

254

Biology The third moult gives rise to the pupa, which is similar to the prepupa but the legs, antennae and wings (when present) are much more developed and better defined. In addition, the penial sheath is more elongate and triangular. The pupa also remains beneath the test. The adult male appears after the last moult but remains beneath the waxy test until fully developed, when it backs out from beneath the test and begins to actively search for females. Adult males are elongate, with a distinct neck region, well-developed legs and antennae and may be either winged or wingless. When winged, only the fore-wings are present. The head is sclerotised, with two to five pairs of simple eyes and usually with a pair of lateral ocelli. Being devoid of mouthparts, the adult males only live from between a few hours to about a week.

ADULT FEMALE The adult females of all soft scales possess mouthparts and feed by imbibing phloem sap. After the last moult and prior to oviposition, the adult females of most species increase in size and volume; this increase in volume may be as great as 6 times (e.g., in Parthenolecanium corni (Bouchr) (Habib, 1957)). During this growth phase, several stages can be identified (these are often also present in earlier instars, but are less marked). These stages run into each other.

a. Period of size increase. The body size increases gradually, mainly in length, e.g., Parthenolecanium corni (Bouchr) (Habib, 1957), Toumeyella pinicola Ferris (Kattoulas and Koheler, 1965), Coccus hesperidum Linnaeus (Annecke, 1966) and Pulvinariella mesembryanthemi (Vallot) (Washburn and Frankie, 1985). The size, shape and volume of the adult female of a given species can be highly variable, and this can be due to changes caused by the actual host plant (e.g., in P. corni (Ebeling, 1938)) and also to the choice of settling and feexling sites (leaf surface, branches, forks between twigs and buds, proximity of leaf veins, etc.). b. Change in body colour. Associated with the size increase, the body changes colour, generally becoming darker due to the dorsum becoming sclerotised with age. On the dorsal tegument, new pigmented areas may appear, which in some species are very conspicuous and distinctive, as in Eulecanium tiliae (Linnaeus). In addition, other characteristic features may appear, such as striations, areas of wax secretions, etc. c. Dorsoventral swelling of the body. When the female has completed the period of size increase, the dorsum becomes convex - in some species remarkably so. This convexity is correlated with the development of ovaries, the accumulation of ovarian eggs and also with the formation of the brood chamber. d. Formation of the brood chamber or ovisac. In several subfamilies within the Coccidae (Ceroplastinae, Coccinae (tribes Coccini, Paralecaniini and Saissetiini), Eulecaniinae and Myzolecaniinae) the eggs are deposited beneath the female body under the venter, within a space referred to as the 'brood chamber'. This chamber is formed by the progressive development of a cavity beneath the abdomen just prior to and during oviposition. By the time oviposition has been completed, the abdomen has become so shrtmken through the loss of eggs that the venter may touch the dorsum, with the entire cavity beneath filled with eggs. The sclerotised body overlaying the brood chamber then forms a protective shield for the eggs and lst-instar nymphs. In some genera, e.g., Physokermes Targioni Tozzetti and

General life history

255

Rhodococcus Borchsenius, the structure of the brood chamber resembles that of the Kermesidae (see Bullington and Kosztarab, 1985). Species in the subfamilies Filippiinae and Eriopeltinae and in the tribe Pulvinariini (subfamily Coccinae) lay their eggs in a white ovisac, formed of long, waxy filaments se~:reted by ventral wax glands (see Section 1.1.2.7). These ovisacs are felt-like or cottony and are located behind or beneath the body. In some species, such as Eriopeltis festucae (Fonscolombe), the ovisac completely encloses the body of the adult female, but in others, such as those in the genus Pulvinaria Targioni Tozzetti, the ovisac lies entirely beneath the body, often forcing the adult to withdraw its stylets and move forward as it oviposits. Other subfamilies, such as the Cardiococcinae and Cyphococcinae, secrete a translucent wax test and the body of the adult female shrivels into the anterior end whilst ovipositing, so that the glassy test then forms the protective brood chamber.

EGG Generally the eggs are uniformly covered with wax filaments secreted from the ventral tubular ducts and multilocular disc-pores (Tamaki et al., 1969; Gerson, 1980; see also Section 1.1.2.7). According to Tamaki et al. (1969) and Hamon et al. (1975), the presence of the wax filaments prevents the eggs from desiccating and from sticking together. The number of eggs per female varies enormously both between and even within species. The average fecundity is affected by temperature, the density of the scales, the size of the adult females and the species and edaphic conditions of the host plant. Usually the number of eggs is proportional to the size of the female body and so varies from a few dozens or hundreds to several thousand. For example, Kawecki (1958) found that small specimens of P. corni produced about 150 eggs while big individuals oviposited more than 5,000. Likewise, Podoler et al. (1981) found that the number of eggs produced by Ceroplastesfloridensis (Comstock) ranged from 52 to 1329 per female in the spring generation, as compared with 84 to 409 in the autumn generation.

REFERENCES Amitai, S., 1969. Morphological identifications of the stages of the Florida wax scale, Ceroplastesfloridensis Comst. (Coccoidea). Israel Journal of Entomology 4: 89-95. Annecke, D.P., 1966. Biological studies on the immature stages of soft brown scale, Coccus hesperidum Linnaeus (Homoptera: Coccidae). South African Journal of Agriculture Sciences, 9: 205-228. Beardsley, J.W. and Gonz~iles, R.H., 1975. The biology and ecology of armored scales. Annual Review of Entomology, 20: 47-73. Ben-Dov, Y., 1968. Occurrence of Sphaerolecanium prunastri (Fonscolombe) in Israel and description of its hitherto unknown third larval instar. Annales des Epiphyties, 19" 615-621. Ben-Dov, Y., 1970. A redescription of the Florida wax scale Ceroplastesfloridensis Comstock (Homoptera: Coccidae). Journal of the Entomological Society of Southern Africa, 33: 273-277. Bodenheimer, F.S., 1935. Studies on the zoogeography and ecology of palearctic Coccidae. I-1II. EOS, 10: 237-271. Bodenheimer, F.S. and Harpaz, A., 1951. Holometabolic development in the males of Coccoidea. Bulletin of the Research Council of Israel, 1 (3): 133-135. Bullington, S.W. and Kosztarab, M., 1985. Revision of the family Kermesidae (Homoptera) in the Nearctic region based on adult and third instar females. Virginia Polytechnic Institute and State University, Agricultural Experiment Station, Bulletin 85-11 : 1-118. Camporese, P. and Pellizzari, G., 1994. Description of the immature stages of Ceroplastes japonicus Green (Homoptera: Coccoidea). Bollettino di Zoologia Agraria e Bachicoltura, Ser. H, 26: 49-58. Danzig, E.M., 1980. Coccoids of the Far east of USSR, with a phylogenetic analysis of the Coccoid fauna of the world. Nauka, Leningrad, 366 pp. (In Russian). Ebeling, W., 1938. Host-determined morphological variations in Lecanium corni. Hilgardia, 11:613-631. Gerson, U., 1980. Wax filaments on coccoid eggs. Israel Journal of Entomology, 14: 81-85. Habib, A., 1957. The morphology and biometry of the Eulecanium corni group, and its relation to hostplants. Bulletin de la Soci~t~ Entomologique d'Egypte, 41: 381-410.

256

Biology Hamon, A.B., Lambdin, P.L. and Kosztarab, M., 1975. Eggs and wax secretion of Kermes kingi. Annals of the Entomological Society of America, 68:1077-1078. Hoelscher, C.E., 1967. Wind dispersal of brown soft scale crawlers, Coccus hesperidum (Homoptera: Coccidae), and Texas citrus mites, Eutetranychus banksi (Acarina: Tetranychidae) from Texas citrus. Annals of the Entomological Society of America, 60 0): 673-678. Kattoulas, M.E. and Koheler, C.S., 1965. Studies on the biology of the irregular pine scale. Journal of Economic Entomology, 58 (4)" 727-730. Kawecki, Z., 1958. Studies on the genus Lecanium Burro. IV. Materials to a monograph of the brown scale Lecanium corni Bouch6 (Homoptera: Coccoidea: Lecaniidae). Annales Zoologici, 4 (9): 135-230. Pellizzari Scaltriti, G., 1982. Osservazioni biologiche sulla Euphilippia olivina Berl. & Silv. nel Veneto. Memorie della Societ~ Entomologica ltaliana, (1981), 60: 289-297. Pellizzari, G. and Camporese, P., 1994. The Ceroplastes species (Homoptera" Coccoidea) of the Mediterranean basin with emphasis on C. japonicus Green. Annales de la Socirt6 Entomologique de France (N.S.), 30: 175-192. Podoler, H.I., Bar-Zacay, R. and Rosen, D., 1979. Population dynamics of the Mediterranean black scale, Saissetia oleae (Olivier), on citrus in Israel. 1. A partial life table. Journal of Entomological Society of Southern Africa, 42: 257-266. Podoler, H.I., Dreishpoun, Y. and Rosen, D., 1981. Population dynamics of the Florida wax scale, Ceroplo~tesfloridensis (Homoptera: Coccidae) on citrus in Israel. 1. A partial life table. Acta Oecologica, Oecologia applicata, 2(1): 81-91. Quaglia, F. and Raspi, A., 1982a. Osservazioni eco-etologiche su un lecaniide dannoso all'olive in Toscana: Euphilippia olivina Berlese e Silvestri (Rhynchota, Coccoidea). Frustula Entomologica, (1979), nuova serie, 2(15): 85-112. Quaglia, F. and Raspi, A., 1982b. Note eco-etologiche sulla Philippia oleae (O.G. Costa) infeudato sull'olivo in Toscana. Frustula Entomologica, (1979), nuova serie, 2 (15): 197-229. Saakyan-Baranova, A.A., 1964. On the biology of the soR scale Coccus hesperidum L. (Homoptera: Coccoidea). Entomologicheskoe Obozrenye, 43: 268-296. Silvestri, F., 1939. Compendio di Entomologia Applicata (Agraria, Forestale, Medica, Veterinaria). Parte speciale, Tipografia Bellavista, Portici, Vol. 1(1-2): 974 pp. Snowball, G.J., 1970. Ceroplastes sinensis Del Guercio (Homoptera: Coccidae), a wax scale new to Australia. Journal of Australian Entomological Society, 9: 57-64. Tamaki, Y., Yushima, T. and Kawai, S., 1969. Wax secretion in a scale insect, Ceroplastes pseudoceriferus Green (Homoptera: Coccidae). Applied Entomology and Zoology, 4: 126-134. Washburn, J.O. and Frankie, G.W., 1985. Biological studies of iceplant scales, PulvinarieUa mesembryanthemi and Pulvinaria delottoi (Homoptera: Coccidae), in California. Hilgardia, 53 (2): 1-27. Washburn, J.O. and Washburn, L., 1984. Active aerial dispersal of minute wingless arthropods: exploitation of boundary-layer velocity gradients. Science, 223: 1088-1089. Williams, M.L. and Kosztarab, M., 1972. Morphology and systematics of the Coccidae of Virginia, with notes on their biology (Homoptera: Coccoidea). The insects of Virginia, No. 5. Virginia Polytechnic Institute and State University, Research Division Bulletin, 74: i-viii + 1-215.

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1.2.1.2 Embryonic Development; Oviparity and Viviparity ERMENEGILDO TREMBLAY

EMBRYONIC DEVELOPMENT The mature oocyte in members of the family Coccidae is very similar to that noted in the Diaspididae (Koteja, 1990). Indeed, even the so-called "Krassilstschick cell', which was considered to be typical of the pedicel of diaspidid ovarioles, has also now been shown to be present in the Coccidae. The spermathecae are usually well developed (De Marzo et al., 1990) and, in Sphaerolecanium prunastri (Fonscolombe), were found to contain sperm bundles and free spermatozoa (Tremblay, 1961). Oogenesis, the production of polar bodies and fertilization were also studied in this species and were found not to differ from those known for diaspidoids. The first synchronic and asynchronic divisions of the zygotic nucleus and its derivatives (cleavage nuclei) lead to the formation of the blastoderm and vitelline or yolk nuclei (Fig. 1.2.1.2.1,A). The latter are cleavage nuclei, which are surrounded by a dense cytoplasm, and which remain in the yolk mass when the cleavage nuclei migrate towards the periphery of the egg to give rise to the blastoderm. At the same time, some cells at the posterior egg pole tend to form a group rather than arranging themselves in the single blastoderm layer. These cells are the first "germ cells" which appear in coccids (as in the diaspidids) at the posterior egg pole when the invagination, which gives rise to the embryo, starts. Once the germ cells, i.e. the primordial gonads, have appeared, they show some peculiar characters which allow them to be easily distinguished from blastoderm cells. In species of Pulvinaria, Saissetia, Coccus and Parthenolecanium, Teodoro (1916, 1921) observed the first germ cells as round cells with a chromatin-rich nucleus in the caudal tract of the invaginating germ band, although in S. prunastri, Tremblay (1961) observed them in the early blastoderm stage, even before the start of polar proliferation which precedes the invagination process, when they appeared as larger and less chromophilous cells than the blastoderm cells. This dissimilarity between the observations of Teodoro and Tremblay in the apparent structure of the germ cells is probably due to the different histological procedures; this may also account for the difference in the time of their detection in early embryos. Circumstantial evidence, however, is in favour of their very precocious appearance, which should closely coincide with blastoderm formation. The differentiation of the germ band, which leads to the first appearance of the embryo proper and of the amnion and superficial extraembryonic envelope (serosa), starts with a cellular proliferation which takes place in the blastoderm wall, located at the posterior egg pole. This proliferation produces a polycellular layer which corresponds to the wellknown "ventral plate" of the classical embryonic scheme, whose name is indicative of its typical ventral position. This original position is found in margarodids (e.g., Icerya

Section 1.2.1.2 references, p. 260

258

BioloEg,

spp.) and diaspidoids (e.g., species of Quadraspidiotus and Pseudaulacaspis) but not in those Coccidae so far examined, in which the cellular proliferation starts in a position clearly polar (Fig. 1.2.1.2.1, B,C). The invagination process (anatrepsis) which follows proceeds towards the anterior egg pole and produces the usual bilayered band (Fig. 1.2.1.2.1,D).

Fig. 1.2.1.2.1. A - T h e blastoderm stage ofPulvinaria v/t/s (L.): b, blastoderm; y, yolk; vu, vitelline nuclei. B, C - Two consecutive stages of the invagination process in P. v/t/s, leading to the formation of the germ band. D - An early embryo of Saissetia oleae (Olivier): a, amnion; g, germ band: s, serosa. E - An embryo of Coccus hesperidum L. showing the amniotic cavity (ar in which sections of antennal, buccal and locomotory rudiments are visible. In none of the sections shown in this figure are germ cells represented (atier Teodoro, 1916, 1921).

At first, the two cellular layers of this invagination appear identical in histological sections, but they quickly evolve into a thicker layer (the germ band) and a thinner layer (the amnion). The distinction between the two layers becomes more evident as the invagination proceeds because, in contrast to the active proliferation of the cells of the germ band, the amniotic cells rapidly become flattened due to their less intensive division. The same flattening process occurs in the superficial extraembryonic

Embryonic development; oviparity and viviparity

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blastoderm which, thus, evolves into the outer serosal membrane enveloping the yolk, surrounded by its vitelline membrane and the invaginating band. The germ band represents the early embryo (Fig. 1.2.1.2.1,E), which is thus formed with its cephalic parts downwards or, in other words, emerging from the polar blastoderm, and with its abdominal region directed towards the anterior egg pole. As anatrepsis proceeds, the embryo undergoes a torsion which is typical of all Coccoidea and which makes it difficult to obtain a complete view in histological sections as compared with complete preparations. With the evolution of the germ band into the segmented embryo and of the amnion as an internal membrane facing its ventral side, the thin fissure separating the two original layers becomes the amniotic cavity. The first description of the differentiation of the mesoderm as a thin layer all along the germ band was given by Teodoro (1916) for Pulvinaria vitis (L.). The mesoderm layer is produced when anatrepsis has completed the first curve, soon after the germ band has reached the anterior egg pole. In sections, it rapidly looses its linear aspect and evolves into a dozen groups or masses of cells, as in other insects. At this stage, groups of degenerating nuclei, named "paracytes", were described by Strindberg (1919) in front of the invaginating germ band before it reached the anterior egg pole. The cells to which these nuclei belonged were considered to be derivatives of the amniotic layer but no suggestions were made as to their significance. Anatrepsis finishes with the formation of segments and appendages (metamerization) and the appearance of stomodeal and proctodeal invaginations. This stage is then followed by katatrepsis, i.e. in which the growth of the embryo rapidly changes direction, with its cephalic parts moving towards the anterior egg pole. In this def'mitive position, the ventral side of the embryo with its appendages comes into contact with the chorion, while the dorsal region becomes exposed to the yolk mass. This process is interpreted as an embryonic movement which facilitates the embryogenesis of internal tissues and organs. The studies referred to above were all done prior to the 1960's and since then there has been no further research on soft scale embryogeny and further work in this field is urgently neeAed.

OVIPARITY AND VIVIPARITY

There has been much discussion with regard to the definition of ovoviviparity versus oviparity and viviparity. Koteja (1990) mentions the rather lengthy report by Hagan (1951) on the 19th-century controversy as to whether Coccus hesperidum L. is oviparous or viviparous. In the opinion of the present author, this controversy has been caused by inadequate evaluations as to whether the egg shell (chorion) was present or absent. In fact, the delicate membrane which envelopes the nymphs of some ovoviviparous species when they emerge from the vulva orifice has often been considered an amniotic membrane or even a possible derivative of the serosa (Koteja, 1990). It is here agreeA with Koteja that this thin involucre is not of amniotic origin, since the amnion disappears during early embryogenesis. On the other hand, it is not here accepted that this membrane could be a serosal derivative or some other structure different from a true chorion. On the basis of what is known in other animals, it appears that only in viviparous insects will the chorion be totally lacking as a result of changes associated with this reproductive adaptation. This complete loss happens both when adenotrophic structures have evolved for the nourishment of the embryo and when they are absent (e.g., in viviparous aphids). In contrast, the chorion is always present in oviparous animals, where there is a continuous range of structure, from a robust egg shell to a delicate chorionic membrane. This view, therefore, considers that ovoviviparity is a

Section 1.2.1.2 references, p. 260

Biology

260

form of oviparity because, even when nymphs emerge from the vulva orifice by their own means, the empty egg envelopes remain in the maternal oviduct. In some cases even environmental conditions can induce oviparous females to retain their eggs in the oviduct and thus to shift toward ovoviviparity. In the genus Coccus, the eggs laid by C. pseudomagnoliarum (Kuwana) can hatch after only a few hours but may take up to 3 days (Quayle, 1915; Barbagallo, 1970), while the nymphs of Coccus hesperidum hatch at most 4 hours (usually 2-5 minutes) after deposition (Annecke, 1966). In this latter species, naked nymphs have been seen emerging from the vulva orifice but thin egg shells have been shown to remain in the female genital tract (see Hagan, 1951, for a synthesis of old data). Saakyan-Baranova (1964) reported that the slightest mechanical damage to the eggs, such as by dissecting the sexually mature females of C. hesperidum, caused the egg shells (improperly defined as ovisac by Saakyan-Baranova, 1964) to peel off caudally, leaving the nymph bare. Other known cases of "crawler producing" females in coccids have been reported for two species of Toumeyella, namely T. pinicola Ferris (Kattoulas and Koehler, 1965) and T. liriodendri (Gmelin) (Bums and Douley, 1970), both of which are oviparous but in which this is as close to ovoviviparity as in Coccus hesperidum. In Coccoidea in general, it seems that freshly laid eggs of oviparous species always contain at least a germ band. In this sense, all scale insects are oviparous but with a tendency towards ovoviviparity. Further work, however, is needed to confirm this assumption.

REFERENCES Annecke, D.P., 1966. Biologicalstudies on the immature stages of the soft brown scale, Coccushesperidum Linnaeus (Homoptera Coccidae). South African Journal of Agricultural Science, 9: 205- 228. Barbagallo, S., 1970. Notizie sulla presnza in Sicilia di una nuova Cocciniglia degli agrumi, Coccus pseudomagnoliarum (Kuwana). Entomologica, 10: 121-139. Burns, D.P. and Douley, D.E., 1970. Biology of the tulip tree Scale, Toumeyella liriodendri Gmel. (Homoptera). Annals of the Entomological Society of America, 63: 228-235. De Matzo, L., Romano, V. and Tranfaglia, A., 1990. Types of the female reproductive system in some scale insects (Homoptera: Coccoidea). Proceedingsof the VI InternationalSymposium of Scale linsects Studies, Krakow, Poland, August 1990, 2: 41-46. Hagan, H.R., 1951. Embryology of Viviparous Insects. Ronald Press, New York, 472 pp. Kattoulas, M.E. and Koehler, C.S., 1965. Studies on the biology of the irregular pine scale, Toumeyella pinicola Fen'is. Journal of Economic Entomology, 58: 727-730. Koteja, J., 1990. Embryonic development, ovipary and vivipary. In: D. Rosen (Editor), Armored Scale Insects their Biology, Natural Enemies and Control. Elsevier, Amsterdam, pp. 233- 242. Quayle, H.J., 1915. The citricola scale. University of California Agricultural Experiment Station Bulletin 255: 405-421. Saakyan-Baranova, A.A., 1964. On the biology of the soR scale Coccus hesperidum L. (Homoptera Coccoidea). EntomologicalReview, 43: 135-147. Strindberg, H., 1919. Zur Entwicklungsgeschichte der oviparen Cocciden. Zoologischer Anzeiger 50:113-139. Teodoro, G., 1916. Osservazioni sulla ecologia delle Cocciniglie con speciale riguardo alia morfologia e alia fisiologia di questi insetti. Redia, 11: 129-209. Teodoro, G., 1921. Sulla embriologia delle Cocciniglie. Redia, 14: 137-141. Tremblay, E., 1961. Osservazionisulla cariologia e sulla simbiosi endocellularedi alcuni Coccini. Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', Portici, 19: 215-260.

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261

1.2.1.3 Endosymbionts ERMENEGILDO TREMBLAY

INTRODUCTION The first information on the symbionts of Coccidae was obtained as a by-product of an anatomical study of Coccus hesperidum L. by Leydig (1854), who reported the presence of bodies, around 4 #m long and probably parasitic, in the haemolymph of this common soft scale. The bodies were described as lanceolate-shaped and capable of multiplying by budding at one end. A series of more or less occasional records followed. It is clear from Table 1.2.1.3.1 that some of these early records were rather detailed. One of them (Putnam, 1880) even included the discovery of the hereditary transmission of the symbionts through the eggs of a soft scale. This was long before the symbiotic nature of the association with these microorganisms was ascertained. To the present author's knowledge, the first suggestion that these yeast-like microorganisms were symbiotic must be credited to Conte and Faucheron (1907), more than half a century after the information provided by Leydig. With a good deal of guesswork, even if with great caution, they hypothesised that a mutualistic symbiotic association might exist between these microorganisms and the four species of soft scales investigated by them (see Table 1.2.1.3.1).

MORPHOLOGY OF THE SYMBIONTS

The morphological descriptions of coccid symbionts show little agreement and are sometimes contradictory. The reasons for this discordance can be found in the specificity of the associations and in the variability of the symbionts within each scale species (see below). In addition, a frequent cause of confusion is the misidentification of external contaminants as endosymbionts. Unfortunately, this has happened in almost all cases in which a successful isolation in pure culture of symbionts has been claimed (Table 1.2.1.3.1). The consequence of this frequent mistake is that the only reliable descriptions are those given by zoologists who derived them from histological preparations only (see Teodoro, 1918; Granovsky, 1929; Tremblay, 1961). Also of interest are those given by some experienced microbiologists (Schwartz, 1924, 1932; Steinhaus, 1955). The coccid symbionts can be described as elongate microorganisms, commonly pear-shaped or spindle-shaped, capable of multiplication by terminal budding (Fig. 1.2.1.3.1) and with an average length ofbetween 3 and 10 #m. Depending on the stage and physiological conditions of the host scale, the symbionts often appear roughly rectangular, about 5 #m wide and 30-40 #m long, although sometimes reaching 100/~m in length (Steinhaus, 1955) (see below). Their internal structure shows little uniformity (Fig. 1.2.1.3.1,B,C). The use of several staining techniques reported by early authors (Teodoro, 1918; Buchner, 1921; Granovsky, 1929)provided evidence of refractive granulations and fat vacuoles, but unfortunately histochemical details, as well as ultrastructural studies, are totally lacking.

Section

1.2.1.3 references, p. 266

262

Biology TABLE 1.2.1.3.1 Species of Coccidae for which information on endosymbiosis is available. References denoted with an asterisk * give information on the probable systematic position of the symbiotic microorganisms.

Species

References

Ceroplastes rusci (L.)

Berlese (1906)*.

Chloropulvinaria floccifera (Westwood)

Conte and Faucheron (1907)*; Teodoro (1912).

Chloropulvinaria psidii (Maskell)

Buchner (1921).

Coccus hesperidum L.

Leydig (1854); Moniez (1887); Conte and Faucheron (1907)*; Teodoro (1912); Buchner (1930); Schwartz (1932).

Coccus longulus (Douglas)

Buchner (1912)*.

Eucalymnatus tessellatus (Signoret)

Nur (1972).

Eulecanium kunoense (Kuwana)

Steinhaus (1955).

Eulecanium tiliae (L.)

Tremblay (1961).

Lecanium sp.

Breest (1914).

Neopulvinaria innumerabilis (Rathvon)

Putnam (1880); Brues and Glaser (1921).

Parasaissetia nigra (NietneO

Smith (1944)*; Steinhaus (1951,1955).

Parthenolecanium cerasifex (Fitch)

Nur (1972).

Parthenolecanium corni (Bouch~)

Buchner (1911)*; Brain (1923)*; Schwartz (1924", 1932, 1935), Benedek and Specht (1933)*; Steinhaus (1955).

Parthenolecanium persicae (F.)

Teodoro (1918).

Parthenolecanium putmani (Phillips)

Nut (1972).

Physokermes piceae (Schrank)

Buchner (1912", 1921).

Pulvinariella mesembryanthemi (Vallot)

Targioni Tozzetti (1867); Poisson and Pesson (1939).

Pulvinaria vitis (L.)

Teodoro (1912, 1916).

Saissetia coffeae (Walke0

Conte and Faucheron (1907)*; Buchner (1912", 1921, 1930); Schwartz (1932).

Saissetia oleae (Olivie0

Conte and Faucheron (1907)*; Teodoro (1912); Granovsky (1929)*; Steinhaus (1955).

Sphaerolecanium prunastri (Fonscolombe)

Tremblay (1961).

Endosymbionts

263

THE NATURE OF THE SYMBIONTS T h e small lanceolate-shaped bodies observed in C. hesperidum by Leydig (1854) later became k n o w n as yeast-like symbionts. Those of other Coccid species (e.g., Parthenolecanium corni (Bouch6), Saissetia oleae (Olivier) and Ceroplastes rusci (L.)) w e r e often claimed to have been grown on synthetic media (Table 1.2.1.3.1) and were classified as species of Aureobasidium (= Pullularia, Dematium), Lecaniocola, Torula, Torulopsis, etc. The most believable view is that these bodies are blastospores or sprout

Fig. 1.2.1.3.1. A - Symbionts in the fat body of Neopulvinaria innumerabilis (Rathvon). B - isolated individual symbionts from the fat body of P. innumerabilis. C - Isolated individual symbionts from Sphaerolecanium prunastri (Fonscolombe). D - Wax cell of PulvinarieUa mesembryanthemi (Vallot) containing symbionts. E - Symbiont transmission to the ovarioles ofLecanium sp. F- Symbiont transmission to the ovarioles of Eulecanium n'liae CL.). G - Symbionts localized at the anterior egg pole of E. tiliae. H - Symbionts localized at the anterior egg pole ofLecanium sp. I - Transitory symbiotic organ close to the embryo of Lecanium sp. (After Brues and Glaser (1921); Poisson and Pesson (1939); Breest (1914) and Tremblay (1961)). cells o f Deuteromycotina Hyphomycetes close to Aureobasidium puUulans De Bary (Brues and Glaser, 1921; Schwartz, 1935), which was thus indicated as the most probable fungal species living in symbiosis with soft scales. On the other hand,

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Biology

Steinhaus (1955) demonstrated that this common surface fungus strongly adhered to the integumental folds and intersegmental areas of scales and remained, therefore, as a constant contaminant, surviving even after strong surface sterilizing procedures. When a few cells of Aureobasidium pullulans from the exterior of the insect were hung in drops of body fluid, they showed intense multiplication in 1-2 days, while the internal symbionts did not show any increase even after 17 days. Moreover, the more precise approach of Steinhaus (1955), using immunodiagnostic techniques, showed that the cultivated A. pullulans and the symbionts of P. corni, Eulecanium kunoense (Kuwana) and Parasaissetia nigra (Nietner) were not identical. However, a certain phylogenetic relationship between the symbionts and the fungus was not totally excluded by this sophisticated type of analysis. The conclusion was that the symbionts may represent forms of Aureobasidium, which cannot be grown on a synthetic medium, originally living on the surface of the plant but which later became adapted to a symbiotic life with soft scales as the result of a constant external association with them. The use of such modem diagnostic techniques as utilized by Munson et al. (1991, 1992) for aphids and mealybugs would be of great interest. Within the family Coccidae, the occurrence of two types of symbionts in the same species has only previously been reported for P. corni (Benedek and Specht, 1933). The Bacillus species indicated by these authors as being "associated" or "secondary" symbionts in around 50 % of the examined individuals were considered to be external contaminants by Schwartz (1935). The findings of Benedek and Specht, however, were confirmed much later by Nur (1972), who found that the yeast-like symbionts were associated with bacteria-like microorganisms in only some of the female Parthenolecanium putmani (Phillips) and Parthenolecanium cerasifex (Fitch) studied. The symbionts of the second type were discovered only during a careful examination by phase contrast and were detected in large numbers, especially in the fat cells. The bacteria-like symbionts in P. cerasifex were found to be rod-like in the diploid arrhenotokous race and neeAle-like in the obligate thelitokous race (Nur, 1972).

LOCALIZATION OF SYMBIONTS Since the time of their discovery, symbionts of all soft scales have been traditionally reported as yeast-like microorganisms freely floating in the host haemolymph and occasionally localized in fat cells which, at the most, only undergo slight changes (Buchner, 1965). They are evenly distributed in the body of mature females, but in the younger instars are more numerous and localized toward the periphery (Granovsky, 1929). In C. rusci, they were estimated to reach 60,000-70,000 microorganisms per individual (Berlese, 1906). In Pulvinariella mesembryanthemi (Vallot), wax cells were often found to include endosymbionts (Poisson and Pesson, 1939). These are apparently captured by phagocytes but continue their reproductive activity by budding and give rise to new microorganisms (Fig. 1.2.1.3.1,D). The wax cells then swell and are presumed to eventually burst, leaving the symbionts again free in the haemolymph. Phagocytizexl symbionts have also been observed in P. corni (Schwartz, 1932). A more specialized type of symbiosis within the Coccidae was found by Tremblay (1961) in Sphaerolecanium prunastri (Fonscolombe) and Eulecanium tiliae (L.), where the symbionts were localized in large, often binucleate, cells (mycetocytes). These symbiont-filled cells originated from normal fat cells whose nuclei seem to have undergone a process of polyploidization. This type of localization is apparently unusual within the family Coccidae and was considered to support the view that the genera Sphaerolecanium and Eulecanium were closely related (Tremblay, 1961, 1977).

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265

HEREDITARY TRANSMISSION OF SYMBIONTS In coccids, no exception is known to the general rule that symbionts are transmitted through the anterior (upper) pole of the growing oocytes (Buchner, 1965; Tremblay, 1977). When the nutrient cord connecting the nurse cells to the growing oocytes is differentiated, some symbionts penetrate through the "neck" of the typical single-egg ovarioles which characterize the females of all Coccoidea (Fig. 1.2.1.3.1,E,F). The penetration seems to start much earlier than in diaspidoids (Breest, 1914). After penetration, they remain in the neck area until the nurse cells cease their activity. Being few in number (usually 10-15; but about 30 in Pulvinaria vitis (Teodoro, 1918)), they do not cause the follicular wall to protrude in the form of a "symbiont pocket" as in the diaspidoids (Tremblay, 1989). At the time the nurse cells begin to degenerate, the symbionts reach the anterior (upper) pole of the egg (Fig. 1.2.1.3.1,G,H). Much more intricate is the transmission of the bacteria-like symbionts described in P. putmani and P. cerasifex by Nur (1972). The presence of the bacteria-like microorganisms was ascertained in over 90% of the embryos in P. putmani but circumstantial evidence suggested that they did not enter the oocytes through the ovariole necks and the nutrient cord as the primary yeast-like symbionts invariably do. In P. cerasifex, it was shown that the needle-like microorganisms of the obligate thelytokous race followed the "transmission route" known for the primary symbionts, and were always found in association with the yeasts at the anterior egg pole in young embryos. The rod-like bacteria found in the diploid arrhenotokous race of P. cerasifex were apparently not transmitted to the offspring. Rather scanty information is available on the movement of symbionts during embryonic development. The most detailed observations still date back to the old paper of Breest (1914) on a Lecanium species living on a palm tree and are limited to the first movements of the symbionts at the anterior pole soon after the formation and invagination of the germ band. In this species, the microorganisms were reported to avoid contact with the yolk mass but to become gradually enveloped by a distinct membrane in a kind of separate "pocket" (Breest, 1914) which was referred to as the "Pilzorgan" (i.e. fungus organ ) by Breest and as the "transitory mycetome" by Buchner (1965). Here the symbionts were described as changing their shape to round, small compact bodies having the appearance of nuclei that were very poor in chromatin. Later, the "pocket" is reached by yolk nuclei and its appearance as an independent symbiotic "organ" localized in the abdominal region of the embryo becomes more evident (Fig. 1.2.1.3.1,I). From this syncytial mass the symbionts should be transferred to fat cells or to haemolymph. The avoidance of contact by the symbionts with yolk was also observed in E. tiliae and S. prunastri by Tremblay (1961) at a very early stage of embryogeny. In the latter species, the symbionts were found to be included in a kind of small "plasma-globule" at the anterior pole of the mature egg.

HOST REGULATION OF SYMBIONT GROWTH As stated previously, several authors have reported the presence of "elongated forms" of the symbionts in soft scales, the number increasing with female age. Similar forms have been obtained by Steinhaus (1955) in experiments with P. corni infesting pear twigs placed in solutions containing polymyxin sulphate and actidione. To a lesser extent, the elongate and even "abnormal" forms also occurred in the untreated controls. These forms were much more common in dead than in healthy scales. Steinhaus considered

Section 1.2.1.3 references, p. 266

266

Biology

that his f'mdings were consistent with Schwartz's (1932) hypothesis that some kind of control on growth and reproduction of symbionts was exerted by the physiological status of the scale insect. The symbionts are thus probably kept at the sprout cell stage and prevented from growing to normal hyphal forms. Phagocytosis is an additional means of regulating symbiont numbers in a healthy insect. The suggestion by Schwartz (1932) that aging is the main cause of decrease of some "formative" and "regulative" substances in the host haemolymph is only partially acceptable. In fact, the hyphal forms (that would be indicative of a decrease of the formative restraint) were found in every stage including the egg (Tremblay, 1961). According to Tremblay (1961), the appearance of the elongate forms might indicate a decrease in vitality of the host scale due not only to aging but also to other weakening causes.

THE SIGNIFICANCE OF SYMBIOSIS The yeast-like symbionts of Coccidae do not engage the host organisms in the intimate participation processes documented for other groups of scale insects, such as pseudococcids and diaspidids (for a review, see Tremblay, 1989). The rather uniform type of localization in haemolymph, even if involving normal or polyploidized fat cells in some species, is an indication of a rather weak relationship. One of the reasons for uniformity might be that these insects do not seem to have undergone the changes in feeding behaviour known for pseudococcids, diaspidoids and several other groups (see review by Koteja, 1985). On the other hand, a clear indication that the relationship has reached the stage of a permanent link is provided by the obligatory mechanism of hereditary transmission. Even more impressive is the rather complex early embryogeny revolving a kind of transitory mycetome, which, if confirmed for other Coccid species, can be accepted as a strong proof of the intensity of the relationship. Unfortunately, biochemical evidence of the advantages offered to these scale insects of harbouring the symbionts is totally lacking. According to Buchner (1965), the data provided by Schwartz (1924), which were derived from pure cultures obtained from the P. corni symbionts, should prove the ability of these microorganisms to utilize urea, uric acid, guanine, xanthine and other purinic compounds. However, the reliability of Schwartz's methods has been questioned by Steinhaus (1955), who cast serious doubts on the sterilization techniques adopted by Schwartz and by other researchers to avoid contamination by external microorganisms. Some consideration also deserves to be given to the bacteria-like microorganisms described from some Coccid species. In the opinion of the present author, these bacteria might represent external microorganisms which are in the process of acquisition and adaptation to a symbiotic life with soft scales. However, they do not seem to have reached the obligatory status which is typical of true symbionts. Their next step might be a status of accessory or secondary symbionts, resembling the secondary endosymbionts of several aphid species, which have the appearance of gram-negative rod-shaped bacteroids (Iaccarino and Tremblay, 1973; Munson et al., 1991).

REFERENCES Benedek, T. and Specht, G., 1933. Mykologischbakteriologische Untersuchungen fiber Pilze und Bakterien als Symbionten in Kerbtieren. Zentralblatt fiir Bakteriologie, Parasitenkunde und Infektion Abteilung, 1, 130: 74-90. Berlese, A., 1906. Sopra una nuova specie mucidinea parassita del Ceroplastes rusci. Redia, 3: 8-15. Brain, C.K., 1923. A preliminary report on the intracellular symbionts of South African Coccidae. Annals of the University of Stellenbosch, 1: 1-48. Breest, P., 1914. Zur Kenntniss der Symbiontenfibertragung bei viviparen Cocciden und bei Psylliden. Archiv fiir Protistenkunde, 24: 263-276.

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Brues, C.T. and Glaser, R.W., 1921. A symbiotic fungus occurring in the fat-body of Pulvinaria innumerabilis Rath. Biological Bulletin, 40: 299-324. Buchner, P., 1911. Uber intrazellulare Symbionten bei Zuckersaugenden Insekten und ihre Vererbung. Sitzungsberichte der Gesellschafl ftir Morphologie und Physiologic (Mfinchen), 27: 89- 96. Buchner, P., 1912. Studien an intrazellularen Symbionten. 1. Die intrazellularen Symbionten der Hemipteren. Archiv fiir Protistenkunde, 26: 1-116. Buchner, P., 1921. Tier und Pflanze in Intrazellularen Symbiose. Borntriiger, Berlin, 462 pp. Buchner, P., 1930. Tier und Pflanze in Symbiose. Borntriiger, Berlin, 900 pp. Buchner, P., 1965. Endosymbiosis of Animals with Plant Microorganisms. Interscience Publishers, New York, London, Sydney, 909 pp. Conte, A. and Faucheron, L., 1907. Prrsence de levures dans le corps adipeux de divers coccides. Comptes Rendus de l'Academie des Sciences, Paris, 145: 1223-1225. Granovsky, A.A., 1929. Preliminary studies of the intracellular symbionts of Saissetia oleae (Bernard). Transactions of the Winsconsin Academy of Sciences, Arts and Letters, 24: 445-456. laecarino, F.M. and Tremblay, E., 1973. Comparazione ultrastrutturale della disimbiosi di Macrosiphum rosae (L.) e Dactynotus jaceae (L.) (Homoptera, Aphididae). Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', Portici, 30:319-329. Koteja, J., 1985. Essay on the prehistory of the scale insects (Homoptera, Coccinea). Annales Zoologici, 38:461-503. Leydig, I., 1854. Zur Anatomic yon Coccus hesperidum. Zeitschrif~ ~ r Wissenschaflliche Zoologic, 5: 1-12. Moniez, R., 1887. Sur un champignon parasite du Lecanium hesperidum (Lecaniascus polymorphus nobis). Bulletin de la Soci~t6 Zoologique de France, 12" 150-152. Munson, M., Baumann, P., Clark, M.A., Bauman, L., Moran, N.A., Voegtlin, D.J. and Campbell, B.C., 1991. Evidence for the establishment of aphid Eubacterium endosymbiosis in an ancestor of four aphid families. Journal of Bacteriology, 173: 6321-6324. Munson, M.A., Baumann, P. and Moran, N.A., 1992. Phylogenetic relationships of endosymbionts of mealybugs (Homoptera: Pseudococcidae) based on 16S rDNA sequences. Molecular Phylogenetics and Evolution, 1: 26-30. Nur, U., 1972. Diploid arrhenotoky and automictic thelytoky in soft scale insects (Lecaniidae: Coccoidea: Homoptera). Chromosoma (Berlin), 39: 381-401. Poisson, R. and Pesson, P., 1939. Contribution a l'rtude du sang des Coccides (Hrmipt~res Homopt~res Sternorrhyncha). Le sang de Pulvinaria mesembryanthemi Vallot. Archives de Zoologic Experimentale et G~n~rale, 81" 23-32. Putnam, J.D., 1880. Biological and other notes on Coccidae. Proceedings of Davenport Academy of Sciences, 2: 293-347. Schwartz, W., 1924. Untersuchungen fiber die Pilzsymbiose der Schieldliiuse. Biologisches Zentralblatt, 44: 487-527. Schwartz, W., 1932. Untersuchungen fiber die Pilzsymbiose der Schieldl/iuse (Lecaniinen). Archiv fiir Mikrobiologie, 3: 453-472. Schwartz, W., 1935. Untersuchungen fiber die Symbiose von Tieren mit Pilzen und Bakterien. IV. Archiv fiir Mikrobiologie, 6: 369-460. Smith, R.H., 1944. Bionomics and control of the nigra scale, Saissetia nigra. Hilgardia, 16: 225-288. Steinhaus, E.A., 1951. Report on diagnoses of diseased insects 1944-1950. Hilgardia, 20: 629-678. Steinhaus, E.A., 1955. Observations on the symbiotes of certain Coccidae. Hilgardia, 24: 185-205. Targioni Tozzetti, A., 1867. Studii sulle Cocciniglie. Memorie della Societa Italiana di Scienze Naturali, 3: 1-87. Teodoro, G., 1912. Ricerche sull'emolinfa dei Lecanini. Atti Accademia Veneta Trentina Istriana, 5: 72-84. Teodoro, G., 1916. Osservazioni sulla ecologia delle Cocciniglie con speciale riguardo alia morfologia e alia fisiologia di questi insetti. Redia, 11: 129-209. Teodoro, G., 1918. Alcune osservazioni sui saccaromiceti del Lecanium persicae Fab. Redia, 13: 1-5. Tremblay, E., 1961. Osservazioni sulla cariologia e suUa simbiosi endocellulare di alcuni Coccini. Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', Portici, 19: 215-260. Tremblay, E., 1977. Advances in endosymbiont studies in Coccoidea. Bulletin of the Virginia Polytechnic Institute, Research Division, 127: 23-33. Tremblay, E., 1989. Coccoidea endocytobiosis. In: Schwemmler, W. and Gassner, G. (Editors), Insect Endocytobiosis: Morphology, Physiology, Genetics, Evolution. CRC Press Inc. Boca Raton, Florida, pp. 145-173.

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Soft Scale Insects - Their Biology, Natural Enemies and Control

Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.

269

1.2.2 Honeydew 1.2.2.1 Morphology and Anatomy of Honeydew Eliminating Organs CHRIS P. MALUMPHY

DEFINITION OF HONEYDEW The origin of the accumulated sugary deposits, commonly known as honeydew, was once shrouded in mystery and the Roman naturalist Pliny gravely pondered on whether he should call it the sweat of the heavens, the saliva of the stars or a liquid provided by the purgation of the air (Imms, 1990). Honeydew results from liquid eliminated by certain groups of homopterous insects, but the precise def'mition varies among authors. Auclair (1963) def'med honeydew as "the liquid droplet excretion from the alimentary tract as released through the anus by aphids, coccids and many other plant sucking insects". Williams and Williams (1980) found this definition unsatisfactory as the word honeydew derives from popular usage denoting sugary deposits and not liquid elimination. They considered that the word honeydew implied "a characteristic ability of some plant-sucking insects, all of them Homoptera, to produce, under certain circumstances, sugary accumulations that result from liquid excretions through the anus". This has important biological connotations, namely that honeydew-producing insects tend to eliminate copious amounts of liquid, live gregariously and are sedentary or semisedentary (Williams and Williams, 1980). The term 'honeydew' used in this work embraces both definitions indicating the sugary deposits and the liquid elimination. In this work, honeydew is not considered to be 'excreted', as excretion is the active process by which an organism rids itself of the "waste products that arise as a result of metabolic activity" (Anon., 1987). Honeydew-producing insects are mostly phloem feeders that imbibe large quantities of plant fluid in order to meet their nutritional requirements. This is because the phloem sap, although rich in carbohydrates, contains low levels of soluble nitrogen compounds which are necessary for protein-building. The surplus carbohydrate solution is eliminated as honeydew. To achieve this, the gut is modified to form a 'filter chamber', which allows the large amounts of watery food to bypass the mid-gut and pass straight into the rectum to be voided (discussed in Section 1.1.2.6). This process allows the material passing through the mid-gut to be processed more efficiently and gets rid of the water in as short a time as possible (McGavin, 1993)

HARMFUL EFFECTS OF HONEYDEW Honeydew can be harmful to the insects that produce it, either directly or indirectly. Direct harm occurs from self-contamination and from contamination of the immediate environment. The insects can become trapped and asphyxiated in the syrupy deposits. With Coccidae, the active first-instars are particularly vulnerable, as anybody who has

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cultured soft scales will be aware. An indirect effect is the loss of host-plant vigour, partly due to a reduction in photosynthetic area as the surface of the plant becomes coated with a film of honeydew. This film serves as a medium for the growth of black sooty moulds (discussed in Section 1.2.2.2) increasing the rate of leaf death and abscission (Bach, 1991). The sooty moulds growing on the honeydew may also be entomophagous or at least kill the honeydew-producing insects by enveloping them (Nixon, 1951). The harmful effects of honeydew on Coccidae have been demonstrated experimentally by Way (1954) on Saissetia zanzibarensis Williams and by Bach (1991) on Coccus viridis (Green).

DISPOSAL OF HONEYDEW Disposal of honeydew away from the immediate vicinity of the individual producer, and other individuals in the population is important for the well-being of sedentary honeydew-producers. The quantity of honeydew that accumulates is dependent on the population density of the producers and species of host plant. When their populations reach high densities, mobile homopterans can avoid the problems of contamination by accumulated honeydew by moving on to new plants (Williams and Williams, 1980). Less mobile homopterans have developed other mechanisms (discussed below) which are not always effective. Many honeydew producers are associated with ants which feed on the honeydew, often removing it directly from the producer (Way, 1963). Some Coccidae modify their excretory behaviour in the presence of ants (Williams and Williams, 1980). Myrmecophilous Coccidae can often exist without attendant ants but ant-attended populations can have significantly greater population densities and higher reproductive rates than unattended populations. This is partly due to the removal of honeydew by the ants but also to the protection from predators and parasitoids, exclusion from herbivore competition, provision of shelter, transportation to more favourable feeding sites and functioning as 'nannies' (Bach, 1991). The complex mutualistic relationship between Coccidae and ants is discussed in detail in Section 1.3.5. Ants also enable Coccidae to exist in confined places where, in the absence of ants, self contamination with honeydew would quickly reduce their numbers; for instance Pulvinaria vitis (Linnaeus) is usually found in exposed situations and often produces copious quantities of honeydew. Antattended populations can exist beneath peeling bark on mature grapevine trunks (personal observation). Coccidae that live within plant stems or are subterranean are also usually ant-attended. Honeydew is typically disposed of by coating each droplet in powdery wax and then projecting it away from the body. Insects that do this often live on the undersides of leaves so that the honeydew is more likely to fall away and not contaminate adjacent individuals. A variety of morphological structures associated with the anus have been evolved in different homopteran taxa to achieve this. Aphididae project honeydew droplets by kicking them from the anus with a hind leg or by flicking the droplet with their cauda (Broadbent, 1951); Aleyrodidae flick honeydew away with their lingula while Coccidae use a complex anal apparatus (Williams and Williams, 1980). The use of this apparatus as a taxonomic character in the Coccidae has been discussed in detail by several authors (Hamon and Williams, 1984; Hodgson, 1994; Steinweden, 1929; Williams and Kosztarab, 1972) and its' morphology is described below, mainly taken from Hodgson (1994), whose morphological terminology is also followed here.

MORPHOLOGY AND ANATOMY OF THE ANAL APPARATUS OF COCCIDAE The anus is surrounded by a sclerotised ring, bearing setae and pores, positioned at the base of an invaginated tube. The opening of this tube is covered by a pair of plates

Morphology and anatomy of honeydew eliminating organs

271

w h i c h are located at the end o f the anal cleft. s h o w n in F i g s . 1 . 2 . 2 . 1 . 1 and 1 . 2 . 2 . 1 . 2 .

d"

T h e structure o f the anal apparatus is

",-.

f

A

\

I

Anal tube

I 1 I I I

'

Supporting bar

A qal plate '

"...

I

Discal seta

Ano-genital fold -.

>*

Subdiscal seta

I

Lateral margin setae

Subapical setae .~~

Apical seta

~ A n a l cleft

.

Ventral View

Dorsal view

t

Anus

Anal tube

.i / / \

/

/

/

II 7-~-----"-~---

~~-Anai-ring setae

Anal plate -------~, X \ \ \ \

/

I I

" '

/

/

. cleft Anal

B

Fig. 1.2.2.1.1. Anal area of an adult female Coccidae. A - Anal plates and associated structures. B - Anal ring invaginated.

Section 1.2.2.1 references, p. 274

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272

Anal cleft The anal cleft, which divides the posterior margin, varies in length. It may be long, as in Protopulvinaria Cockerell, where it almost reaches the centre of the body, or short, as in Drepanococcus Williams & Watson. Anal plates The anal plates are a major character for the family and are present in all adult female Coccidae, with the exception of Physokermes Targioni Tozzetti, and are otherwise only known in the Eriochitonini in the family Eriococcidae. Each plate is sclerotised and usually triangular in shape but often has the outer margins rounded. When closed the plates are approximately quadrate or 'kite-shaped', with the two inner margins contiguous. In typical Cardiococcinae and Filippia Targioni Tozzetti, the inner margins diverge posteriorly and bear spinose setae along their margin. The two outer margins can be very unequal in length. In the genera Kilifia De Lotto, Milviscutulus Williams & Watson, Protopulvinaria Cockerell and Udinia De Lotto, each anterior margin (also referred to as antero-lateral or cephalo-lateral margin) is longer than the posterior margin (also referred to as postero-lateral or caudo-lateral margin) and the plates are described as pyriform. In the Ceroplastinae Atkinson the anterior margins are relatively short and lie almost at right-angles to the long axis of the body whilst the posterior margins are longer and convex. In Cryptostigma Ferris, the plates are rounded laterally, being almost reniform or bean-shaped. Each plate is usually separate but may be joined anteriorly, as in Drepanococcus, by a slender sclerotised bridge. In Pseudopulvinaria Atkinson the anal plates stand at right-angles to the body and are fused at both the anterior and posterior ends, forming a crown-like structure which surrounds the anal ring. In Austrolichtensia Cockerell, there is an additional rectangular plate posterior to the anal ring, bearing a group of long setae. In the subfamily Ceroplastinae Atkinson, adult females are covered in a thick coating of wax at maturity, so the anal plates are carried on a densely sclerotised caudal process in order to reach the outer surface of the wax. The caudal process may be longer than the rest of the body.

Anal plate and associated setae There are usually apical and/or subapical setae present on each plate. In typical Myzolecaniinae, there are numerous setae on the dorsal surface. In many genera, such as Alecanochiton Hempel, Megapulvinaria Yang, Paractenochiton Takahashi, Saissetia D6planche and Udinia, there is one enlarged seta in the middle of the posterior half of each plate, referred to as the discal seta. Setae may also occur on the posterior margin and inner margin. The latter, may appear to be on the dorsal surface in slide preparations where the anal plates are slightly open. In what are possibly the more primitive genera, there are usually two and often more spinose setae along the inner margin of each anal plate and the plates diverge posteriorly from each another. In Megapulvinaria maxima (Green), the setae along the inner margin are spinose spatulate. The surface of the anal plate may be ridged, as in Melanococcus Williams & Watson and Pulvinarisca Borchsenius.

Ano-genital fold and associated setae The ano-genital fold is a membranous fold, more or less at fight angles to the long axis of the body, located between the anus on the dorsum and vulva on the venter. This fold usually has setae at either comer and along the margin, referred to as the anterior margin or fringe setae. In addition, there may be groups of setae on the ventral surface anterior to the ano-genital fold referred to as the hypopygial setae. On either side of the ano-genital fold there are frequently a pair of sclerotised bars, referred to as supporting bars or ventral thickenings, which extend anteriorly beneath the derm and may be associated with muscles for opening the plates. The setae on the lateral margins of the

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273

ano-genital fold are referred to as the lateral margin or sub-apical setae. Setae are entirely absent from the anterior and lateral margins of the ano-genital fold in Psilococcus Borchsenius. Anal-tube The eversible membranous anal-tube is corrugated with longitudinal parallel folds enabling it to expand and be more flexible. It may be long, as in Pulvinaria Targioni Tozzetti, or short, as in many of the Myzolecaniinae which are dependent on ants to remove the honeydew.

Fig. 1.2.2.1.2. Anal aparatus in 3rd-insizr nymph ofPulvinaria vitis (L.)" anal ring everted with seize splayed open; as - anal seize, a t ' - anal ring, a t - anal tube, a p - anal plate.

Anal-ring The anal ring surrounds the anus and is located at the base of the anal tube. The ring consists of two semi-circular sclerotised plates bearing setae, and one or more rows of thimble-like pores which are openings to the wax glands. In most species there are four pairs of anal-ring setae; three large pairs and one smaller pair. Halococcus formicarii Takahashi has 16 pairs of anal-ring setae. In a few genera, such as Physokermes and Rhodococcus Borchsenius, the anal-ring is greatly modified and may lack both setae and wax pores. In Austrolichtensia, wax pores are absent and the setae are set in a group along the posterior margin. The anal-ring pores produce a tube of densely matted, fine wax filaments which covers each seta in a sleeve of wax which protrudes from the anal cleft. Wax production is discussed in Section 1.2.3.2.

Section 1.2.2.1 references, p. 274

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274

ELIMINATION MECHANISM OF THE ANAL APPARATUS OF COCCIDAE Williams and Williams (1980) described the excretion and propulsion of a droplet of 'honeydew' by Pulvinaria iceryi (Signoret). First, the anal plates open by an upward and outward movement on their anterior hinged margins and the anal tube is everted. The anal tube, with the anus at its extremity, is then projected upwards between the plates and the anal setae, which are normally bunched together whilst invaginated, become splayed open. A droplet of honeydew is then eliminated from the anus and held between the wax-coated setae. As the droplet forms, it becomes coated in wax particles (Foldi and Pearce, 1985). The anus is then sharply withdrawn, reverting to its invaginated state. As the anal-ring is retracted, the anal setae are forced together and this sudden inward action propels the droplet of honeydew outward. The rectal musculature, which is responsible for the elimination of the droplet, is not directly involved in the propulsion of the droplet away from the body.

REFERENCES Anonymous, 1987. Oxford Concise Science Dictionary. Oxford University Press, Oxford. 758 pp. Auclair, J.L., 1963. Aphid feeding and nutrition. Annual Review of Entomology, 8: 439-490. Bach, C.E., 1991. Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus r and plants (Pluchea indica). Oecologia, 87: 223-239. Broadbent, L., 1951. Aphid excretion. Proceedings of the Royal Entomological Society, London (A), 26: 97-103. Foldi, I. and Pearce, M.J., 1985. Fine structure of wax glands, wax morphology and function in the female scale insect, Pulvinaria regalis Canard (Hemiptera: Coccidae). InternationalJournal of lnsect Morphology and Embryology, 14: 259-271. Hamon, A.B. and Williams, M.L., 1984. The Soft Scale Insects of Florida (Homoptera: Coccoidea: Coccidae). Arthropods of Florida and Neighboring Land Areas, Vol. 11. Florida Department of Agriculture & Consumer Services, Gainesville, 194 pp. Hodgson, C.J., 1994. The Scale Insect Family Coccidae: An Identification Manual to Genera. CAB International, Wallingford. 639 pp. Imms, A.D., 1990. Insect Natural History. Collins New Naturalist Series, Bloomsbury Books, London. 317 pp. McGavin, G.C., 1993. Bugs of the World. Blanford, London. 192 pp. Nixon, G.E.J., 1951. The association of ants with aphids and coccids. Commonwealth Institute of Entomology, London. 36 pp. Steinweden, J.B., 1929. Bases for the generic classification of the coccid family Coccidae. Annals of the Entomological Society of America, 22: 197-243. Way, M.J., 1954. Studies on the association of the ant Oecophylla longinoda (Latr.) (Formicidae) with the scale insect Saissetia zanzibarensis Williams (Coccidae). Bulletin of Entomological Research, 45: 113-134. Way, M.J., 1963. Mutualism between ants and honeydew producing Homoptera. Annual Review of Entomology, 8: 307-344. Williams, M.L. and Kosztarab, M., 1972. Morphology and systematics of the Coccidae of Virginia with notes on their biology (Homoptera: Coccoidea). Research Division Bulletin Virginia Polytechnic Institute and State University, 74: 1-25. Williams, J.R. and Williams, D.J., 1980. Excretory behaviour in soft scales (Hemiptera: Coccidae). Bulletin of Entomological Research, 70: 253-257.

Soft Scale Insects - Their Biology, Natural Enemies and Control

Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.

275

1.2.2.2 Sooty Moulds RICHARD K. MIBEY

INTRODUCTION The term sooty moulds is used here for the saprophytic fungi forming black superficial colonies on living plants infested with honeydew producing Homoptera, particularly scale insects (Coccoidea). These moulds are quite separate taxonomically from the black mildews (Meliolaceae) and phytopathogenic fungi which can also form black superficial colonies on leaves and twigs of living plants but which are not associated with insect honeydew. True sooty moulds form large crusts on leaves, stems, fruits and any part of the plant on which honeydew has fallen from homopterous insects. However, although sooty moulds are associated with scale insects and other honeydew producers, they can also occur in their absence.

TAXONOMY Sooty moulds are ascomycetes and mitosporic fungi, possibly with ascomycetous affinities. Although the teleomorph and anamorph states are frequently found in the same colonies, either one of the two states can occur alone. The taxonomy of this group of fungi is complex, mainly because several species can grow together in harmony and stages of different species have often been described under one name. For instance, Fumago vagans Pers, the most common sooty mould on green leaves of Tilia, Salix and Ulmus in Europe and parts of North America, is a mixture of Cladosporium and Aureobasidium (Woronichin, 1926; Friend, 1965). Some species are highly pleomorphic and this increases the confusion in mixed colonies. It is not uncommon for some species to have as many as three anamorphic states, in addition to the ascostromata. Hughes (1976) recognised 5 families of ascomycetes in his work on sooty mould fungi but did not place them in a separate Order. The classification used here for the sooty mould fungi follows that of Hawksworth et al. (1995), who placed these fungi in five families, namely the Antennularielliaceae, Capnodiaceae, Chaetothyriaceae, Euantennariaceae and Metacapnodiaceae, all within the Order Dothideales. This order does not include the families Meliolaceae, Asterinaceae, Parodiopsidaceae and related families, which were often included by earlier workers. As an assistance to the non-mycologist, a glossary of most of the terms used in this section is supplied at the end of the Section. The following taxonomic description of the families is taken from Hawksworth et al. (1995).

Section 1.2.2.2 references, p. 285

Honeydew

276

FAMILY" ANTENNULARIELLIACEAE Woron. (1925) Superficial mycelium irregular, dark, smooth or rough-walled, adpressed or erect; ascomata small, perithecial, more or less globose, stalked or sessile, opening by a small poorly-def'med lysigenous pore, sometimes with hyphal appendages; interascal tissue absent; asci small, ovoid, fissitunicate, 1-; ascospores hyaline to brown, usually 1-septate, sheath lacking. Anamorphs coelomycetous and hyphomycetous, if the latter, then conidia elongate and multiseptate. Saprobic, usually epiphytic, cosmopolitan, the genera Achaetobotrys and Antennulariella with only two species are included in this family. Type genus: Antennulariella Woron. (1915) = Capnocifferia Batista, in Batista and Ciferri (1963a) = Capnocrinum Bat. & Cif. (1963) Type species: A. fuliginosa Woron. (1915) Pycnidia meristogenous, globose to pyriform, 30-45 #m; conidia hyaline, one-celled, oval, 5 x 1.5 #m; ascomata much larger than pycnidia, 60-75 #m, with hyphal appendages; ascospores 2-celled, hyaline, 10 x 3-4 #m, with upper cell broader than lower one.

FAMILY: CAPNODIACEAE (Sacc.) Holm. ex Theiss. (1916) Mycelium superficial, well-developed, dark, composed of more or less cylindrical hyphae with mucous coating; ascomata small, sometimes vertically elongated, thin-walled, covered in a mucous layer, sometimes setose, usually with a clearly def'med ostiole, interascal tissue absent; asci saccate, fissitunicate; ascospores brown, septate, sometimes muriform. Anamorphs pycnidial, elongate, sometimes stipitate. Saprobic, usually on insect exudates on leaves and branches. The following 13 genera with 57 species are included in the family: Aithaloderma, Anopeltis, Callebaea, Capnodaria, Capnodium, Capnophaeum, Ceramoclasteropsis, Echinothecium, Hyaloscolecostroma, Phragmocapnias, Scoriadopsis, Scorias and Trichomerium. Type genus: Capnodium Mont. (1849a) Anamorphs: Fumagospora and Phaeoxyphiella Type species" C. salicinum Mont. (1849a) = Polychaeton salicinum (Mont.) O. Kuntze (1891) Ascomata black, more or less ovoid to ellipsoidal, sessile or shortly stalked, ostiolate at maturity, non-setose, scattered or in groups. Asci bitunicate, 8-spored; ascospores brown, usually 3-septate, with one or more longitudinal septa.

Fumagospora Arnaud. Pycnidia elongate, borne on short or long robust stalks: flask-shaped to cylindrical to long subulate, tapering to a long narrow neck which terminates in a fringe of hyaline, tapered hyphal extensions around ostiole. Conidia at first hyaline and one-celled, later turning brown and transversely 3-, occasionally 2-, 4- or 5-septate, with one to all of cells longitudinally septate. Fumagospora pycnidia are produced by Capnodium salicinum Mont.

Sooty moulds

277

Phaeoxyphiella Bat & Cif. Pycnidia flask-shaped but barely stalked: cylindrical or tapered neck terminates in an ostiole surrounded by blunt ends of hyphae. Conidia fusoid, straight or occasionally variously bent, reddish brown to brown, with an acute apex and narrow, fiat basal scar: mostly 15-septate though fewer septae are common and occasional conidia to 18-septate. Phaeoxyphiella pycnidia are produced by Capnodium walteri Saccardo.

FAMILY: CHAETOTHYRIACEAE Hansf. ex M.E. Barr (1979). Mycelium largely superficial, with narrow cylindrical brown hyphae, sometimes with setose appendages; ascomata often formed beneath a subiculum, spherical or flattened, often collapsing when dry, apex more or less papillate, with a periphysate ostiole; peridium thin-walled; hymenium usually 1+; interascal tissue of short apical periphysoids; asci saccate, fissitunicate; ascospores hyaline or pale, transversely septate or muriform. Anamorphs hyphomycetous. Epiphytic or biotrophic on leaves; mostly tropical. The family has the following 8 genera (27 syn.) and 75 species: Actinocymbe,

Ceramothyrium, Chaetothyrium, Euceramia, Microcallis, Phaeosaccardinula, Treubiomyces and Yatesula. Type genus: Chaetothyrium Speg. (1888). Type species: C. guaraniticum Speg. (1888) Mycelium hyaline to subhyaline, barely constricted at septa, hyphal cells 1.8-3.6 #m wide, dense pellicular cells over ascoma pale golden brown to brown. Setae arise from scattered cells ofhyphal network, singly or in groups of 2 to 4, non-septate, dark brown, thick-walled, subulate, up to 330 x 11 #m, base lobed and swollen. Ascomata yellowish to pale brown in water, to 150 #m in diam., pellicle over ascomata bears up to 20 laterally scattered setae similar to those borne on hymenium but devoid of pigmented cells around their base. Asci bitunicate, more or less ellipsoidal but tapered slightly at base, 8-spored and 45-56 x 18-20 #m in size. Ascospores hyaline, 3-septate at maturity, more or less ellipsoidal but somewhat broader above than below, finally slightly constricted at sepia, 18-21 x 5-5.5 #m. No conidial state has been associated with C. guaraniticum.

FAMILY: EUANTENNARIACEAE S. Hughes & Corlett ex S. Hughes (1972). Mycelium superficial, dark, hyphae cylindrical, forming a flattened mat but frequently with erect branches; ascomata more or less spherical, small, superficial, with a small lysigenous pore, peridium dark, with hyphal appendages; interascal tissue absent; asci saccate, fissitunicate; ascospores brown, transversely septate or muriform, sometimes attenuated at apices. Anamorphs hyphomycetous. Epiphytic, widely distributed. Four genera: Euantennaria, Rasutoria, Strigopodia and Trichopeltheca and 15 species are

recognisezl. Type genus: Euantennaria Speg. (1918). Mycelium in the form of a repent network, individual hyphae more or less cylindrical and cells usually longer than wide. Ascomata subglobose, darkly pigmented,

Section 1.2.2.2 references, p. 285

Honeydew

278

thick-walled, ostiolate at maturity, and bearing cylindrical hyphal appendages. Asci bitunicate, usually 8-spored but, in some asci, a few ascospores may become larger than usual, possibly at the 'expense' of others that remain small or immature; ascospores brown, 3- to multiseptate and ends of larger spores mucronate. Anamorphs: Hormisciomyces and Plokamidomyces Type species" E. tropicicola Speg. (1919).

FAMILY: METACAPNODIACEAE S. Hughes & Corlett (1972). Mycelium superficial, dark, copious, hyphae strongly constricted at septa with more or less spherical cells, tapering towards apices; ascomata superficial, small, more or less globose, black, thin-walled, with a periphysate ostiole; peridium of pseudoparenchyma; interascal tissue of periphysoids; asci more or less saccate, fissitunicate; ascospores brown, transversely septate, sometimes ornamented. Anamorph hyphomycetous, conidiogenous cells tretic. Epiphytic? on insect exudates or resin, widespread. Only one genus with six species is recognised, namely Metacapnodium. Type genus: Metacapnodium Speg. (1918). Hyphae moniliform and noticeably tapered towards their ends, smooth or roughened throughout or only distally roughened; cells barrel-shaped and sometimes strongly inflated, usually broader than long and occasionally up to 45 /xm wide. Ascomata subglobose to broadly ellipsoid, sometimes with a short robust stalk, dark brown to black, thick-walled, ostiolate at maturity and bearing tapering hyphal appendages laterally or at distal end. Asci bitunicate and usually 8-spored, in some asci only a few ascospores may develop fully, others remaining either as initials or maturing as dwarfed ascospores; ascospores 3- or 5-septate or of variable (5-11) septation, ellipsoid, golden brown to dark brown and rounded at ends. Anamorphs" Capnobotrys, Capnocybe, Capnosporium and Capnophialophora. Type species: M. juniperi (Phillips & Plowright) Speg. (1918). = Capnodium juniperi (Phillips & Plowright) Speg. (1918). = Polychaeton juniperi (Phillips & Plowright) O. Kuntze (1891).

OCCURRENCE AND DISTRIBUTION Although this group of fungi has a worldwide distribution, it is most common in the tropics. However, the distribution of sooty moulds is largely dependent on that of the Homoptera that produce the honeydew and their host plants. The surface of living leaves - the phylloplane - is not only a suitable substrate for fungi such as sooty moulds, but also for bacteria, algae, lichens, mosses and liverworts and the many animals which browse on these epiphytes. There appears to be relatively few publications on the sooty moulds. Sooty moulds are known to derive their nutrients from the honeydew produced by many species of Homoptera. As defined by Auclair (1963), honeydew is a liquid excretion from the alimentary tract, as released through the anus by aphids, coccoids and many other plant sucking insects. Honeydews are complex mixtures of various compounds, mainly sugars but also including free amino acids, proteins and minerals, together forming a nutritious food (Auclair, 1963; Way, 1963). The main components of coccid honeydews appear to be water-soluble carbohydrates (mostly sugars) and

Sooty moulds

279

water, along with a small amount of nitrogen-containing compounds and traces of other substances (Hackman and Trikojus, 1952; Ewart and Metcalf, 1956). The high carbohydrate content makes honeydew an important energy source for many organisms, including birds, ants, small beetles, flies, wasps, honeybees and bumble bees (Moiler, 1987).

EARLY OBSERVATIONS There are a substantial number of early accounts on the association of sooty mould fungi with insects. For instance, in Sri Lanka, Gardner (1849) reported that "the coffee plants had assumed a deep black colour, having all the appearance of soot having been thrown over them in great quantities, but the black fungus never makes an appearance on the tree till after the Coccus or bug has been on it a long time". This was followed by Berkeley (1849) who pointed out that Gardner's observations were similar to those found on both the leaves of exotic plants in England and to serious outbreaks in orange plantations in the Azores and Madeira. Gardner (1849) also stated that "as certainly as the scale never appears on the upper surface of the leaf, so surely does the fungus never appear on the under one". Later, the sooty mould fungus Limaciniafernandeziana was found by Johow (1896) to be closely associated with an insect of the family Coccidae, causing a lot of damage. In his account of the sooty mould Capnodium citricola, McAlpine (1896) indicated that he had never found this fungus in the absence of scale insects and that the fungus always occurred after the appearance of the insects.

H O S T P L A N T - S O O T Y M O U L D INTERACTIONS

Sooty moulds appear to show little preference for particular host-plants. Thus, in New Zealand, Hughes (1976) found Trichopeltheca asiatica Bat., Costa & Cif. on more than 80 species ofFilicales, Gymnospermae, dicotyledons and monocotyledons; Euantennaria mucronata (Mont.) Hughes on over 39 different host species and Acrogenotheca elegans (Fraser) Cif. & Bat. on 33 different hosts, while Capnobotrys dingleyae Hughes has been found on Taxus in Europe and on Dacrydium, Phyllocladus and Podocarpus in New Zealand. In Europe, Capnobotrys neesii Hughes has been collected on Abies, Buxus, Corylus, Rubus and Sambucus. However, some species do appear to have a much more restricted range, although this needs confirmation from further collections. Thus, Metacapnodium juniperi (Phill. & Plowr.) Speg. has only been recorded from Juniperus and Antennatula pinophila (Nees ex Pers.) Strauss has only been found on Abies. On the other hand, there are records of several species of sooty moulds on the same host. Thus, in Malaysia, Kwee (1988) found the following sooty moulds on guava infested with a variety ofHomoptera: Aithaloderma clavatisporum, Limacinula musicola,

Phragmocapnias betle, Scoriasphilippensis, Trichomeriumgrandisporum,Leptoxyphium sp., Polychaeton sp. and Tripospermum sp., while on Durio zibethinus infested with whiteflies and mealybugs, Kwee (1989) found Phragmocapnias betle, Scorias spongiosa, Trichomerium grandisporum, Trichopeltheca asiatica, Leptoxyphium sp., Polychaeton sp. and Tripospermum sp. As sooty moulds are somewhat susceptible to being washed off by heavy rams, clearly the leaf surface can be an important factor in their presence and this was confirmed by Sparks and Yates (1991), who found that the rough granulated leaves of certain pecan (Carya illinoensis) cultivars tended to harbour a greater volume of sooty moulds than the smoother-leaved varieties.

Section 1.2.2.2 references, p. 285

280

Honeydew Sooty moulds tend to be restricted to the surfaces on which the honeydew falls. Thus, Hughes (1976), working on the sooty moulds of New Zealand, found the splashings and run-off of honeydew from scale insects on the trunks of Nothofagus extended to the surroundings, including the surfaces of stones and other vegetation. This honeydew supported a thick and continuous carpet of mould. Similar observations were reported by Moiler (1987).

INSECT - SOOTY MOULD INTERACTIONS

It is clear that sooty moulds have been recorded in association with a wide range of different Homoptera (Tables 1.2.2.2.1 and 1.2.2.2.2). How specific these associations are is unclear. Mibey (unpublished observations) recorded Scorias spongiosa (Schw.) Fries on the honeydew of Coccus species on several unrelated plants in Kenya - Coffea arabica, Citrus sinensis, Ehretia cymosa and Eriobotrya japonica. It would seem that the specificity of particular sooty mould species needs further study. However, just as the differences in the chemistry of the honeydew of homopterous insects can effect the ants which attend them (reviewed in Section 1.3.5), so also could this affect the species of sooty moulds associated with a particular homopteran. It would seem quite possible that not only could the proportions of the basic components of honeydew affect sooty mould associations, but also the secondary plant chemicals, which may fred their way into the honeydew from the sap of the host plant.

TABLE 1.2.2.2.1 Records of sooty mould fungi associated with honeydew of Coccoidea. Sooty mould

Scale insect

Location

Effect on plant"

Reference

Capnodium citri

Coccus viridis (Green)

India

reduced photosynthesis

Haleem,1984

Limacinia fernandazina

indet.

South America

death

Johow, 1896

Indet.

Ceroplastes floridensis Comstock

Israel

discolouration grapefruit

Mansourand Whitcomb, 1986

Indet.

Coccus sp.

Sri L a n k a

discolouration

Berkeley,1849

lndet.

Coccus alpinus De Lotto Planococcus kenyae (Le Pelley)

Kenya

leaf discolouration KenyaCoffee, 1990 coffee

Indet.

Coccus hesperidum Zambia Linnaeus

discolouration mango

Javaid,1986

Indet.

Coccus viridis

Hawaii

leaf death; abscission

Bach, 1991

Indet.

Cribrolecanium andersoni (Newstead)

South A f r i c a

discolourationcitrus

Brinkand HewilI, 1993

Indet.

Protopulvinaria pyriformis Cockerell

South Africa

stained avocado

Steyn et al., 1993

Indet.

Pulvinaria sp.

Azerbaidjan

unknown - grapes

Mamedov,1987

Sooty moulds

281 TABLE 1.2.2.2.1 (continued) Sooty mould

Scale insect

Location

Effect on plant"

Reference

Indet.

Parasaissetia nigra (Nietne0 Saissetia coffeae

India

fruit drop -

Shivarama Krishnan et al., 1987

Santalum album

(Walker) Indet.

Parthenolecanium corni (Bouche') Planococcus ficus

France

unknown

Caries, 1985

USA (Florida)

discolouration-

Hamon, 1986

(Signoret) Indet.

Philephedra floridana

Conocarpus erectus

Nakahara & Gill

P. tuberculosa Nakahara & Gill Indet.

Eriococcus coriaceus

Australia

foliar discolouration to Eucalyptus

(Maskell)

Vranjic and Gullan, 1990

blakely~ lndet.

Uhracoeolostoma brittini Morales

New Zealand

discolouration Nothofagus beech

Moiler, 1987

Indet.

Orthezia insignis

India

discolouraion -

Srikanth et al., 1988

Spain

weakening of Ulmus Romero-Casada and minor Romero-Casada, 1985

India

death of shoots mulberry

Siddapaji et al., 1984

India

stunting - pigeon pea

Patel et al., 1990

Cyprus

unknown

Serghiou, 1983

Israel

twig death -

Mendel et al., 1983

Browne Indet.

Gossyparia spuria 0Vlodeer) (as G. ulmO

Indet.

Icerya aegyptiaca (Douglas)

Indet.

Maconellicoccus hirsutus

(Green) Indet.

Planococcus cirri

(Piss,,) Indet.

Planococcus sp.

Cupressus Indet.

Pseudococcidae

Nigeria

death - Eupatorium

Iheagwam, 1983

odoratum Indet.

Rastrococcus invadens

Benin

reduced shoot formation

Bokonon-Ganta and N ~ h w a n d e r , 1995

(Williams) * these include the pathogenic effects of the coccoid plus the effects of the sooty mould.

TABLE 1.2.2.2.2 Records of sooty mould fungi associated with the honeydew of Homoptera other than Coccoidea. Sooty mould

Homopteran

Location

Effect on plant"

Reference

Aleurocanthus woglumi

India

leaf discolouration

Dharpure et al., 1994

ALEYRODIDAE

Capnodium cirri

Asby

Section 1.2.2.2 references, p. 285

282

Honeydew TABLE 1.2.2.2.2 (continued)

Sooty mould

Homopteran

Location

Effect on plant*

Reference

Capnodium sp.

Aleurocanthus woglumi

India

yield loss

Rajak and Diwakar, 1987

Capnodium walteri

Trialeurodes merlini

Canada

death

Hughes, 1976

Indet.

A leurocy bo tus

Mauritania, Senegal, Nigeria, Niger, Burkino Faso

withering and death

Adam, 1989

Mauritania Senegal, Niger, Nigeria Burkino Faso

withering and death

Adam, 1989

Matsui, 1995

spp.

Indet.

Aleurocybotus indicus David & Subramaniam

Indet.

Bemisia argentifolia

Japan

irregular ripening of tomatoes

Indet.

Bemisia tabaci

U S A (California)

reduced growth and Horowitz, 1988 function - cotton

(Gennadius) Indet.

Bemisia tabaci

USA (California)

discolourationcantaloupe

Nuessly and Perring, 1995

Indet.

Trialeurodes vaporariorum

Hawaii

yield loss - tomato

Johnson et al., 1992

Japan

severe damage

Maeda et al., 1988

Tasmania

defoliation, turgor loss- Boronia sp.

Mensah and Madden, 1992

India

discolouration -

Rajagopal et al., 1990

(Westwood) PSYLLIDAE Indet.

Ctenarytaina thysaneura (Ferris & Klyver)

Indet.

Heteropsylla cubana

Leucaena

(Crawford) Indet.

Psylla pyri

France

unknown

Geoffrion, 1984

(Linnaeus) Indet.

Psylla pyricola

U S A (Pennsylvania) leaf damage - pear

Savinelli and Tetrault, 1984

Thailand

discolouration Durian

Tigrattanamont and Pramual, 1990

Mauritius

reduction in ear formation maize

Annon., 1986

USA (Florida)

unknown sugarcane

Nguyen et al., 1984

India

unknown - maize Mole, 1984 sugarcane, sorghum

India

discolouraion of

(F6rster) Indet.

Tenaphalara malayensis Crawford

CICADELLIDAE Indet.

Peregrinus maidis Ashmead

Indet.

Perkinsiella saccharicida

-

Kirkaldy Indet.

Pyrilla perpusilla Walker

APHIDIDAE

Chaetophoma quircifolia

Tuberculatus paiki

Capnodium sp.

indet.

Hille Ris Lambers

Rao et al., 1991

Q ue rc l~s

USA (Georgia)

reduced photosynthesis - pecan

Wood et al., 1988

Sooty moulds

283 TABLE 1.2.2.2.2 (continued)

..Sooty mould

Homopteran

Location

Effect on plant"

Reference

Indet.

Aphis gossypii

Egypt

withering of citrus

EI-Nagar et al., 1982

Nigeria

death - Eupatorium

lheagwam, 1983

Glover Indet.

Aphis gossypii

odoratum Indet.

Aphis spiraecola

USA (Virginia)

decreased photosynthesis- apple

Kaakeh et al., 1992

Israel

twig death -

Mendel et al., 1983

Patch Indet.

C~nara cupressi

Cupressus

Buckton Indet.

Eulachnus rileyi

Israel

Indet.

Metapolophium dirhodum

discolouration

Halperin, 1986

Pinus halepensis Pinus brutia Pinus pinea

Williams

Spain

slight damage

-

Pons

et al.,

1989

maize

(Walker)

Rhopalosiphum padi (Linnaeus)

Sitobion avenae (Fabricius) Indet.

Metapolophium The Netherlands dirhodum Rhopalosiphum padi Sitobion avenae

leaf senescence

Rabbinge et al., 1983

Indet.

Pterochloroides persicae (Chol.)

Tunisia

unknown - peaches

Par-Trigui et al., 1987

Indet.

Pterochloroides persicae

Romania

unknown - plum, peach

Hondru et al., 1986

Indet.

Pterocallis alni

New Zealand

discolouration -

Bulloch, 1986

(De Geer) Indet.

Sarucallis kahawaluokalani

China, Japan, Korea, Italy, USA (Florida), Hawaii

Lagerstroemia indica

indet.

USA (Georgia)

defoliation - pecan

Metcalfa pruinosa

Italy

crop loss - soybean, Ciampolini et al. 1987 figs, lemons, apples, pears, plums and peaches

Nigeria

withering, death of rice

(Kirk.) Indet.

Alnus. unknown -

Patti, 1984

Sparks, 1992

FLATIDAE Indet.

(Say)

DELPHACIDAE Indet.

Nilaparvata maeander

Adam, 1984

* these include the pathogenic effects of the homopteran insect plus the effects of the sooty mould.

Section 1.2.2.2 references, p. 285

284

Honeydew Sooty moulds can also act as food for some insects. Thus, the earwing Forficula auricularia L. was found to feed on both the hop aphid (Phorodon humuli (Schrank)) and on the sooty moulds which appeared on their honeydew (Buxton and Madge, 1977). Fungal spores are usually dispersed in the air and by droplet splash. However, it has also been reported that soft scales can assist in the transmission of sooty moulds; thus Nath (1973) considered that Coccus hesperidum and Ceroplastes floridensis were the most important of several scale insects studied with regard to the dispersal of Capnodium citri in citrus orchards in West Bengal. Presumably this was through the crawlers, which are thought to be mainly dispersed by the wind, accidentally carrying spores with them.

EFFECTS OF SOOTY MOULD ON HOST PLANTS It can be difficult to separate the effects of sooty mould fungi on the plants from the parasitic effects of the homopterous insects which produce the honeydew, and many of the effects on the host plants given in the literature are likely to be caused by the insect. However, some direct effects of the sooty moulds have been found, usually associated with heavy infestations. For instance, the sooty mould Capnodium sp. has been shown to have a pronounced effect on the net photosynthesis of the leaves of pecan (Wood et al., 1988). The thick cover of this fungus was found to block 98% of the light penetrating the leaf, reducing photosynthesis by 70 %. In addition, the temperature of the abaxial leaf surface was increased by 4 %, and this may also have contributed to the reduction in leaf photosynthesis. Reductions in photosynthesis have also been recorded by K a ~ e h et al. (1992) associated with sooty moulds on the honeydew of Aphis spiraecola Patch on apple leaves. Reduced photosynthesis leading to early senescence and/or smaller fruits has been recorded many times. In New Zealand, Blank (1987) found that severe infections of sooty moulds on tamarillos (Cyphomandra betacea) infested with the whitefly Trialeurodes vaporariorum (Westwood) led to leaf and fruit drop. The fruits were smaller and yield was reduced by 43 %. Populations as few as 50 adult whiteflies per leaf led to sooty mould contamination, 17-39% defoliation and a loss in yield of 19-30%. Other examples are: Base and Roy (1973) with sooty moulds on the honeydew of Dialeurodes citri and Aleurocanthus husaini on citrus; EI-Nagar et al. (1982) on Citrus sinensis; Sparks (1992) on pecans in Georgia (USA); Bach (1991) on Pluchea indica infested with Coccus viridis (Green) (where substantial early leaf loss occurred when ants were excluded); Alam (1989) on rice infected by the aleyrodid Aleurocybotus indicus David & Subramaniam in Burkina Faso, Nigeria and Niger; Jlin et al. (1988) with the sooty mould Chaetothyrium citri on the leaves of citrus infected by Dialeurodes citri Ashmead, and Mibey (personal observations) with sooty moulds on Mangifera indica. Reduced yield can also be caused by sooty moulds contaminating the inflorescence, as on mangoes (Prakash, 1991). The chlorophyll content of grapefruit leaves was reduced when covered by Capnodium citri, and this was associated with an increase in total sugars and a reduction in phenolic compounds (Shashi et al., 1992). Other physiological changes in the leaves include changes in the concentrations of certain inorganic ions, as in mango leaves infected with Capnodium ramnosum, with increases in Fe and K and decreases in Na, Mn and Ca (Kulkarni and Kulkarni~ 1978), while Vova and George (1978) found an increase in catalase activity but no increase in peroxidase activity in a number of common plants infected with Capnodium sp. The thick mat formed by sooty moulds can also lead to uneven ripening of fruit, as with tomato fruit covered with sooty moulds on the honeydew of the whitefly Bemisia tabaci Gennadius in Japan (Matsui, 1995), while Johnson et al. (1992) found a 5% reduction in the yield of tomatoes caused by sooty moulds on the honeydew of the whitefly T. vaporariorum. In addition, the presence of

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285

sooty moulds on the honeydew of aphids significantly reduced the sale value of cured tobacco leaves (Lucas, 1975). The presence of sooty moulds on a crop can be detected by remote sensing. For example, in an aerial survey of winter wheat infected with Sitobion avenae (F.) and Rhopalosiphum padi (L.), the infected areas of the crops could be identified by dark foci which were found to be associated with sooty moulds, mainly Cladosporium spp. (Greaves et al., 1983). Similar results were obtained by Everitt et al. (1994) in their areal survey of citrus blackfly.

CONTROL Not infrequently the presence of sooty mould fungi on crops is economically more significant than the damage caused by the producers of the honeydew on which the fungi live. Even where this is not the case, the presence of the sooty moulds is always a significant addition to the damage caused by the associated insects. Thus, the most effective control of sooty mould is through the elimination of the honeydew producers for, without the honeydew, the fungi would not be able to grow. However, occasionally it may be necessary to control the actual fungi. In Mexico, this was achieved as a byproduct of sprays against citrus leaf spot (Alternaria limicola) on Mexican lemon (Citrus aurantifolia) by the use of mancozeb and the detergent "Ariel', as this mixture was also found to give effective control of the sooty mould Capnodium citri (Orozco, 1991). In India, the fungicides Wettasull (sulphur) and gum acacia were found to be effective in controlling the sooty mould fungi Microxyphium columnatum, Leptoxyphium fumago and Tripospermum myrti on mangoes (Prakash, 1991). Other examples are the fungicides Benlate (benomyl) and Morocide (binapacryl) against the sooty mould Chaetothyrium citri on citrus in India (Jlin et al., 1988) and Bordeaux mixture and Thiorit (sulphur) against Capnodium ramnosum on mango in Bangladesh (Ahmed et al., 1991). However, Katole et al., (1994) found that copper oxychloride was ineffective when used alone against Capnodium citri on Nagpur mandarins in India, whereas better control was obtained when insecticides were added. Some control has also been claimed using neem leaf concoctions against Capnodium citri (Khune et al., 1985).

CONCLUSIONS With the separation of the Astermaceae, Meliolaceae and related families from the sooty moulds, the latter form a discrete order, the Dothideales, whose families (Antermularielliaceae, Capnodiaceae, Chaetothyriaceae, Euantennariaceae and Metacapnodiaceae) are intimately associated with the honeydews produced mainly by homopterous insects. Even so, the sooty mould fungi are a rather poorly studied group and there is much still to be discovered regarding their general biology and especially their specificity to particular honeydew producers and their host plants.

REFERENCES Ahmed, H.U, Hossein, M.M., Alam, S.M.K., Hug, M.I. and Hossain, M., 1991. Efficacy of different fungicides in controlling anthracnoses and sooty moulds of mango. Bangladesh Journal of Agricultural Research, 16: 74-78. Alam, M.S., 1984. Incidence of brown planthopper and whitefly (Hemiptera: Aleyrodidae) in Nigeria. International Rice Research Newsletter, 9: 13-14. Alam, M.S., 1989. Whitefly (Hemiptera: Aleyrodidae) a potential pest of rice in West Africa. International Rice Research Newsletter, 14: 3, 38-39. Annon., 1986. Annual Report, Mauritius Sugar Industry Research Institute, 58. Reduit Mauritius. Auclair, J.L., 1963. Aphid feeding and nutrition. Annual Review of Entomology, 8: 439-490.

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Honeydew Bach, C.E., 1991. Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus viridis) and plants (Pluchea indica). Oecologia, 87: 233-239. Base, S.K. and Roy, A.J., 1973. Sooty mould and black speck of citrus leaves and fruits. Progressive Horticulture, 5: 53-55. Berkeley, M.J., 1849. A notice of a mould attacking the coffee plantations in Ceylon. Journal of the Royal Horticultural Society, London, 4: 7-8. Blank, R.H., 1987. The effect of greenhouse whitefly spray thresholds on tamarillo yield. Proceedings of the New Zealand Weed and Pest Control Conference, 1989: 157-160. Bokonon-Ganta, A.H. and Neuenschwander, P., 1995. Impact of the biological control agent Gyranusoidea tebygi on the mango mealybug, Rastrococcus invadens, in Brazil. Biocontrol Science and Technology, 5: 95-107. Brink, T. and Hewitt, P.H., 1993. Parasitoids of the whitefly powdery scale, Cribrolecanium andersoni (Newstead) (Hemiptera: Coccidae), a pest of citrus. International Journal of Pest Management, 39: 99-102. Bullock, B.T., 1986. Causes of damage to some wild mango fruit trees in Zambia. International Pest Control, 28: 98-99. Buxton, J.H. and Madge, D.S., 1977. The food of the European earwig (Forficula auricularia L.) in hop gardens. The Entomologist's Monthly Magazine, 112:1348-1351; 231-237. Caries, L., 1985. How should one control grapevine mealybug? Arboculture-Fruitiere, 32: 30-31. Ciampolini, M., Grossi, A. and Zottarelli, G., 1987. Damage to soyabean through attack by Metacalfa pruinosa. Informatore-Agrario, 43: 101-103. Dharpure, S.R., Sharma, M.L., Rai, H.S. and Sangar, R.B.S., 1994. Chemical control of citrus blackfly, Aleurocanthus woglumi and sooty mould disease of citrus with conventional insecticides alone and in combination with fungicides. International Journal of Tropical Agriculture, 12: 273-277. EI-Nagar, S., Ismail, I.I., Atria, A.A. and Nagar, S.E.I., 1982. Assessment of damage by Aphis gossypii Glover on Citrus sinensis var. nobilis. Bulletin de la Socirt6 Entomologique d'Egypte, 64: 149-153. Everitt, J.H., Escobar, D.E., Summy, K.R. and Davis, M.R., 1994. Using airborne video, global positioning system, and geographical information system technologies for detecting and mapping citrus blackfly infestations. South Western Entomologist, 19: 129-138. Ewart, W.H. and Metcalf, R.L., 1956. Preliminary studies of sugars and amino acids in the honeydews of five species of coccids feeding on citrus in California. Annals of the Entomological Society of America, 49: 441-447. Friend, R.J., 1965 What is Fumago vagana? Transactions of the British Mycological Society, 48: 371-375. Gardner, G., 1849. Extracts from a report by George Gardner, Esq., on the coffee blight of Ceylon, addressed to the Secretary to the Government. Journal of the Royal Horticultural Society, London, 4: 1-6. Geoffrion, R., 1984. Pear psyllids - history, economic importance. Bulletin SROP, 7: 13-15. Georghiou., 1988. Synergism: potential new approach to whitefly control. California Agriculture, 42: 21-22. Greaves, D.A., Hooper, A.J. and Walpole, B.J., 1983. Identification of yellow barley dwarf virus and cereal aphid infestations in winter wheat by aerial photography. Plant Pathology, 32: 159-172. Hackman, R.H. and Trikojus, V.M., 1952. The composition of honeydew excreted by Australian coccids of the genus Ceroplastes. The Biochemical Journal, 51:653-65 Haleem, S.A., 1984. Studies on fruit quality of sweet orange as affected by soft green scale and sooty moulds. South Indian Horticulture, 32: 267-269. Halperin, J., 1986. Eulachnus rileyi, a new pine aphid in Israel. Phytoparasitica, 14: 319. Hamon, A.B., 1986. The genus Philephedra, in Florida. Entomology Circular, Division of Plant Industry, Florida Department of Agriculture & Consumer Services, 281" 1-2. Hawksworth, D.L., Kirk, P.M., Sutton, B.C. and Peglar, D.M., 1995. Ainsworth and Bisby's Dictionary of the Fungi (8th Ed). International Mycological Institute, Bakeham Lane, London. xii + 616 pp. Hondru, N., Margarit, G. and Pops, I., 1986. A new aphid pest of fruit orchards, Pterochloroidespersicae. Analele Institutului de Cercet~iri Penetru Protectia Plantelor, 19: 151-154. Horowitz, A.R., Toscano, N.C., Youngman, R.R., Kiddo, K., Knabble, J.J. and Georghiou, G.P., 1988. Synergism: potential new approach to whitefly control. California Agriculture, 42: 21-22. Hughes, S.J., 1976. "Sooty moulds". Mycologia, 68: 451-691. lheagwam, E.U., 1983. Insect fauna of the Siam weed, Eupatorium odoratum. Beitriige zur Tropischen Landwirtschaft zur Tropischen Landwirtschaft und Veterin~re, 21:321-327. Javaid, I., 1986. Causes of damage to some wild mango fruit trees in Zambia. International Pest Control, 28: 98-99. Jlin, V.B., Roy, A.J. and Rana, B.S., 1988. Chemical control of citrus sooty mould caused by Chaetothyrium citri (Am.) Fisher. Progressive Horticulture, 20: 176-178. Johow, F., 1896. Estudios Sobre la Flora de las islas de Juan Fernandez Cervantes. Santiago de Chile, 287 pp. Johnson, M.W., Caprio, L.C., Coughlin, J.A., Tabashnik, B.E., Brousenheim, J.A. and Welter, S.C., 1992. Effect of Trialeurodes vaporariorum (Homoptera: Aleyrodidae) on yield of fresh market tomatoes. Journal of Economic Entomology, 85: 2370-2376. Kaakeh, W., Pfeiffer, D.G. and Marini, R.P., 1992. Combined effects of spirea aphid (Homoptera: Aphididae) and nitrogen fertilization on net photosynthesis, total chlorophyll content and greenness of apple leaves. Journal of Economic Entomology, 85: 939-946.

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287 Katole, S.R., Kolhe, A.V., Kale, K.B., Muqueen, A. and Khiratkar, S.D., 1994. Pesticidal management of sooty mould syndrome on citrus. Crop Research, Hisar, 8: 141-144. Khune, N.N., Patile, B.G., Kale, K.B., Newsaker, V.B., Wangikar, P.D. and Moghe, P.G., 1985. In vitro studies on the effect of fungicides and plant extracts against the fungus of sooty mould of Nagpur oranges. PKV Research Journal, 9: 95-97. Kwee, L.T., 1988. Studies on some sooty moulds on guava in Malaysia. Pertanika, 11: 347-355. Kwee, L.T., 1989. Studies on some lesser known mycoflora of durian: sooty mould and black mildew. Pertanika 12: 159-166. Kulkarni, D.K. and Kulkarni, U.K., 1978. Physiology of mango leaves infected with Capnodium ramnosum Cooke. II. Mineral contents. Biovigyanum, 4: 173-174. Lucas, G.B., 1975. Diseases of tobacco. 3rd ed. Biological Consultancy Associates. Raleigh, N.C., 622 pp. Maeda, M., Masuda, T. and Takano, T., 1988. Severe occurrence of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood) on strawberry. Annual Report, Society for Plant Protection, Northern Japan, 39: 235-236. Mamedov, D.S., 1987. Effective against scales. Zashchita-Rastenii, 2: 49. Mansour, F. and Whitecomb, W.H., 1986. The spiders of a citrus grove in Israel and their role as biocontrol agents of Ceroplastesfloridensis. Entomophaga, 31 : 269-276. Matsui, M., 1995. Efficiency of Encarsia formosa in suppressing population density of Bemisia tabaci on tomatoes in plastic greenhouses. Japanese Journal of Applied Entomology and Zoology, 39:25-31. McAlpine, D., 1896. The sooty mould of citrus trees: a study in polymorphism. Proceedings of the Linnean Society of New South Wales, 21" 722-724. Mendel, Z., Golan, Y., Madar, Z., and Solel, Z., 1983. Insect pests and diseases of cypress in Israel. La-Yaaran, 33: 37-41. Mensah, R.K. and Madden, J.L., 1992. Factors affecting Ctenarytaina thysanura oviposition on Boronia megastigma terminal shoots. Entomologia Experimentalis et Applicata, 62: 261-268. Moiler, H., 1987. Honeydew - a south Island beekeeper's bounty. N e w Zealand Beekeeper, 195: 31-33. Mole, U.N., 1984. Unusual occurrence of PyriIla on rabi sorghum. Journal of the Maharashtra Agricultural University, 9: 231. Nath, D.K., 1973. Insect transmission of sooty mould (Capnodium sp.) to orange orchards at Darjeeling District, West Bengal. Science and Culture, 39: 262-263. Nguyen, R., Sosa, O. and Mead, F.W., 1984. Sugarcane delphacid, Perkinsiellasaccharidica. Entomological Circular, Division of Plant Industry, Florida Department of Agriculture and Consumer Services, 265, 2pp. Nuessly, G.S. and Perring, T.M., 1995. Influence of endosulfan on Bemisia tabaci 0lomoptera: Aleyrodidae) populations, parasitism, and lettuce infectious yellow virus in late-summer planted cantaloupe. Journal of Entomological Science, 30:49-6 I. Orozco, Santos M., 1991. Control of citrus leaf spot (Alternaria limicola) and other diseases of Mexican lemon, (O'trus aurantifolia) with Mancozeb and detergent sprays. Revista Mexicana de Fitopatologia 9: 129-133. Par-Trigui, A., Cherif, R. and Par-Trigui, A., 1987. The brown aphid: Pterochloroidespersicae, a new pest of fruit trees in Tunisia. Annales del l'institutdel Tunisie, 60: 1-12. Patel, I.S., Dodia, D.A. and Patel, S.N., 1990. First record of Maconellicoccus hirsutus (Homoptera: Pseudococcidae) as a pest of pigeon pea (Cajanua cajan). Indian Journal of Agricultural Science, 60: 645. Patti, I., 1984. An aphid injurious to Lagerstroemia in Italy. Informatore Fitopatologico, 34: 12-14. Pons, X., Comas, J. and Albajes, R., 1989. Maize aphids in north east Spain. Acta phytopathologica et Entomologica Hungarica, 24: 173-176. Prakash, O., 1991. Sooty mould disease of mango and its control. InternationalJournal of Tropical Plant Diseases, 9: 277-280. Rabbinge, R., Sinke, C. and Mantel, W.P., 1983. Yield loss due to cereal aphids and powdery mildew in winter wheat. Mededelingen van de Rijksfaculteit Landbouwwetenschappen te Gent. International Symposium of Crop Protection, 48:1159-I 168. Rajak, R.L. and Diwakar, M.C., 1987. Kolshi problem in orange orchards of Vidarbha region (Maharashtra). Plant Protection Bulletin, Faridabad, 39: I-2. Rajagopal, D., Naik, K. and Gowda, M.K.M., 1990. Subabul psyllid and itsoutbreak in Karnataka. Current Research, University of Agricultural Science, Bangalore, 19: 9-12. Rao, D.J., Nigam, M.P. and Sengupta, K., 1991. Seasonal variation of Tuberculatus (Orientuberculoides) paila" (Homoptera: Aphididae) on oak plant (Quercus serrata) Thunberg. Indian Journal of Sericulture, 30: 59-63. Romero-Casado, J. and Romero-Casado, J., 1985. Gossyparia ulmi, one more cause of weakening in elms. A morphological and biological study. Boletin del Servicio de Defensa Contra Plagas e Inspection Fitopatologica, 11: 45-58. Savinelli, C.E. and Tetrault, R.C., 1984. Analysis of pear psylla populations and associated damage in Pennsylvania pear orchards. Environmental Entomology, 13: 278-281. Serghiou, C.S., 1983. The citrus mealybug, Planococcus citri Risso - carob moth, Ectomyelois ceratoniae, pest complex on grapefruit and its chemical control. Technical Bulletin, Agricultural Research Institute, Nicosia, Cyprus, 56: 1-17.

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Honeydew Shashi, K., Cheema, S.S. and Kapoor, S.P., 1992. Some of the biological changes in citrus leaves infected with sooty mould, Capnodium cirri. Journal of Research, Punjab Agricultural University, 29: 354-356. Shivarama Krishnan, V.R., Nagaveni, H.C and Rajamuthu Krishnan, 1987. Poor seed setting in sandal. Mycoforest, 23: I01-I03,243-244. Siddapaji, C., Puttaraju, T.B. and Venkatagiriyappa, S., 1984. Icerya aegyptiaca a new pest of mulberry in India and its control. Current Science, 53: 1298-1299. Sparks, D., 1992. Stress factors affecting fruit set on pecan in Georgia. 83rd Annual Report, Northern-Nut Growers Association, 1993: 57-62. Sparks, D. and Yates, I.E., 1991. Pecan cultivars susceptibility to sooty mould related to leaf surface morphology. Journal of American Horticultural Science, 116: 6-9. Srikanth, J., Reddy, G.V.P., Mallikarjunappa, S. and Kumar, P., 1988. Records of Or~hezia inaignis Browne (Homoptera: Ortheziidae) on Parthenium hysterophorus L. Entomon, Kariavattom (India), 13: 2, 185-186. Steyn, W.P., Du-Toit, W.J. and De Villiers, E.A., 1993. Effect of insect growth regulator CGA 211446, on the third instar of the heart-shaped scale on avocados. Yearbook, South African Avocado growers Association, 16: 116-117. Tigrattanamont, S. and Pramual, C., 1990. Economic importance of the durio psyllid, Tenaphalara manayenais in Thailand. Kaen-Kaset, 18: 152-159. Vranjic, J.A. and Gullan, P.J., 1990. The effect of a sap-sucking herbivore, Eriococcus coriaceus (Homoptera: Eriococcidae), on seedling growth and architecture in Eucalyptus blakelyi. Oikos, 59:157-162. Vova, A.B. and George, V.C., 1978. Catalase and peroxidasc activities of Capnodium-infected leaves of some common plants. Science and Culture, 44: 139-140. Way, M.J., 1963. Mutualism between ants and honeydew producing Homoptera. Annual Review of Entomology, 8: 307-344. Wood, B.W., Tedders, W.L. and Reilly, C.C., 1988. Sooty mould fungus on pecan foliage suppresses light penetration and net photosynthesis. HortScience, 23: 851-853. Woronichin, N.N., 1926. Zur Kcnntnis dcr Morphologie und Systcmatik der Russtaupilzc Transkaukasiens. Annals of Mycology, 24:231-265.

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Glossary of the mycological terminology used in this Section In order to provide supplementary information for entomologists who might not be familiar with the mycological terms used here, this glossary contains most of the terms used in the taxonomic part of this section.

Anamorph

asexual form or morph of a fungus, characterised by the presence or absence of conidia; also known as the "imperfect state'.

Ascoma (pl. ascomata)

an ascus containing structure; ascocarp.

Ascomycotina

the largest group of fungi; producing sexual spores, the diagnostic feature for which is the ascus.

Ascospores

spores produced in an ascus.

Ascus (pl: asci)

a sac-like cell diagnostic of an Ascomycotina teleomorph, in which ascospores are produced by free-cell formation.

Biotrophic

an obligate parasite.

Bitunicate

an ascus in which the inner wall is elastic and expands greatly beyond the outer wall at the time of ascospore liberation.

Coelomycetous

anamorphs in which the conidia are formed in distinct structures, such as conidiomata.

Conidia

non-motile asexually produced spores produced by conidiomata.

Conidiogenous

producing conidia.

Conidioma

a specialised multi-hyphal, conidia bearing structure.

(pl. conidiomata) Epiphytic

a plant living on another plant but not as a parasite.

Fissitunicate

a bitunicate ascus whose wall layers split during ascospore discharge ('jack-in-the-box').

Fusoid (fusiform)

spindle-like; narrowing towards the ends.

Hymenium

the spore bearing layer of a fruit body.

Hyphomycetous

anamorphs in which the conidia are not borne in discrete conidiomata but are on separate hyphae or hyphal aggregates.

Lysigenous pore

a pore formed by the breakdown of cells.

Meristogenous

formed by the growth and division of one hypha.

Moniliform

having swellings at regular intervals, like a string of beads.

Mucronate

ending in a sharp point.

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Muriform

a spore which has septae in more than one plane - a dictyospore.

Mycelium

a loose mass of hyphae (filaments); the vegetative body of a fungus.

Ostiole

any pore by which spores are freed from an ascigerous or pycnidial fruit-body.

Papillate

having papillae or small rounded processes.

Pellicle

a delicate outside membrane.

Pellicular

cells

cells forming the pellicle, a delicate outside membrane.

Peridium

the wall or limiting membrane of a sporangium or other fruit body.

Periphysate

having hair-like projections (periphyses) inside or near the ostiole.

Periphysoids

short hyphae originating above the level of the developing asci but not reaching the base of the cavity.

Perithecium

a closed ascomata with a pore at the top, a true ostiole and a wall of its own.

(pi" perithecia) Pieomorphic

having more than one independent form or spore stage in the life cycle.

Pycnidium

an ostiolate conidioma of fungal tissue, frequently +flask-shaped, the entire inner surface of which is lined with conidiogenous cells.

(pi: pycnidia) Pycnidial

ascomata which produce pycnidia.

Repent

fiat, creeping or prostrate hyphae

Saccate

like a sac or bag.

Saprobic

a fungus using dead organic material as food and commonly causing decay.

Stipitate

stalked.

Subiculum

a net-like, wool-like or crust-like growth of mycelium under fruitbodies.

Subulate

slender and tapering to a point.

Teleomorph

sexual form or morph, i.e. characterised by ascomata; also referred to as the "perfect state".

Tretic

conidiogenesis in which each conidium is limited by an extension of the inner wall of the conidiogenous cell.

Sq[t Scale Insects- Their Biology, Natural Enemies and Control Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.

1.2.3

291

Soft Scales as Beneficial Insects

1.2.3.1 Scale Insect Honeydew as Forage for Honey Production HARTWIG KUNKEL

INTRODUCTION Many zoological textbooks mention the beneficial aspects of scale insects (Coccoidea), particularly as producers of shellac by species of the Tachardiidae, of carmine by Dactylopius coccus Costa (Dactylopiidae) and of wax by the soft scale Ericerus pela (Chavannes) (see Section 1.2.3.2), but do not mention their honeydew, which is the main product used by bees to make honey in many regions of the world. Beekeepers are not interested in publicising the fact that the most costly, tasteful honey comes from the faeces of unknown insects. The idea of using the nectar of fragrant flowers is clearly more attractive, as can be seen in any encyclopedia or at exhibitions of bees and honey. However, this is not true for many zoogeographical regions, particularly those with large forests or which have dry summers or, indeeA, in areas where much of the weed flora has been decimated following the application of ferilizers or herbicides. In these areas, honey is produced from honeydew. Honeydew is also an important food source to many organisms in addition to bees and other insects, such as birds in New Zealand (Gaze and Clout, 1983) and Colombia (K6ster and Stoewesand, 1973) and even man (e.g. "manna', see Bodenheimer and Theodor, 1929).

DISTRIBUTION AND DIVERSITY OF SPECIES VISITED BY HONEY-BEES Dalman (1826), then the Director of the Stockholm Museum of Natural History, was the first to describe the connection between coccid honeydew and bees. Indeed, he discovered the bud-like Coccus hemicryphus on Norway spruce (Picea abies) precisely because it was visited by honey-bees. With the description of what is now known as Physokermes hemicryphus, Dalman (1826) also found the main honeydew producer for bees over a large part of Europe.

REGIONS WHERE THE HONEY-BEE IS ENDEMIC Although honey bees are thought to have originated in Southern Asia, I have been unable to locate any information on relationships between coccids and bees from there or from Africa where the honey-bee may have been first domesticated.

Section 1.2.3.1 references, p. 299

Soft scales as beneficial insects

292

Areas where Norway spruce is endemic Physokermes hemicryphus (Dalman) is found mostly on the Norway spruce, Picea abies and seems to be the main honeydew source in regions where the Norway spruce is endemic and has not been planted by man. In regions where the Norway spruce is only present following its introduction by man, no large populations of P. hemicryphus have been observed. In addition, P. hemicryphus is absent from areas with extremes of climate, such as north of a line between Oslo and Stockholm, beyond an unknown eastern border in Russia and also in the High Alps. I have estimated that about 50% of all honey produced in Middle Europe is from honeydew, including mixed honeys. In Austria, for which the best data are available, this figure is up to about 80% in some areas (Ruttner, 1956, 1960; Fossel, 1956, 1974). Here and in other parts where the Norway spruce forests are endemic, P. hemicryphus is surely the source of more than half the honeydew honey, the other main source being 2-3 aphids of the genus Cinara. Austria is also the region where P. hemicryphus has been most extensively studied (e.g., Stem, 1841; Kaluza, 1940; Fossel, 1960; Pechhacker, 1976, 1984, 1988). In Germany, Schmutterer (1954, 1956, 1958, 1965) described some aspects of its ecology, and was the first to discriminate between Physokermes piceae (Schrank) and P. hemicryphus. There are numerous reports on honey-bee visits to P. hemicryphus (Fig. 1.2.3.1) from France (Vosges Mountains), Switzerland, Austria, Slovenia, Germany, the Czech Republic, Norway and Sweden (see Kunkel and Kloft, 1985). In the past, honeydew honey has played an important role in trade between Eastern Europe (Poland, the Baltic States, West Russia) and the West. I believe, as did Stem (1841), that this massive production of honey was correlated with the large populations of P. hemicryphus in the large forests of these Eastern regions. Other important honeydew sources in this area and throughout much of Europe are 2-3 Cinara species (Aphidinea) on spruce and fir and also 5 species of Coccidae and a species of kermesid, but these are of minor importance (Table 1.2.3.1.1).

TABLE 1.2.3.1.1 Data on species of Coccoidea, apart from Physokermes hemicryphus, visited by honey-bees in Middle Europe.

Honeydew producer

Host plants

References

Physokermes piceae (Schrank)

Picea abies, Spruce (especially young plants)

Ratzeburg, 1844; Schmutterer, 1952a; Fossel, 1960; Pechhacker, 1984.

Parthenolecanium rufulum (Cockerell)

Caslanea sativa, Sweet Chestnut Quercus robur oak

Fossel, 1963; Kunkel and Klofl, 1965.

Parthenolecanium comi (Bouch6)

Fraxinus excelsior ash Robinia pseudoacacia, false acacia Ulmus glabra, mountain elm

Fossel, 1963. Pechhacker (in litt., 1981);

Parthenolecanium fletcheri (Cockerell)

Thuja occidentalis

Phyllostroma myrtilli (Kaltenbach)

Vaccinium myrtillus , bilberry

Arnhart, 1926; Gontarski, 1949; Schmutterer, 1952b, 1958; ~ l e i n , 1956; Klofl, 1959; Berner, 1967. Klofl, 1960.

Kermes quercus (Linnaeus)

Quercus roboris Quercus petraea

Fossel, 1963.

Gontarsld, 1940; Michel, Geinitz, 1958.

1942;

Scale insect honeydew as forage for honey production

293

Fig. 1.2.3.1.1. Physokermespiceae (Schrank). A - with a large droplet of honeydew. B - with a visiting honeybee (Apis meUifera) foraging for honeydew. (Photographs by Hattenschwiler).

Southern Europe, especially Greece Along the Aegian coast of Greece and Turkey, the margarodid Marchalina hellenica (Gennadius) is common on the Aleppo pine, Pinus halepensis and plays a dominant role as a honeydew source for bees. This scale insect has been studied by Ermin (1950) in Turkey and by Nicolopoulos (1965) and particularly Santas (1980, 1983), who has added

Section 1.2.3.1 references, p. 299

294

Soft scales as beneficial insects

substantially to our knowledge based on his work in Greece. In this region, 60 % of all honey production is dependent on the honeydew of M. hellenica and only about 35 % on nectar. The remaining 5 % is also actually honeydew honey, but from the interior of Greece collected from aphids and a few other species of scale insect - 4 Coccidae and an aclerdid (Table 1.2.3.1.2). In other parts of southern Europe, honeydew honey also plays an important economic role. Thus Ferrazzi (1983) estimated that, in North Italy, up to 100% of all honey came from honeydew, although he did not name the source. The honeydew producers seem to be diverse and even include whiteflies (Aleyrodinea) (Santas (1983) in Greece) and Flatidae (Fulgoroidea) (Barbattini (1988) in Italy). Data for other areas are urgently required. However, it is likely that other scale insects will still be important in southern Europe, in particular P. hemicryphus, which is here found on fir rather than on spruce: onAbies cephalonica in Greece, onAbies alba in The Apennines (Italy; Kloft, 1962) and in the conifer zone of Romania (Daghie et al. 1972); from Physokermes piceae on fir in Bulgaria (Tsankov et al., 1983). Other honeydew sources reported are Ceroplastes rusci (Linnaeus) on Ficus carica from Split in Croatia (Pechhacker, in lit.) and from Parthenolecanium corni (Bouch6) on Robinia pseudacacia in Romania (see Crane et al., 1984).

TABLE 1.2.3.1.2 Data on species of Coccoidea visited by honey-bees in Greece. Honeydew producer

Host plants

References

Physokermes hemicryphus (Dalman) A major source

Abies cephalonica, Cephalonian fir

Santas, 1983, 1988.

Parthenolecanium comi (Bouch6)

Corylus avellana, hazel Crataegus spp, hawthorne

Santas, 1983, 1985b.

Eulecanium sericeum (Lindinge0

Abies cepahlonica

Santas, 1983, 1988.

Pulvinaria pistaciae (Bodenheimer)

Pistacia spp., pistachio

Santas, 1985a.

Aclerda berlesii Buffa

Arundo donax,

Santas, 1989

a major source in southern reed

REGIONS WHERE THE HONEY-BEE HAS BEEN INTRODUCED The United States of America In the mountains of Oregon and California, the main source of honeydew is the margarodid Xylococcus macrocarpi (Coleman) which is found on the bark of mainly Calocedrus decurrens from which is produced the famous white cedar honey. However the literature is rather poor, with only an analysis of cedar honey by White et al. (1962) and a few general references (Vansell, 1932; Pellett, 1937, 1976). Data on other sources are equally sparse. Apparently the coccid Neopulvinaria innumerabilis (Rathvon), which has a wide host range on deciduous trees (Schmutterer and Kloft, 1957), is visited by bees (Putnam, 1880, in Williams, 1983). In addition, a Physokermes sp. has also been reported as being visited by bees in Massachusetts (Gates, 1909). Gates (1909) also reported much honeydew honey, mostly mixed with nectary honey, from large areas east of the Mississipi and up to New York and New England. A gall-like coccoid (probably a species of Coccidae or Kermesidae) on the oak Quercus virginiana in Texas also excretes honeydew used by bees (Pellet, 1976).

Scale insecthoneydew asforagefor honeyproduction

295

The Southern Hemisphere Within the southern Hemisphere, the only group of coccoids which has been recorded as supplying honeydew for honey production is the Margarodidae. Zealand Recently there has been a considerable upsurge in interest in 'bush' or 'forest honey' in the northern part of South Island (Cook, 1971; 1981; Dalzell and Singers, 1975; Morales et al., 1988). This honey is primarily dependent on the margarodid Ultracoelostoma assimile (Maskell), although U. brittini Morales (Morales, 1991)also appears to be important. These two species are found in the Nothofagus (southern beax~h) forests, especially on N. solandri var. solandri. However, about 30 species of scale insect have been reported off Nothofagus spp. (Walton, 1979) and many secrete honeydew which could also contribute to beech honeydew honey. Most of this honey is collected by wandering beekeepers, some of whom have more than ten hives. In the Chatham Islands, U. dracophylli Morales on Dracophyllum sp. is also thought to be a source of honeydew for bees (Morales, 1991).

New

South America No particular areas within South America have been noted for honeydew honey although it is considered that its' use will be widespread here (see Barth, 1971, for Brazil). No specific species have been identified. The only records are by Reichholf and Reichholf (1973) from Blumenau in South Brasil and K6ster and Stoewesand (1973) near Bogota, Colombia, both of whom considered that the honeydew was secreted by species of Margarodidae, with the typical long wax tube for honeydew excretion. K6ster and Stoewesand (1973) believed it might have been a Xylococcus sp., the adult female living inside a bark gall. However, its' adult female was described as having welldeveloped legs and other non-Xylococcus characters. The host plants were Mimosa bracaatinga, formerly planted for its high tannin content in Brasilia, and Inga sp., planted as shade trees in coffee plantations in Colombia, both belonging to the family Mimosaceae. Thus both records are for large, rather uniform plantations, with bees introduced by man. Nonetheless, these plantations do provide a locally important honeydew source. As in New Zealand, a few nectar-feeding birds may also be dependent on this. For instance, some migratory hummingbird species appear to stop over in these areas and then compete with the bees for the honeydew. Other insects, such as wasps, ants and flies, also feed on this product, but on the ground or on plant surfaces.

SOME ASPECTS OF THE ECOLOGY OF HONEYDEW AND HONEY-BEES Wherever the importance of honeydew in honey production has been studied, it has been found that the former is almost as attractive as nectar, even though bees prefer the latter (Kunkel and Kloft, 1985). However, while nectaries are accompanied by specific signals for the bees from the plants (such as colour and guide-lines), honeydew is randomely deposited on various surfaces and is therefore much more difficult to locate and is probably mainly found by chance whilst visiting a flower or searching for water. The scale insects which act as a source of honeydew belong to the families Coccidae, Pseudococcidae, Margarodidae, Kermesidae, Aclerdidae and Eriococcidae, many ofthem living on the bark of trees. All are phloem feeders. However, not all coccoids feed in the phloem, some (mainly Diaspididae and relatives) have secondarily changed to feeding from other cells (called "localbibitors" rather than the "systembibitors') which feed on phloem and xylem (Kunkel, 1967, 1968; Kloft and Kunkel, 1969). These non-phloem

Section 1.2.3.1 references, p. 299

296

Soft scales as beneficialinsects feeAers take up a much reduced volume of sap, mainly from the parenchyma and little, if any, honeydew is eliminated so that they are of no significance to bees.

The attractiveness of the honeydew Why then are some coccid sources of honeydew more attractive than others? This is probably due to the size of the honeydew droplet. Most of the species from the regions mentioned above build up large droplets which retain much water and which present a striking optical signal. Thus the members of the family Margarodidae (i.e. the Margarodinae, Xylococcinae and Monophlebinae) secrete a long tube of wax from the anal ring pores and through this build up a large droplet of honeydew on their apex by frequent production of small amounts of honeydew from the anus. This honeydew is collected by the bees whilst they are on the wing and thus the bees will only be competing with other honeydew-feeding animals, such as hummingbirds, where these are present. However, some margarodids lack this tube (e.g. Xylococculus macrocarpae Coleman from the USA and Marchalina hellenica from Greece); these appear to have convergently reduced this tube to a broken wax sack, which is lost with the honeydew droplets when they fall off. This procedure is similar to the coating of wax which covers the honeydew droplets produced by the Aphidinea and Psyllidinea and appears to be the basic way in which the stickiness of honeydew is neutralised in many Sternorrhyneha (Kunkel, 1972). Coccoids of some of the more advanced families, i.e. Coccidae, Pseudococcidae and Eriococcidae, expel their honeydew in a shower of small droplets. However, it is considered that ant attendance of these scale insects has resulted, in the course of evolution, with the coccoid producing a collection of large droplets at its anus rather than expelling them forcibly (Kunkel, 1973). This is perhaps what happened with P. hemicryphus. This species is now only weakly attended by ants and so Kunkel and Klofi (1985) have speculated that their ancestors suffered high selection pressures, and then may have modified their developmental period from spring to the early summer months, when ants are more interested in lachnids and the honeydew gets a better chance to be removed by the bees.

Amounts of honeydew To be of use to both bees and beekeepers, the honeydew source needs to produce large amounts at any given time and within a given locality. Thus, these sources require the following characteristics: (i) the elimination of honeydew by individual coccoids should be high per unit time; (ii) the coccoids should be abundant in any given locality, and (iii) this population needs to be accessible to bees and beekeepers. In Middle Europe, about 70% of the Sternorrhyncha species visited by bees possess a filter gut. Within the Aphidinea, aphids of similar body mass but with a filter gut produce 2-4 times more honeydew than those without, both groups developing on trees (Kunkel and Kloft, 1977). Most honeydew production in the Coccoidea is by the females and then only during particular periods during their development. Thus, P. hemicryphus only produces significant amounts of honeydew during the prereproductive period of the adult female (Schmutterer, 1956), while the Xylococcus sp. from Brazil (Reichholf and Reichholf, 1973) appears to be only important during their 2nd- and 3rd-instars. Schmutterer (1956)estimated the rate of honeydew production by P. hemicryphus was about 0.6#1 per hour, only about 6% of the 10#1 noted by Reichholf and Reichholf (1973) for Xylococcus sp; while in aphids without a filter gut, the rate has been found to be about 0.09#1 per hour for the peach potato aphid Myzus persicae (Sulzer). Because the diameter and length of the stylet channels in margarodids and coccids appears to be very similar (see Pesson (1944) for data on Pulvinaria sp. and Icerya sp.), it would appear that other factors are affecting the flow, such as climate, the viscosity of the phloem sap and the host plant (i.e. whether deciduous or coniferous).

297

Scale insect honeydew as forage for honey production

FACTORS AFFECTING THE BUILD-UP OF SCALE INSECT POPULATIONS One important factor which may affect the abundance of a population at any given time is whether a species is wholly or partially parthenogenetic. Parthenogenesis allows rapid reproduction during periods when the conditions, particularly the food source, are favourable. Thus, P. hemicryphus only produces a few males, whereas with P. piceae the sex ratio is approximately 50:50 (Schmutterer, 1952a). Another important coccid species for apiculturists in Europe is Parthenolecanium fletcheri (Cockerell) which appears to be entirely parthenogenetic (Schmutterer, 1952b). Another possible factor is voltinism. The margarodids which are of importance to apiculturists (Table 1.2.3.1.3) are not as obviously univoltine as the soft scales.

Table 1.2.3.1.3 Species of Margarodidae as important sources oh honeydew for honey production Honeydew producer

Main host plant

Regions

Marchalina hellenica (Gennadius)

lh'nus halepensis, aleppo pine

Turkey and Greece, along the coasts of the Aegian Sea

Calocedrus decurrens, incense cedar

USA, mountains of Oregon and California

Xylococcus spp.

Mimosa bracaatinga Inga sp.

Brazil, near Blumenau; Colombia, near Bogota

Ultracoelostoma assimile (Maskell)

Notophagus solandri

New Zealand, northern part of South

Xylococcus macrocarpi (Coleman)

Island

Effects of waterstress in the host plant on population growth The interaction of the parasitic coccoid with its host-plant is a close one, the rate of growth of the coccoid depending very much on the quality of the plants sap. As this contains rather limited amounts of nitrogen upon which the insect depends for growth, quite small changes in the nitrogen content of the sap can have dramatic effects on population growth rates. One factor which can modify the nitrogen balance within the plant is waterstress. Whilst under waterstress, plants mobilise nitrogenous compounds in order to change the osmotic pressure in the phloem. Kunkel and Kloft (1985) noted that the quality of the honeydew produced by M. persicae on wilting radish (Raphanus sativus) changed with time. Initially there was a 6-fold increase in the amount of carbohydrate, followed by a period when free amino acids increased up to 4-fold. It seems possible, therefore, that waterstressed trees might, for a time, have enriched phloem sap with a much higher amino acid concentration, stimulating increased population growth rates of the coccids. This was evidently the case with Parthenolecanium corni on plum (Prunus domestica) and Physokermes piceae on spruce (Picea abies) (Thiem, 1938) and with Parthenolecanium fletcheri on Thuja occidentalis (Schmutterer, 1952b).

Effects of changes in soil fertility on population growth of coccids It is therefore not surprising that changing the soil fertility also changes the population growth rate of many Stemorrhyncha. Clearly nitrogen fertilizers have a similar affect to that of water stress in terms of making more soluble nitrogen available. However,

Section 1.2.3.1 references, p. 299

298

So3~ scales as beneficial insects

changes in the potassium (K) balance can also have marked effects, but these are the reverse to those with increased nitrogen - i.e. resulting in decreased populations (see Kunkel and Kloft, 1985; Brfining, 1967, for scale insects). The application of K to potassium poor soils has proved to be a good way of reducing aphid and coccid populations. Since the initial successes of Nicolaisen (1923) and Scheller (1932) - with the woolly apple aphid Eriosoma lanigerum (Hausmann) numerous other experiments have also shown this effect (see Kunkel and Kloft, 1985). Thus, Brfining (1967) noted marked differences in the populations of Parthenolecanium rufulum (Cockerell) and P. corni (Bouchr) on trees with and without added K (Table 1.2.3.1.4). Smimoff and Valero (1975) obtained similar results with the soft scale Toumeyella parvicornis (Cockerell) on jack pine (Pinus banksiana).

TABLE 1.2.3.1.4 Reduction in population density of two species of Parthenolecanium after application of NPMg fertilizers with and without K to potassium poor soils, where no. is the density of scales per 10 cm 2 bark on branches of the host trees and % refers to the percentage of the population on potassium poor soils.

Soft scale insect

Host plant

Without potassium % pop.

With potassium no % pop.

no.

Parthenolecanium rufulum (Cockerell)

Quercus rubra

8.78

100

0.82

9.3

Parthenolecanium corni (Bouchr)

Robinia pseudoacacia

9.09

100

0.26

2.9

How do the changes in K levels in the soil affect the plant physiologically? K appears to reduce the soluble part of the nitrogen fraction in plants (Schmalfuss, 1933) and this appears to be due to a number of factors acting together: - The uptake of ammonium ions is reduced by the competition of the same sized K ions; - increased levels of K promotes greater enzymatic activity in the assimilation chain, leading to more ATP and (again together with K) therefore greater demand to synthesize more insoluble protein (Mengel, 1968); - high K levels outside the phloem forces the ATPase pump in the cell membranes between the sieve elements and the companion cells to pump in K ions whilst pumping out protons. In order to correct the changed pH, an active symport of protons and sucrose takes place back into the phloem. However, this causes a change in the osmotic value and it is speculated here that there is then likely to be an outflow of free amino acids which is missed by those coccids imbibing phloem sap.

THE ROLE OF APICULTURISTS For bees to be able to take advantage of honeydew, it is necessary for them to be in large uniform forests at particular times and places. Thus, the period available for tapping the honeydew of P. hemicryphus is only about 30 days during May-June, while the optimal time for visiting the margarodid M. hellenica is August-October - after which the weather is too cool for bees (Ermin, 1950; Santas, 1980; 1983). Outside these periods, the bees need other food sources and it is therefore not surprising that the honey from honeydew is mainly tapped by commercial beekeepers wandering over large distances. In addition to requiring licences for setting up their hives, these apiculturists need to be able to reach the honeydew-rich areas and this needs tracks or roads. Thus the opening of new roads into the national forests along the west coast of the United States was described by Pellett (1937) as "opening some promising new bee pastures".

Scale insect honeydew as forage for honey production

299

Clearly the distance of the hives from the honeydew source can have a marked affect on the amount collected. Pechhacker (1977) set up hives at different distances (0, 0.5, 1.0 and 1.5 kin) from trees infested with the lachnid Cinara pectinatae (Nrrdlinger) and found a linear decrease in the amount of honey harvested per hive with increasing distance from the honeydew source. This amounted to about -1.42 kg/100m over a period of 3-6 days - a very substantial effect, which was even greater on rainy, cool days. Another problem for apiculturists is the widespread use of insecticides. Indeed, in Greece a judicial conflict exists between the filbert-tree growers and the apiculturists. P. corni is a major problem on filberts, but Santas (1983; 1985b) has suggested that this problem could be overcome if the sprays against this coccid were applied during its lstor 2nd-instar. At this stage the bees take no notice of the small amount of honeydew that is produced and the scale is at its most vulnerable to the insecticide. The same problem occurs with Pulvinaria pistaciae Bodenheimer on pistachio in Greece (Santas, 1985a) and we know of similar conflicts in Middle Europe associated with cereal fields and orchards (see Kunkel and Kloft, 1985). Indeed, in orchards and forests the honeydew producing insects may not be the target of the sprays but may, nonetheless, be killed along with the pest insects (see Pechhaeker (1974) with regard to P. hemicryphus and P. piceae in Austria). The ability to forecast the availability of honeydew would also be very valuable. The amount of honeydew honey harvested each year varies, as does the exact timing of the maximum honeydew flow. This has been studied by Pechhacker (1976; 1988) who counted the number of 2nd-instar nymphs of P. hemicryphus in winter on particular trees and then compared this with the rate of infestation by young adults, both of which were found to provide good data as to where to place the hives. Another factor which can effect the amount of available honeydew in Middle Europe, where the main honeydew source is soft scales, is the degree of protection given by ants. The effect of ants is to dampen the fluctuations in the populations of the honeydew producers by excluding natural enemies, so that honeydew tends to be more available in the presence rather than in the absence of ants. Thus Wellenstein (1977), when comparing some test forests, obtained 1.7 times more honey in areas protected by ants. In order to increase populations of the honeydew producing coccids, some apiculturists have tried disseminating their eggs and crawlers but apparently without success. This is thought to be due to differential susceptibility of the host trees. Nassonov pheromone has also been tried in an attempt to guide the bees to the honeydew source but again apparently without success (H. Kunkel, unpublished data).

REFERENCES Arnhart, L., 1926. Wer hat die den Tannenhonig liefernde Baumlaus (Lachnuapichme) entdeckt? Archiv ftir Bienenkunde, 7: 257, 260. Barbattini, R., 1988. Produzione di miele della melata di Metcalfa pruinosa (Say). Informatore Agrario, 44:49-51. Barbattini, R., Guimanni, A.G. and Poiana, M., 1988. Composizione durnica della melata e del miele da essa derivata. Ape Nostra Arnica, 10:1%23. Barth, O. M., 1971. Mikroskopische Bestandteile brasilianischer Honigtauhonige. Apidologie (Paris), 2: 157-167. Berner, U., 1967. Die Bienenweide. Ulmer Stuttgart, 222 pp. Bodenheimer, F.S. and Theodor, O., 1929. Ergebnisse der Sinai-Expedition 1927 der Heb~ischen Universitiit, Jerusalem. J. C. Hinrichssche Buchhandlung, Leipzig. 143 pp. Briining, D., 1967. Befall mit Eulecanium corni Bchd. f. robinarium Dgl. und Eulecanium rufulum Ckll. In Dfingungsversuchen zu Laubgeh617.en. Archly fiir Pflanzenschutz, 3: 193-200. Cook, V.A., 1971. Beech honeydew's export potential. New Zealand Journal of Agriculture, 122: 51. Cook, V.A., 1978. Bright prospects for beekeeping. New Zealand Journal of Agriculture, 1978: 24-25. Cook, V.A., 1981. New Zealand honeydew from beech. Bee World, 62: 20-22. Crane, E., Walker, P. and Day, R., 1984. Directory of important world honey sources. International Bee Research Association, London, 384 pp.

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Soft scales as beneficial insects Daghie, V., Cirnu, I. and Cioca, V., 1972. Beitrage zur bakteriziden und bakteriostatischen Wirkung des Lecanienhonigs (Physokermes sp.) aus der Nadelholzzone. XXIII International Congress of Apiculture Moskau (USSR) 1971, Apimondia Publ. House Bucharest (Romania): 619-620. Dalman, J.W., 1826. Om nagra Svenska Arter af Coccus; samt de inuti dem f'6rekommande Parasit-insekter. Kungliga Svenska Vetenskapakademiens Handlinger (Stockholm), 3/4: 350-374. Dalzell, K.W. and Singers, W.A., 1975. A survey of some South Island honeydew honeys. New Zealand Journal of Sciences, 18: 329-332. Ermin, R., 1950. Untersuchungen zur Honigtau- und Tannenhonigfrage in der Tfirkei. Revue de la facult6 des sciences de l'universit6 d'Istanbul, Serie B, 15: 185-224. Fennah, R.T., 1959. Nutritional factors associated with the development of mealybugs in cacao. Report of the Cacao Research Institute Trinidad, 1957-1958: 18-28. Ferrazzi, P., 1983. Insetti fitomizi edapsi: incidenca di melata in mieli dell Italia settentrionale. Atti XII Congress Naziolale Italiano di Entomologia, Sestiere, Torino. Fossel, A., 1956. Steirische Honige. Bienenvater (Wien), 77: 156-163. Fossel, A., 1960. Die Fichtentracht. Bienenvater (Wien), 81: 204-229. Fossei, A., 1963. Die wichtigsten Honigtauerzeuger des Steirischen Ennstales. Mitteilungen der Abteilung fiir Zoologie und Botanik am Landesmuseum "Johanneum" Graz, 16:1-21. Fossel, A., 1974. Die Bienenweide der Ostalpen, dargestellt am Beispiel des steirischen Ennstales. Mitteilungen des Naturwissenschafllichen Vereins Steiermark, 104:87-118. Gates, B.N., 1909. Notes on honey bees gathering honey-dew from a scale insect, Physokermes piceae Schr. Journal of Economic Entomology, 2: 466-467. Gaze, P.D. and Clout, M.N., 1983. Honeydew and its importance to birds in beech forests of South Island, New Zealand. New Zealand Journal of Ecology, 6: 33-37. Geinitz, B., 1958. Waldhonig. Siidwestdeutscher lrnker, 10: 296-300. Gontarski, H., 1940. Beitrag zur Honigtaufrage. Zeitschrift fiir angewandte Entomologie, 27: 321-332. Gontarski, H., 1949. Diirfen wir 1949 Blatthonig erwarten? Die Hessische Biene, 84:116-117. Kaluza, G., 1940. Beitriige zur Kenntnis der Biologic und Anatomic der Fichtenquirlschildlaus Physokermes picieae - Lecanium hemicryphum mit besonderer Berficksichtigung des Honigtaues. Zoologischer Anzeiger, 132: 73-84. Klofl, W., 1959. Unsere Honigtau-Erzeuger. 5. Weitere Napfschildl~use als Honigtau-Erzeuger. Deutsche BienenwirtschaR, 10:71-73. Klofl, W., 1960. Die Honigtau-Erzeuger. Bfidel, A. and Herold, E. (Editors), Biene und Bienenzucht, Ehrenwirth Munich, pp. 105-114. Klofl, W., 1962. Praktisch wichtige Probleme der Honigtau-Forschung. Deutsche Bienenwirtschafl, 13: 240-244. Klofl, W. and Kunkel, H., 1969. Die Bedeutung des Ortes der Nahrungsaufnahme pflanzensaugender Insekten fiir die Anwendbarkeit von Insektiziden mit systemischer Wirkung. Zeitschrifl fiir Pflanzenkrankheiten (Pflanzenpathologie) und Pflanzenschutz, 76: 1-8. K6ster, F. and Stoewesand, H., 1973. Schildl~use als Honigtaulieferanten fiir Kolibris und Insekten. Bonner Zoologische Beitr~ge, 24:15-23. Kunkel, H., 1967. Systematische Ubersicht fiber die Verteilung zweier Erniihrungstypen bei den Sternorrhynchen (Rhynchota, Insecta). Zeitschrifl fiir angewandte Zoologic, 54:37-114. Kunkel, H., 1968. Untersuchungen fiber die Buchenwollschildlaus Cryptococcusfagi B~r. (Insecta, Coccina), einen Vertreter der Rindenparenchymsauger. Zeitschrifl fiir angewandte Entomologie, 61: 373-380. Kunkel, H., 1972. Die Kotabgabe bei Aphiden (Aphidina, Hemiptera). Bonner zoologische Beitriige, 23: 161-178. Kunkel, H., 1973. Die Kotabgabe der Aphiden (Aphidina, Hemiptera) unter Einflu8 von Ameisen. Bonner zoologische Beitr~ge, 24:105-121. Kunkel, H. and Klofl, W.J., 1977. Fortschritte auf dem Gebiet der Honigtau-Forschung. Apidologie (Paris), 8: 369-391. Kunkel, H. and Klofl, W.J., 1985. Die Honigtau-Erzeuger des Waldes. In: W.J. KIoR and H. Kunkel (Editors), Waldtracht und Waldhonig in der Imkerei. Ehrenwirth Munich, pp. 47-265. Mengel, K., 1968. Funktion und Bedeutung des Kaliums im pflanzlichen Stoffwechsel. Naturwissenschaflliche Rundschau (Stuttgart), 8: 332-336. Michel, E., 1942. Beitriige zur Kenntnis von Lachnus (Pterolachnus) roboris L., einer wichtigen Honigtauerzeugerin an der Eiche. Zeitschrifl flit angewandte Entomologie, 29: 243-281. Morales, C.F., 1991. Margarodidae (Insecta: Hemiptera). Fauna of New Zealand/Kote Aitanga Pepeke o Aotearoa, no. 21 : 4-123. Morales, C.F., Hill, M.G. and Walker, A.K., 1988. Life history of the sooty beech scale (Ultracoelostoma assimile) (Maskell), (Hemiptera: Margarodidae) in New Zealand Nothofagus forests. New Zealand Entomologist, 11 : 24-37. Nicolaisen, N., 1923. (Short communication: Dfingemittel Kali und Kalk, ein erfolgreiches WurzelBlutlausvertilgungsmittel). Deutsche Obst- und Gemfisezeitung, 18: 10. Nicolopoulos, C.N., 1965. Morphology and biology of the species Marchalina hellenica (Gennadius) (Hemiptera" Margarodidae" Coelostomatiinae). F_.colede Haute I~tudes Agronomiques a Athenes, Laboratoire de Zoologie Agricole et de S6riculture. 31 pp. (in Greek).

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Pechhacker, H., 1974. Uber die Wirkungen chemischer Forstsch/idlingsbekiimpfungen aus der Lufl auf Honigtau-Erzeuger und Ameisen. Anzeiger fiir Schiidlingskunde. Pflanzen-Umweltschutz (Berlin und Hamburg), 47: 42-45. Pechhacker, H., 1976. Zur Vorhersage der Honigtautracht yon Physokermes hemicryphus Dalm. (Homoptera, Coccidae) auf der Fichte (Picea excelsa). Apidologie (Pals), 7: 209-236. Pechhacker, H., 1977. Die wirtschaflliche Bedeutung der Entfernung der Trachtquelle vom Aufstellungsort der Bienen. Apiacta, 12: 15-18. Pechhacker, H., 1984. Zur Populationsentwicklung der Physokermes-Atren. Dissertation (Ph.D.) Universitiit fiir Bodenkulter, Wien. 282 pp. Pechhacker, H., 1988. Zur langfristigen Vorhersage der Physokermes-Fichtentracht. Apidologie (Paris), 19: 73-84. Pellett, F.C., 1937. New bee pastures. American Bee Journal (Hamilton HI.), 77: 181. Pellett, F.C., 1976. American Honey Plants. Dadants and Sons, Hamilton HI., 467 pp. Pesson, P., 1944. Contribution h l'Etude morphologique et fonctionelle de la Tete, de'Appareil Buccal et du Tube Digestiv des Femelles de Coccides. Monographies Publiies par les Stations et Laboratoires de Recherches Agronomiques. ParAs, Imprimeie Nationale, 266 pp. Putnam, J.D., 1880. Biological and other notes on Coccidae. I. Pulvinaria innumerabilis. Proceedings of the Davenport Academy of Science, 2: 293-346. Ratzeburg, J.Th.Ch., 1844. Die Forst-lnsecten etc. Dritter Theil. Die Ader-, Zwei-, Halb- und Geradflfigler. Berlin. 314 pp + 16 tables. Reichholf, H. and Reichholf, J., 1973. "Honigtau" der Bracaatinga-Schildlaus als Winternahrung von Kolibris (Trochilidae) in Sfid-Brasilien. Bonner zoologische Beitr~ge, 24: 7-14. Ruttner, R., 1956. Oberistereichische Honige. Bienenvater, 77: 82-90. Ruttner, R., 1960. Waldtracht und Waldtrachtbeobachtungen in Osterreich. Bienenvater, 81 : 196-203. Santas, L.A., 1980. Marchalina hellenica (Gen.) an important insect for apiculture of Greece. XXVII International Congress of Apiculture Athens (Greece) 1979. Apimondia Bucharest (Romania): 445--448. Santas, L.A., 1983. Insects producing honeydew exploited by bees in Greece. Apidologie, 14: 93-103. Santas, L.A., 1985a. Anapulvinaria pistaciae (BOd.), a pistachio tree scale pest producing honeydew foraged by bees in Greece. Entomologia Hellenica, 3: 29-33. Santas, L.A., 1985b. Parthenolecanium corni (Bouchi), an orchard scale pest producing honeydew foraged be bees in Greece. Entomologia Hellenica, 3: 53-58. Santas, L.A., 1988. Physokermes hemicryphus (Dalman), a fir scale insect useful to Apiculture in Greece. Entomologia Hellenica, 6:11-21. Santas, L.A., 1989. Species of honeydew producing insects useful to Apiculture in Greece. Entomologia Hellenica, 7: 47-48. Scheller, W., 1932. Ist die Kalidfingung ein Bekiimpfungsmittel gegen Blutlaus? Erfurter Fiihrer durch Obstund Gartenbau, 33: 237. Schmalfuss, K., 1933. Untersuchungen fiber den Eweigstoffwechsel yon Kalimangelpflanzen. Phytopathologische Zeitschrift, 5: 207-249. Schmutterer, H., 1952a. Die Okologie der Cocciden (Homoptera, Coccoidea) Frankens. Zeitschrifl fiir angewandte Entomologie, 33: 369-420, 544-584; 34: 65-100. Schmutterer, H., 1952b. Die Lebensbaumschildlaus Eulecanium arion Lgr. (Homoptera, Coccoidea), die Erzeugerin des Lebensbaum-Honigtaues. Zeitschrit~ ffir Bienenforschung, 1: 128-132. Schmutterer, H., 1954. Zur Kenntnis einiger wirtschaRlich wichtiger mitteleurop~ischer Eulecanium-Arten (Homoptera, Coccoidea, Lecaniidae). Zeitschrifl tiir angewandte Entomologie, 36: 62-83. Schmutterer, H., 1956. Zur Morphologie, Systematik und Bionomie der Physokermes-Arten an Fichte (Homoptera, Coccoidea). Zeitschrifl fiir angewandte Entomologie, 39:445-466 Schmutterer, H., 1958. Die Honigtau-Erzeuger Mitteleuropas. Zeitschrifl fiir angewandte Entomologie, 42: 409-419. Schmutterer, H., 1965. Zur 0kologie und wirtschafllicher Bedeutung der Physokermes-Arten (Homoptera, Coccoidea) an Fichte in SiJddeutschland. Zeitschrif~ fiir angewandte Entomologie, 56: 300-325. Schmutterer, H. and Klofl, W., 1957. Coccoidea, Schildliiuse, Scale insects, Cochenilles. Handbuch der Ptlanzenkranldaeiten, 4. Lief., 5 Aufl., V: 403-520. Smirnoff, W.A. and Valero, J., 1975. Effets h moyen terme de la fertilisation par urie ou par potassium sur Pinus banksiana L. et le comportement de ses insectes divastateurs: tel que Neodiprion swainei (Hymenoptera, Tenthredinidae) et Toumeyella numismaticum (Homoptera, Coccidae). Canadian Journal of Forest Research, 5: 236-244. Stern, J., 1841. Ueber Honigthau und den sogenarmten Waldhonig. Monatsblatt ftir die gesammte Bienenzucht (Landshut), 4: 49-60. Tsankov, G., Petkov, V. and Ivanow, Ts., 1983. (A study of honeydew-producing insects and of the chemical composition of honeydew and honeydew honey). Rastenievudni Nauki (Sofia), 20: 133-144. Thiem, H., 1938. Uber Bedingungen der Massenvermehrung yon Insekten. Arbeiten fiber physiologische und angewandte Entomologie aus Berlin Dahlem. Biologische Reichsanstalt fiir Land- und ForstwirtschaR (Berlin), 5: 229-255. Walton, G., 1979. Beech honeydew honey - a vast potential. New Zealand Beepractice, 40: 6-9.

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Wellenstein, G., 197"/. Die Grundlagen der Waldtracht und M6glichkeiten ihrer bienenwirtschafllichen Nutzung. Zeitsehrit~ fiir angewandte Zoologie, 64: 291-309. White, J.W.Jr., Riethof, M.L., Subers, M.H. and Kushnir, I., 1962. Composition of American honeys. Technical Bulletin of the U. S. Department of Agriculture No. 1261, 124 pp. Williams, D.J., 1983. Some aspects of the zoography of scale insects (Homoptera: Coecoidea). In: Z. Kaszab (Editor), Verhandlungen des 10. Internationalen Symposiums fiber Entomofaunistik Mitteleuropas (Verb. SIEEC X. Budapest 1983), pp. 331-333. Vansell, G.H., 1932. Scale insect honeydew from incense cedar. American Bee Journal (Hamilton Ill.), 72: 364. Zoebelein, G., 1956. Der Honigtau als Nahrung der Insekten. Zeitsehrifl Rir angewandte Entomologie, 38: 369-416; 39: 129-167.

Soft Scale Insects - Their Biology, Natural Enemies and Control Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.

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1 . 2 . 3 . 2 The Pela Wax Scale and Commercial Wax Production TING-KU! QIN

INTRODUCTION Scale insects usually protect themselves by secreting wax to cover their bodies. In the family Coccidae, many species produce a large quantity of wax either covering their body or as an ovisac to protect their eggs. Some species of soft scales are regarded as beneficial because they produce wax useful to humans. In particular, the wax produced by the male nymphs of Ericerus pela (Chavannes) and the adult females of some species of Ceroplastes Gray have been utilised for many purposes. This Section deals mainly with wax production by E. pela since it is the only soft scale being used successfully in commercial wax production. However, the wax production of some species of Ceroplastes are also briefly discussed. Ericerus pela has been known by at least ten English names, e. g. wax-producing coccid (Sasaki, 1904), Chinese white wax scale (Kuwana, 1923; Wu, 1980a, b), Chinese wax scale (Essig, 1942), white wax scale (e.g. Wu and Zhoug, 1983; Jiang et al., 1984; Wu, 1987; Wu et al., 1988; Wu and Gao, 1990; Zhao and Wu, 1990; Wu et al., 1991), white wax insect (e.g. Zhang et al., 1990), China wax scale insect (Li, 1985), prototype wax scale (Brown, 1975), wax insects (Chou, 1990), Chinese scale insect (Waku and Foldi, 1984), and pela insect (Zhang, 1984). Some of these names can be confused with those of other species of wax scales, such as white wax scale for Ceroplastes destructor Newstead (e.g. Beattie et al., 1990) and Chinese wax scale for C. sinensis Del Guercio (e.g. Gimpel et al., 1974; Beattie et al., 1990). In order to avoid further confusion, "Pela wax scale" is used in this Section. "Pela" is a pronunciation of Chinese word meaning "white wax'. Moreover, this name relates to both the colloquial and scientific names. The commercial product of the wax produced by E. pela has been widely known as "China wax" outside China (e.g. Chiao and Pen, 1940; 1943; Takahashi and Nomura, 1982; Li, 1985) although there are other local names inside China (Wu, 1989). Therefore, the term "China wax" is employed here for the commercial product of E. pela wax.

HISTORY AND STUDY OF PELA WAX SCALE Ericerus pela is one of the oldest beneficial insects (after silk worms and honeybees) recognised by humans, having been reared for its wax for more than a thousand years. In China, it was recorded that in the Tang dynasty (618-907 A.D.) local governors offered China wax as a special gift to the emperor (Zou, 1981, see Li, 1985). This

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Soft scales as beneficialinsects suggests that the rearing of E. pela in China is at least as old as the Tang dynasty. However, the earliest detailed records of breeding are from the Song dynasty (960-1279 A.D.) (Chou, 1990). During the Ming dynasty (1368-1644 A.D.), the insects were reared and studied in great detail in several important works (e.g. Wang, 1566; Li, 1578; Xu, 1639; see Chou,1990). These authors also discussed the different species of host plants, the distribution and habitats of the insects and the methods of collecting and processing the wax. N. Trigault, a Christian missionary, was the first European to observe the pela wax scale and wrote about wax collection in southern China in 1651 (see Chou, 1990). The news about pela wax scale spread to Europe in the eighteenth century. In 1847, this wax scale was recorded as a new species by Chavannes, who named it Coccus pela according to the pronunciation of the Chinese name "pela'. Lockhat sent samples of China wax and the pela wax scale to England from Shanghai for research in 1853, and Lichtoffen learned the techniques of collecting China wax in Sichuan in 1872 and recorded it in his travel letters (see Chou, 1990). Extensive literature is available on different aspects of E. pela and its wax production, including a number of books (e.g. Xu, 1959; Shaanxi Province Biological Resource Survey Team, 1974; Wang, 1978; Wu, 1989). Research on E. pela is still carried out in various parts of China but the three main research centres are: the Department of Biology, Sichuan University, Chengdu (led by Wu Ci-Bing and Zhong Yuan-Hui), the Southwest Agricultural University, Chongqing (led by Wang Fu), and the Shaanxi Institute of Zoology, Shaanxi (led by Zhang Zi-You and Shao Meng-Ming). The research at Sichuan University has been expanding to many new areas, including the measures needed to increase wax production (Wu, 1981), bionomics (Wu and Zhong, 1983), use of hybrid vigour (Wu, 1987), comparative studies of economic characters from different regions (Wu et al., 1988), male wax glands (Tan and Zhong, 1989), male reproductive system (Wu and Gao, 1990), female neurosecretory system (Peng and Zhong, 1990) and a study of embryonic development (Zhao and Wu, 1990).

BIOLOGY OF PELA WAX SCALE Geographical distribution The Pela wax scale is native to China and has been recorded from 18 provinces (Fig. 1.2.3.2.1). Wang (1963) suggested that E. pela was confined to 26-33 ~ N and that the most suitable region was between 26-29 ~ N. However, Wu (1980a, 1989) disputed Wang's (1963) statements and indicated a wider range from 23044 ' N to 41~ N, 85008 ' E to 121~ E (actually 124035 , E in Benxi, Liaoning province, according to Wu (1989)), and from almost sea level to 2800 metres altitude. In this area, the temperature ranges from -30.4 ~ to 44 ~ indicating that the insects are adapted to a broad range of climatic conditions. Wu's conclusions are supported by Zhang et al. (1986) who recorded natural populations of E. pela at Yongde county, Yunnan, which extends to south of 24 ~ N latitude. Zhang et al. (1990) claimed that the E. pela population occurring in the lower reaches of Jinshajing River, a contiguous area to Yunnan, Sichuan and Guizhou provinces, produced more eggs, had a higher male egg sex ratio, a longer wax-secreting period, a higher wax-producing capacity and therefore higher outputs of wax. Sasaki (1904) considered that E. pela was also native to Japan. Recently, the insect has been recorded from the Primorye Territory of Russia (Danzig, 1965) and from Korea (Paik, 1978). Some authors (e.g. Takahashi and Nomura, 1982; Wu, 1989) have mentioned that E. pela occurs in Europe; but no specific European countries have ever been given.

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r

MONGOLIA ,

H i-'--

I /

/

r

N~'~A

..m

Fig. 1.2.3.2.1. Distribution of Ericeruspela in China. Betweendashed lines: general distribution; Diagonal shading: main region of wax production (Sichuan); horizontal shading: some wax production; black dots: west-, east-, north- and south-most recorded distributions; triangles: distribution in countries other than China. Commercial wax production regions in China China wax is produced mainly in Sichuan province but also in Hunan, Yunnan, Guizhou, Zhejiang, Shaanxi and Shanxi provinces (Fig. 1.2.3.2.1). Historically wax (males) and "seed" (females) production, occurred in separate regions and so males and females were considered to have different ecological requirements (Wang, 1963, 1978). However, Wu (1980a, 1980b) argued that, in order to reproduce successfully, males and females of E. pela should have the same ecological requirements (e.g. climate and host plants) and stated that both the seed and the wax could be produced in the same environments. The historical separation of wax and seed production regions is due to the different purposes of the production. Wu's statements were confirmed by Zhang (1984) who found that the commercial China wax could also be produced in the subtropical regions of Yunnan. Life cycle of pela wax scale In traditional areas of China wax production, E. pela has one annual generation (Fig. 1.2.3.2.2). However, in the subtropical region (Jingdong, Yunnan province), Zhang (1984) found that E. pela only need 10 or 10.5 months to finish a generation. Danzig (1965) noticed that E. pela needed two years to complete one life cycle in southern Primorye, Far East Russia. After analysing the ecological factors affecting the distribution of E. pela, Ke (1981) suggested that this insect may complete two generations annually in the tropics, one generation in the subtropics and a half generation in cold temperate regions.

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Soft scales as beneficial insects

F

F2

MATING

~gd

"

M1

M2

M3

,

~d

M4

Fig. 1.2.3.2.2. Life cycle of Ericerus pela. E: eggs; FI: first-instar female; F2: second-instar female; MI: first-instar male; M2: second-instar male; M3: prepupa; M4: pupa; MS: adult male.

General biology The biology of E. pela has been studied in the univoltine regions by many authors (e.g. Sasaki, 1904; Kuwana, 1923; Chiao and Peng, 1943; Wang, 1963; Cheng, 1974; Zhang and Shao, 1982; Wu and Zhong, 1983; Zhang, 1984; Li, 1985; Wu, 1989). The following description of the life cycle is mainly based on the studies by Cheng (1974), Wu and Zhong (1983) and Wu (1989). The females of E. pela pass through three life stages: first- and second-instar nymphs and adult female; and the males through five stages: first- and second-instar nymphs, prepupa, pupa and adult male. Many soft scale species have three immature stages in the female but E. pela only has two.

i. Egg laying and hatching After overwintering, the fertilised females start laying eggs from as early as the beginning of February to as late as the middle of May in some regions. The number of eggs laid by each female varies greatly depending on the size of the female, ranging from 3,372 (Kuwana, 1923) to 18,047 (Wu and Zhong, 1983). The eggs take 20-34 days to develop. The newly hatched nymphs are pale, soft and feeble, and remain under the female body, but after about 5 days they have become hard and active and are ready to crawl out.

ii. First-instar nymph The yellow or red brown female nymphs become very active and emerge from beneath the female body. They wander on the branches first and then crawl towards a leaf and settle on the upper surface along the veins but do not congregate in groups. They feed there for a half to one month without moving, and this period is called "fixing leaves" or Ding Ye in Chinese. The hatching and emergence of the yellow-white male nymphs is always several days later than the females (usually 2-4, occasionally 6-11). Their behaviour differs from that of female nymphs in that, instead of settling on the upper surface of leaves, they congregate on the under surface and feed there for only two weeks.

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iii. Second-instar nymphs and subsequent stages After the first moult, the second-instar females move from the leaves and settle on 2-3 year-old branches. This is called "fixing stems (Ding Gan in Chinese)" or "fixing branches". The head faces downwards and the abdomen upwards. After the second moult, the adult females appear in late August or September. The second-instar males migrate from the leaves to 2-3 year-old branches and settle, congregating around the branch. In contrast to the female, the head of male faces upwards. Males settle on the leaves after the females but appear on the branches before them. In late August to early September, second-instar males moult into prepupae and stop secreting wax. They become pupae 3-5 days later and the adult males emerge after another 4-8 days. Two to three days after emergence, the males fly off in search of adult females with which to mate. They die shortly afterwards. Males usually live for only 2-5 days. iv. Overwintering After mating, the body of the adult female only gradually enlarges until the following February, but then swells drastically, and when it reaches a length of 3 ram, the body starts to secrete sweet-scented drops (probably honeydew) (Diao Tang in Chinese) (Li, 1985, fig. 4), eventually becoming ball-like and reaching 8-10 (some 14) mm in diameter. The female then begin to lay eggs. Egg-laying lasts for about 10 days and the sweet-scented drops disappear. The eggs are deposited in a cavity beneath the female body. v. Sex ratio The sex of E. pela can be distinguished at every stage including eggs (male egg: pale yellow; female egg: slightly brownish). The sex ratio directly affects wax yields: the more males, the more wax. The sex ratio varies in different populations among the progeny of adult females of different sizes and from different host plants (Wu and Zhong, 1983; Wu, 1989; Zhang et al., 1990). Wu (1989) observed that the ratio of hatching nymphs is usually between 1" 1 and 5" 1 male to female with some extremes (0.12:1 or 6.1:1). Zhang et al. (1990) studied the egg sex ratio of populations from the main wax-production regions (Sichuan, Yunnan and Guizhou) and found that the highest male to female egg sex ratio was from Yunnan province (average 2.23:1, range between 0.25:1 and 22.27:1). vi. Host plants Pela wax scale has been recorded on about 40 species and subspecies of host plants (Table 1.2.3.2.1) mostly in two genera of the family Oleaceae. However, only ash, Fraxinus chinensis Roxb., and privet, Ligustrum lucidum Ait., are widely used to produce China wax, although L. quiboni Carr., L. acutissimum Koehnen and L. compactum Hook are also used in some parts of China. Natural enemies Wu (1989) reviewed information on the natural enemies of E. pela and its host plants and provided advice on their control.

i. Natural enemies of Ericerus pela Several groups of organisms have been reported to attack pela wax scale and these include parasitoid wasps, weevils, coccinellids, bagworm moths, spiders, birds and

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fungi. The parasitoid wasps and the weevils are widespread and are probably the most important natural enemies.

TABLE 1.2.3.2.1 Host plants of Ericerus pela (Chavannes). m_ Species names follow the spelling in "Index Kewensis"; names spelt differently by the original authors; b _ names not found in "Index Kewensis"; " - host plants widely used for wax production. "

Host plants #

References

Oieaceae Chionanthus retusa Lindl. & Paxt.' Fraxinus americana Lima. F. bungeana DC. F. bungeana pubinervis Wangeuh. F. chinensis Roxb.* F. chinensis rhynchophylla (Hance)" F. griflithii C.B. Clarke F. hopeiensis Tang F. longicuspis Sieb & Zucc. F. mandschurica Rupr." F. mariesii Hook.f. F. platypoda Oliv. F. paxiana Lingelsh. F. pubinervis BI. F. retusa Champ. F. sinensis [?=chinensis] b Ligustrum acutissimum Koehne L. amurense Cart." L. compactum Hook.f &Thoms. ~ L. delavayanum Harlot. L. glabrum b L. henryi Hemsl. L. ibota Sieb. L. japonicum Thunb. L. lucidum Ait.* L. medium Franch. &Sav. L. obtusifolium Sieb. &Zucc. L. quiboni Carr. L. robustum BI. L. sinense Lour." L. sinense nitidum Rehd. L. sinense stantonii Rehd. Syringa josikaea Jacq.f. Anacardiaceae Rhus succedanea Lima." Aquifoliaceae llex sp. Celastraceae Celastrus ceriferus b Malvaceae Hibiscus syriacus Linn. Verbenaceae Vitex sp.

Kuwana, 1923; Danzig, 1965 Wu, 1989 Cheng, 1974; Wu, 1989 Kuwana,1923 Cheng, 1974; Wu, 1989 Danzig, 1965; Cheng, 1974; Wu, 1989 Wu, 1989 Wu, 1989 Kuwana, 1923; Danzig, 1965 Wu, 1989; Danzig, 1965 Cheng, 1974; Wu, 1989 Wu, 1989 Wu, 1989 Sasaki, 1904 Wu, 1989 Blanchard, 1883 Cheng, 1974; Wu, 1989 Danzig, 1965 Wu, 1989 Cheng, 1974; Wu, 1989 Blanchard, 1883 Wu, 1989 Sasaki, 1904; Kuwana, 1923 Sasaki, 1904; Wu, 1989 Blanchard, 1883; Cheng, 1974; Wu, 1989 Kuwana, 1923; Danzig, 1965 Wu, 1989 Cheng, 1974; Wu, 1989 Cheng, 1974; Wu, 1989 Cheng, 1974; Wu, 1989 Cheng, 1974 Cheng, 1974 Danzig, 1965 Blanchard, 1883; Danzig, 1965 Tang, 1991 Blanchard, 1883 Blanchard, 1883 Danzig, 1965

(a) Wasps: Pela wax scale is host to 13 species of parasitoids (Wu, 1989), of which three are important: Microterys ericeri Ishii, M. sinicus Jiang and Tetrastichus sp. Jiang et al. (1984) studied the morphology, biology and control of M. ericeri and found that the wasp had 6-7 generations per year. The parasitoid larvae overwinter in the female scale, and the adults emerge and lay their eggs inside both female and male scales. Up to 45.3 % of males and 52.8 % of females of E. pela can be parasitised. (b) Weevil: the weevil, Anthribus lajievorus Chao, occurs in every wax production region. The adults bite the cuticle of the scale and fee~ on the body fluid. They lay their eggs inside the body after biting a hole and, upon hatching, the larvae eat the

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scale's eggs. Anonymous (1976) studied this weevil in detail and found that up to 95.2 % of E. pela could be damaged by the weevil. (c) Coccinellids: two species of coccinellids: Chilocorus kuwanae Silvestri and C. rubidus Hope prey on the scale, but only the latter is important and specialises in preying on the male scales. There is one generation a year and each beetle can eat 10-13 thousand male scales during its life (Wu, 1980c; 1989). (d) Bagworm moths: apart from feeding on the host plants of E. pela, many bagworms also prey on the wax and the enveloped males. The important bagworms are Cryptothelea minuscula Bulter and C. variegata Snellen (Psychidae) (Wu, 1989). (e) Spiders: many spiders spin their webs on the host plants. These webs can trap the adult males when they are flying in search of mates (Cheng, 1974). (f) Birds and rodents: during the sweet-scented drop (probably honeydew production) period, rodents and many birds such as Phoenicrurus auroreus Pallas, Parus major Linnaeus and Pycnonotus sinensis (Gmelin) feed on the female scales (Cheng, 1974). Bird damage can reach up to 91.8% (Wu, 1989). (g) Fungi: Gloesporium sp. causes death of the females of E. pela; 40-83 % of the insects can be infected (Wu, 1989).

ii. Natural enemies of the host plants Apart from natural enemies feeding directly on E. pela, many other organisms can seriously damage the host plants, thus reducing wax production. Moreover, some natural enemies feed on both the insects and the plants (e.g. bagworm moths). Wu (1989) listed 19 species of insect pests belonging to the orders Lepidoptera, Coleoptera, Hemiptera, Orthoptera and Hymenoptera. The most important pests of the host plants varied between regions and between seasons but the armoured scale Pseudaulacaspis pentagona (Targioni Tozzetti) (Diaspididae), the sawfly Macrophya fraxina Zhow & Huang (Tenthredinidae) and the fraxinus aphid Prociphilus fraxini (Fabricius) (Aphididae) are among the most important ones.

Wax secretion and wax glands 1. Wax secretion Females: the wax secreted by the females is of no economic value. First- and second-instar females only secrete a small amount of wax from the spiracular pores, while the adult females secrete a thin layer of wax from tubular ducts on the dorsum and a small amount of white wax from the tubular ducts, multilocular disc-pores and spiracular disc-pores on the venter. Males: the first-instar males start secreting wax filaments 2 to 3 days after "fixing leaves". The wax covers the whole body after 6 or 7 days, although this layer is thin and of no economic value. The useful wax is produced by second-instar males. The density of the fixing area is about 200 individuals per square centimeter and the length of the settling area is 1-1.5 metres. Two to three days after "fixing branches", the male nymphs begin to produce wax filaments (Figs 1.2.3.2.3. A, B). The wax is secreted from the wax glands (details below) associated with tubular ducts (Fig. 1.2.3.2.3. C) on the dorsal and ventral surfaces (Fig. 1.2.3.2.2, M2). Initially, very little wax is secreted, but as the body grows, more and more wax is produced. Eventually, the wax is from 5-10 mm in thickness and entirely envelops the whole aggregation of insects and their branches (Fig. 1.2.3.2.4. A). This is called "wax flowers'. After the moult to the prepupa, wax

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secretion nearly stops. The prepupae, pupae and adult males produce only small amounts of wax. Wu (1989) indicated that second-instar males begin to secrete wax each day at 10 am, with peak daily secretion between 12 noon and 11 pm, and then gradually decreasing.

2. Number and structure of wax glands in the male Tan and Zhong (1989) studied in detail the wax glands in each stage of the male. The wax glands develop from specialised epidermal cells. There are few glands in the first instar but the number gradually increases as the insects grow. The second instar has the highest number of wax glands (about 300), which mature, secrete wax and then degenerate. There are extremely few wax glands in the prepupae. Pupae have no wax glands but a glandular pouch develops on each side of the base of the penial sheath, and each glandular pouch contains a long seta arising from its base (Giliomee, 1967). There are many pygidial gland units (Tan and Zhong, 1989) in each glandular pouch, and these glands mature and secrete a waxy substance which slides along the setae and forms the 2 conspicuous long waxy filaments (4-6 mm) of the living adult male (Giliomee, 1967; Tan and Zhong, 1989) (Fig. 1.2.3.2.2, M5; Fig. 1.2.3.2.4. B). A wax gland of a male nymph consists of a central cell, 3-5 (usually 4) lateral cells, 2 canal cells, a duct with an inner ductule and a terminal knob (Tan and Zhong, 1989, fig.4 [but terminology following Foldi, 1991]). Noirot and Quennedey (1974) divided the gland cells of insects into three classes and Tan and Zhong (1989) regarded the gland cells of E. pela as belonging to class 3, i.e. the canal cell secretes a cuticle canal which penetrates the gland cell and opens to the outside (Noirot and Quennedey, 1974, Fig. 3; Waku and Foldi, 1984). Foldi (1991) recognised five types of wax glands in scale insects and the wax gland of E. pela can be classified into his type 2 (Foldi, 1991, Fig. 2), which he called ducted wax glands. 3. Wax secretion periods in the second-instar male Tan and Zhong (1989) studied the development of the wax glands in the second-instar male nymphs, because the most useful wax is produced by this stage. They recognised five periods with two peaks of secretion: Period I (starting from "fixing branches" and lasting about 25 days): the number and size of the wax glands increase during this period. The average growth of dorsal glands is 0.8-2. l#m/day and that of ventral glands is 1.25~tm/day. The diameter of a dorsal gland ranges from 7.5-37.5#m; that of a ventral gland is 12.5-25.0#m. Mature wax glands are mostly on the dorsolateral parts of the body. Period II (days 25-35): the first peak of wax production occurs in this period, mainly by the dorsal wax glands. The thickness of the wax secretion increases from 0.3 #m/10 days to 1.3 #m/10 days. Most dorsal wax glands then stop growing and the ventral wax glands grow slightly (0.3#m/day) at the end of this period. Period III (days 35-65): at the beginning of this period, some wax glands continue to grow and secrete wax, although those that have already secreted wax begin to degenerate and disintegrate. Period IV (days 65-75): during this period, the second peak of wax secretion takes place, with the secretion being produced by the regenerated wax glands mostly located on the abdomen (at a rate of 1.4#m/day increase in diameter). The wax deposition increases from 0.5 #m/10 days to 1.4 #m/10 days. The number of the wax glands is smaller than in period II but there are more oenocytes around the wax glands and this suggests that the oenocytes probably play an important role in the biosynthesis of the wax.

Period V (days 75-85): most of the wax glands degenerate and only some newly developed glands still grow.

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Fig. 1.2.3.2.3. Ericerus pela (Chavannes), male second instar. A - Scanning electron micrograph of the wax filaments produced by the second-instar male, showing numerous broken wax filaments; scale line: 10 Ira1. B - Scanning electron micrograph of the wax filaments (each 5-6 #m in diameter) produced by the second instar male; enlargements of several wax filaments; note the two types of filaments - smooth surface and longitudinally ridged surface; scale line: 5 #m. C - Tubular duct (13-16 #m long, 5-7 #m in diameter) of the second-instar male. A wax filament is secreted through this tubular duct to the cuticular surface; scale line: 5 #m.

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SoJ~ scales as beneficial insects

PRODUCTION OF PELA WAX SCALE AND ITS WAX "In the production of E. pela and its wax, the insects are the key, the trees are fundamental and the wax is the goal or objective" (Wu, 1989, p. 115). A sophisticated procedure has been developed during the long history of its cultivation. The methods are generally labour intensive. Many key steps have been summarised as easily remembered jingles, such as the one cited above. This section will outline briefly the methods of breeding E. pela for the purpose of wax production.

Seed production The following is mainly after Wu (1989): the females do not produce useful wax but they provide the source of the insects and are thus called " s e ~ ' . The place where the seed is produced is called the "seed source" (Chong Qu) and the place where the wax is produced is called the "wax source" (La Qu). The ~ source and the wax source should be separated in different fields (preferably in the same area to avoid long distance transportation) because the natural enemies in seed sources may continue to attack pela wax scale in wax sources if these are in the same field. In April and May, overwintered seeds (females with eggs, also termed "egg capsules" below) are collected from the fields (Li, 1985, Fig. 5). There are criteria to determine if the seed females are ready to be collected: the colour (red brown), the flexibility (when pushing the dorsum of the body, the touched areas should return to the original position) and the dryness (the body becomes dry). The collected seed insects need to be kept in cool, dry conditions until the egg capsules become hard. Then, large egg capsules which contain large numbers of eggs are selected for establishing new cultures. Once most female nymphs have hatched and some have crawled onto the surface of the egg capsules, they are ready to be wrapped in small bags (3-6 egg capsules per bag) and this process is called "wrapping insects" (Bao Chong in Chinese). When some female nymphs are found moving on the surface of the bags, the bags are hung on the appropriately pruned host plants and this is called "hanging bags" (Gua Bao in Chinese). After the crawlers have been released, care is needed in controlling natural enemies and in cultivating the host plants until the next generation of s e ~ is ready to be collected. These seed females are used for two purposes: either as a source for the next production (i.e. females) or as a source of males for wax production. The exposure of the seed to neutrons produced by decay of Americium-Beryllium (dose = 1 X 104n/cm2, 1 X 105n/cm2 or 1 X 106n/cm2) can significantly increase the wax production. Wu (1989) reported that the exposure of seed to the above three doses of neutrons resulted in an 11-38 % increase in average wax yield. Historically, the wax sources and the s e ~ sources are widely separated, even in different provinces. Therefore, it is necessary to transport the ~ from the source to the wax source. After the seed insects are picked from the trees, they are allowed to dry before packing. They are then packed in a linen or paper bag (about 30 x 24 cm) of gross weight 1.5 kg. The packed bags are transported by person, truck or aeroplane, depending on distance. Great care is required during transportation to avoid damage to the insects due to crowding and heating, and to avoid the nymphs from hatching too early.

Wax production 1. Release of male nymphs The seeds for wax production are kept indoors until the eggs hatch. The process of "wrapping insects" for the wax production is later than for the s e ~ production because the male crawlers always hatch after crawler female. The egg capsules are ready to be wrapped for the wax production when 80-90% of the yellow- or red-brown female crawlers appear on the outside of the shells and some yellow-white male crawlers begin to appear. Basically, the delay in wrapping insects allows the earlier-hatched females to die, so that only male crawlers are released onto the tree. There are two means of

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determining the appropriate time for releasing the male crawlers" (1) random checking of several bags to see if most male crawlers have moved to the inside of the bag. If they have, they should be released immediately; and (2) hanging a couple of bags on a tree in the morning and if many male crawlers have crawled onto the tree and moved towards to the leaves at noon, the crawlers are ready to be released. If the crawlers remain around the bags, it means that they are not ready to be released. The egg capsules can be maintained at 18"C because the nymphs begin to hatch at above 15~ but are inactive below 180C, and so this allows the eggs to hatch but the nymphs do not move out of the shells. After all the nymphs have hatched, the bags can be hung on the trees at the same time so that all the crawlers can settle on leaves in a very short time, thus reducing the loss of insects during the process of "fixing leaves'. The time for "hanging bags" is usually in early May and the best position is from young branches near leaves because male crawlers are not as active as females, and once they leave the bag, they move up and immediately fix on leaves. 2. Post-release management Once the insect bags have been hung in the tree, the greatest threat is from storms which wash away the male nymphs. Therefore, during inclement weather, the bags are brought indoors and then hung out again after the storm. Management after release is summarised as follows: (1) examine the progress of "fixing leaves" and, if the leaves are too crowded, move some bags to another tree on which fewer insects are "fixing leaves'; (2) collect fallen leaves or bags and return them to the trees if they still have male nymphs; (3) monitor and control the natural enemies, for example, adult and larval coccinellids of C. rubidus; these are dislodged by hitting the tree regularly every 2-3 days using a stick and then killing the beetles on the ground; (4) fertilise the host trees to provide nutrients to encourage the males to produce more wax; (5) prune the flowering and newly developed branches because they consume plant resources which otherwise would be available to the scale. 3. Harvesting wax flower The Wax flower is the thick wax which completely envelops the aggregation of second-instar male nymphs and their branches (Fig. 1.2.3.2.4. A). When the wax surface is full of small holes with two long white waxy filaments extruding from each hole (Fang Jian in Chinese) (Fig. 1.2.3.2.4. B), the nymphs have become pupae and wax secretion has stopped. Once the first white filaments appear, the nymphs under the wax are checked and, if their body is pale yellow-brown with a black dorsum to the thorax, the wax flower is ready to be collected. If the insect's body has become brown, the wax flowers should be collected immediately because the males will emerge very soon. The quality and quantity of the wax may be reduced if collected too early or too late after male emergence. The wax can be collected easily when wet and therefore the most suitable weather for collection is light rain, or just after rain, or on a free morning before the dew has dried. If wax collection is done at noon or in the afternoon of a dry day, the wax should be sprayed with clean water before collection, otherwise part of the wax will remain on the tree or the wax will be easily broken and fall to the ground. There are two methods of collection: "cutting branches" or "leaving branches". If the branches are weak and have already been used twice, the wax-laden branches are cut down, and this allows new shoots to grow. If the branches have been used only once, they should still be strong and healthy, and should be left to rest for a year before being used again; in this case, the wax is scrapeA off and the branches are retained. Preferably the wax should be processed on the day of collection, but if not it should be stored in a cool and ventilated place to avoid heating.

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Fig. 1.2.3.2.4. Wax of Ericerus pela (Chavannes). A - Photograph of "wax flowers" enveloping the aggregated bodies of the second-instar males on a branch of privet tree; scale line: 10 mm. B - Illustration of wax aggregated on a branch (= "wax flower'). Arrows point to the protruding wax filaments secreted from the glandular pouches of the adult male; scale line: 10 mm.

CHEMICAL AND PHYSICAL PROPERTIES OF THE W A X

Chemical characteristics The chemical composition of the wax (unrefined or raw wax) has been investigated by several authors (e.g. Hashimoto and Mukai, 1967; Tamaki, 1970; Hashimoto and Kitaoka, 1971; Takahashi and Nomura; 1982). Using gas chromatography (GC) and gas chromatography-mass spectroscopy (GC-MS), Takahashi and Nomura (1982) confirmed the results by Hashimoto and Mukai (1967) that the main components of the wax produced by E. pela are wax esters (92.5 %) together with some other classes of lipids (hydrocarbons 0.8%, free alcohols 0.4%, free fatty acids 0.2% and unidentified compounds 4.1%). The identified components of the wax esters are C2s, C30 and C32 alcohols and the corresponding fatty acids, with an additional C~ acid. In addition, Wu (1989) mentioned that C27 alcohol and C27 fatty acid were also present. The most abundant of the wax esters is cerotyl cerotate, hexacosyl hexacosanoate (C25H51COOC26I-/53) (55.2 %), followed by hexacosyl tetracosanoate (22.4 %) and hexacosyl octacosanoate (16.7%), and these three components constitute 94.2% of the total crystalline wax secreted by E. pela. Takahashi and Nomura (1982) also analysed the constituents of the hydrocarbons and the free fatty acids using GC and/or GC-MS. They found that the hydrocarbon fraction of the crystalline wax was composed of n-hentriacontane (31.4%), n-nonacosane (28.7 %), n-tritriacontane (17.7 %), 3-methylnonacosane (9.5 %), n-heptacosane (5.0%), 3-methylheptacosane (3.7 %), methylpentatriacontane (3.0 %), n-pentatriacontane (2.7 %), n-pentacosane (1.3 %)and unidentified constituents (2.0 %)[percentage total greater than

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100% but correctly cited from Takahashi and Nomura (1982, table 3)]. The free fatty acids after methylation are methyl oleate (40.4%), methyl stearate (34.3%), methyl palmitate (6.8 %), methyl myristate (4.1%), methyl archidate (1.4 %) and unidentified material (13.0 %). The analyses of both Hashimoto and Mukai (1967) and Takahashi and Nomura (1982) were based on wax collected from Ligustrum japonica Thumb. in Japan. In China, however, the wax is harvested mainly from L. lucidum brit. and Fraxinus chinensis Roxb. and its composition has not been studied in detail. Nevertheless, one would not expect the wax produced in China and Japan to be different since Brown (1975) stated that none of the chemical constituents of coccid waxes are directly derived from the host plants. Hashimoto and Mukai (1967) noticed that triglycerides and phospholipids are major components of the lipids in the body of the male pela wax scale but they were not detected in the wax secreted by the insects. Physical and chemical characteristics of refined wax Wu (1989) summarisexl the characters of refined China wax. It is white or slightly yellow with a soft and shiny surface and no odour. It is hard with a slight brittleness, and a broken section shows needle- or pellet-like crystals. China wax is not soluble in water, and only slightly soluble in alcohol and ether. It is soluble in organic solvents such as formalin, benzene, toluene, xylene, trichlorethylene, chloroform and petroleum ether. After analysing 60 samples of China wax from different wax-production regions in 1980, the China Wax Standard Working Group of the Ministry of Commerce of the People's Republic of China concluded that the physical and chemical constants for China wax (probably commercial products) were as follows: melting point = 82.9~ acid value = 0.7, saponification value = 79.5, iodine value = 4.1, water or vapour material = 0.09 % and non benzene soluble material at 15~ = 0.08 %. These constants are different from those listed by Hashimoto and Mukai (1967) who analysed the raw wax (=wax-shell) and found: melting point = 85.0-85.6 ~ acid value = 0.8, saponification value = 107.4 and iodine value = 0.3.

COMMERCIAL PRODUCTS OF CHINA WAX There are two classes of commercial products from China wax, i.e. semifinished wax and refined wax. The processing of these classes of wax is explained below.

Semifinished wax The wax may be processed by either boiling or steaming. Boiling is the traditional method and is still widely used. Steaming can produce better quality wax but requires a steamer which is usually too small, and hence is not widely employed in wax processing. 1. Boiling method First grade wax and "crusted wax"" wax flowers are boiled in water at a wax:water until all the wax has melted. The wax forms the top layer and into a mould, where it is left to solidify (Fig. 1.2.3.2.5). This is the first Finally, cold water is added to the boiler so that any remaining wax becomes wax is called "crusted wax".

Section 1.2.3.2 references, p. 319

ratio of 2" 1 is removed grade wax. solid. This

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Soft scales as beneficial insects

Second grade wax: after the first grade wax and crusted wax are taken, the remaining bodies of male pupae are transferred to a large bamboo or wicker basket and washed with clean water until all yellow colour is removed. The washed remains are poured into a vat to soak, with a change of water 2-3 times a day for 2 days. The water is then drained and the remaining insect bodies are wrapped in a bag and boiled to obtain more wax. The wax is transferred to a container, boiled once more in the boiler, poured into a mould and cooled to solidify. This is the second grade wax.

2. Steaming method The difference between the steaming and boiling methods is in making the first grade wax. The processing of other grades of wax is the same. The wax flowers are steamed to allow the wax to melt and flow into the water but the insect bodies remain in the steamer. The melted wax is the first grade wax and the remains are used to make second or other grades of wax. Some buyers accept the above semi fmi shed wax but others only accept the refined wax (see below).

Refined wax The semifinished wax can be ref'med as "rice core wax" (Mi Xing La in Chinese) or "horse tooth wax" (Ma Ya La in Chinese). Rice core wax is produced by mixing different proportions of the first (50-70 %) and second (30-50%) grade wax. There are different methods of mixing these two grades of wax" either by using water and boiling or by melting the wax without water. These processes allow further refinement of the wax. Horse tooth wax is produced from all wax not suitable for making rice core wax. The method is the same as for making rice core wax and the intention is to further refine the wax.

The steaming method can also be used to make rice core wax and horse tooth wax. The wax produced using this method is better than that from the traditional boiling method.

Fig. 1.2.3.2.5. Stacks of wax cakes after processing, each weighing about 5 kilograms (from Li, 1985).

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Uses of China wax China wax has been used as a candle-making material in China for centuries. It must have played a important role in people's lives before substitute waxes were discovered and before electricity was invented. However, it is still used now for many other purposes (Li, 1985; Wu, 1989). Industry: (1) because of its light, shiny, non-deformable characteristics and high accuracy in producing shapes, China wax is an ideal material for casting moulds, particularly in the manufacture of aeroplane instruments and in mechanical and precision instrument production; (2) it can be used for the insulation of cables, electrical equipment and insulated wires, and as an anti-corrosive coating on ammunition; (3) in the paper industry, China wax can be used as an ingredient of emulsified sizing preparations, for sizing high-gross paper, filling and shining agents in paper productions such as tracing paper, waxing paper, paper for coating sweets and for decorating fancy foods, etc.; (4) it is used as an ingredient in polishes for automobiles and tyres in the car industry, as a dressing ingredient, and in f'mishing preparations and various polishes such as shoe creams, pastes and polishes in the leather industry; as an ingredient in sizing, finishing, and waxing clothes and sewing thread in the textile industry; in the preparation of various inks and as modelling wax in teaching aids; (5) it is also used to polish furniture. Pharmacy and medicine: China wax has long been used in traditional medicine in China. Li (1578, see Wu, 1989, p. 4), who was a well known physician of the Ming Dynasty, summarises: "Pela (China wax) is lukewarm and non-poisonous, it can restore vital energy and stop bleeding, relieve pain and reinforce weakness, restore muscles and set broken bones; taking it as pills can kill worms; polishing the head can cure baldness". Some of the above statements made by Li (1578) may have no scientific basis but it shows that China wax has been used as traditional medicine for hundreds of years. It can be used by itself or as an ingredient with many other traditional medicines. Nowadays, the medicinal uses of China wax have been expanded to heal uterus epilepsy, pelvic infection, uterus atrophy, and for wound swelling, breach of skin, chronic gastritis and rheumatism (Wu, 1989). China wax is widely used in pharmaceutical production, e.g. in coating pills and for sealing medicine bottles to prevent the drugs from denaturing during storage. Agriculture and horticulture: China wax is used as a grafting agent in grafting fruit trees, to prevent desiccation and to stop rain water getting into graft cuttings and hence increase the success of grafting. The remaining material (pupae of the insects) after processing the wax is ideal food for pigs and other husbandry animals. In addition, China wax can be used to make imitation fruits and flowers. For most of the above uses, a number of other waxes can replace China wax. However, China wax has advantages over other waxes because its melting point (83-86 ~ is higher than that of many other waxes, such as the widely used paraffin wax (50-60~ Kuwana (1923, p. 405) predicted that "this interesting insect-wax [China wax] industry may at some future date become extinct'. However, although production has declined since the 1940's, China wax industry shows no signs of extinction and the wax is still being produced and widely used in China. Indeed, the production of China wax cannot now meet the increasing demand in areas such as in the paper and drug manufacturing industries. Moreover, production and use of China wax does not cause any contamination to the environment and increased demand for environmentally safe products will stimulate greater production of China wax.

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Soft scales as beneficial insects

Yield of China wax There are apparently no statistics on the overall yield of China wax from China. All estimates of wax production probably apply only to Sichuan province--the main waxproducing region. Sasaki (1904) stated that the wax harvested in a year was 600,000 Chin (300 tons). Wilson (1913, see Kuwana, 1923) mentioned that 50,000 piculs (3,000 tons) of wax was an average production in a poor year but in a favourable year, the yield was more than double this figure. Chiao and Pen (1940) recorded that about 2,800 tons of China wax were produced annually in Sichuan. However, Wu (1989) stated that, since 1949, the highest annual production of China wax has been 590 tons and production has never fulfilled the great demand.

WAX PRODUCTION OF SPECIES OF CEROPLASTES The females of all species of the wax scales (subfamily Ceroplastinae) produce a thick layer of wax which covers the body. The wax composition of at least 9 species of Ceroplastes has been analysed (e.g. Gilby and Alexander, 1957; Broch6re and Polonsky, 1960; Faurot-Bouchet and Michel, 1965; Tamaki and Kawai, 1968; Tamaki et al., 1969; Hashimoto and Kitaoka, 1971; Rios et al., 1974; Naya et al., 1981; Pawlak et al., 1983). The chemical composition of the wax of the cover is discussed in Section 1.1.2.5. Blanchard (1883) recorded that the wax secreted by at least 8 species of Ceroplastes could be useful. In particular, the wax of C. ceriferus (Fabricius) has been used as medicine (Essig, 1942) and in candle production (Cotes, 1891) in India. J. Anderson (see Blanchard, 1883; Cotes, 1891) observed people in Madras eat the wax of C. ceriferus. Blanchard (1883) suggested that an industry might be established to process the wax of C. rusci (L.). Some species of Ceroplastes have been used for millenia for the production of wax in Central and South America (Brown, 1975). The Indians of the southwestern United States of America have used a similar wax product produced from the irregular wax scale, C. irregularis Cockerell, to water-proof or seal baskets and pottery (Essig, 1931).

CONCLUSION Although many soft scales produce wax, few provide wax useful to people. While some species of Ceroplastes are considered to be pests, the wax produced by females of other species has been utilised for centuries in India and Central and South America. However, to-date the most useful wax producer among the soft scales is E. pela. This species has been reared commercially in China for more than a thousand years. The wax produced by the second-instar males of this insect is composed mainly of wax esters together with small amounts of hydrocarbons, free alcohols and free fatty acids. The commercial product that is processed and refmed from this wax is widely known as China wax. Apart from use in traditional candle-making, China wax has many industrial applications. The China wax industry has declined since other waxes (especially paraffm wax) were discovered, but the melting point of China wax is higher than that of many other waxes and hence it is safer to use. Nowadays the production of China wax cannot meet the increasing demands. Moreover, the use and production of China wax is environmentally friendly.

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ACKNOWLEDGEMENTS I thank Dr Jing Dao-Chiao of Guizhou Agricultural College, China, Professor Shozo Takahashi of Kyoto University, Japan, Dr Toshiya Hirowatari of University of Osaka Prefecture, Japan, and Dr Yair Ben-Dov of the Agricultural Research Organization, Israel, for providing me with literature; Mr Sueo Nakahara and Dr Douglass R. Miller of the United States Department of Agriculture, USA, for arranging the loan of material of E. pela, Professor Li Zi-Zhong, Mr Luo Lu-Yi, Mr Liu Zuo-Yi and Dr Jing DaoChiao of Guizhou, China, for collecting and sending me specimens of E. pela; Professor Tang Fang-De (=Tang Fang-teh) for checking page numbers of some references; Professor Li Chen-Kang for his permit to reproduce Figure 11 from Li (1985) in Fig. 1.2.3.2.5 of this Section; Dr Chris Reid for help in translation of French text; Dr Pete Cranston for ideas on the structure of this paper; Dr Jonathan Banks for reading the section on chemical composition and chemical characteristics of the wax; Dr Bruce Halliday for reading and commenting on the manuscript; the Electron Microscopy Unit at the Australian National University (ANU) for facilities and assistance with the SEM micrography; and Mr Keith Herbert of the Division of Botany and Zoology, ANU, for reproducing the photographs. My special thanks go to Dr Penny Gullan who helped me in many ways and especially for critically reviewing the text and correcting the English. The manuscript was improved by comments from the reviewers.

REFERENCES (References marked with an asterisk not seen by the author). Anonymous., 1976. Studies on Anthribus niveovariegatus Roelofs. Acta Entomologica Sinica, 19(4): 401-409 (In Chinese with English summary). Beattie, G.A.C., Weir, R.G., Cliff, A.D. and Jiang, L., 1990. Effects of nutrients on the growth and phenology of Gascardia destructor (Newstead) and Ceroplastes sinensis Del Guercio (Hemiptera: Coccidae) infesting citrus. Journal of the Australian Entomological Society, 29: 199-203. Blanchard, R., 1883. Les Coccidds Utiles. Librairie J.-B. Bailliere et Fils, Paris, 117 pp. Brochdre, G. and Polonsky, J., 1960. Sur la structure d'un nouvel acide alicyclique: l'acide gascarlique isold de la gomme laque de la cochenille Gascardia madagascariensis. Bulletin de la Socidt~ Chimique de France, 54: 963-967. Brown, K.S., 1975. The chemistry of aphids and scale insects. Chemical Society Review, 4(2): 263-288. Chavannes, A., 1847. Mdmoire sur deux Coccus c~riferes du Bresil. Bulletin de la Socidtd vaudoise Sciences Naturelles, 2:209-216. Cheng, F.K., 1974. Studies on the wax scale Ericerus pe-la Chavannes, with investigation into the rearing experiences by the masses. Acta Entomologica Sinica, 17(4): 376-382+2 plates (In Chinese with English summary). Chiao, C.Y. and Pen, D.S., 1940. China wax or insect wax industry ofSzechuan [=Sichuan]. China Journal, 32(3): 107-113. (Abstract in Review of Applied Entomology, Series A, 29: 153). * Chiao, C.Y. and Peng, D.S., 1943. China wax or insect wax industry in Szechwan [=Sichuan]. II. Further studies on wax insects. Journal of the West China Border Research Society (B), 14: 128-132. (Abstract in Review of Applied Entomology, Series A, 32: 41). * Chou, I., 1990. A History of Chinese Entomology. Tianze Press, Xi'an, Shaanxi, China, 245 pp. Cotes, E.C., 1891. White insect wax in India. Indian Museum Notes, 32 (1891): 91-97. Danzig, E.M. 1965. The wax scale -- Ericerus pela Chav. (Homoptera, Coccoidea) in the USSR. Zoologicheskii Zhurnal, 44(4): 537-546 (in Russian with English summary). Essig, E.O., 1931. A History of Entomology. MacMillan, New York, 1029 pp. Essig, E.O., 1942. College Entomology. MacMillan, New York, 900 pp. Faurot-Bouchet, E. and Mickel, G., 1965. Composition des cires d'insectes. II. Cires des cochenilles Ceroplastes rusci, Icerya purchasi, Pulvinaria floccifera et Quadraspidiotus perniciosus. Bulletin de la Socidtd de Chimie Biologique, 47" 93-97. * Foldi, I., 1991. The wax glands in scale insects: comparative ultrastructure, secretion, function and evolution (i-lomoptera: Coccoidea). Annales de la Socidtd Entomologique de France (N.S.), 27(2): 163-188. Gilby, A.R. and Alexander, A.E., 1957. Studies of cuticular lipides of arthropods. I. The influence of biological factors on the composition of the wax from Ceroplastes destructor. Archives of Biochemistry and Biophysics, 67(2): 302-306. Giliomee, J.H., 1967. Morphology and taxonomy of adult males of the family Coccidae (Homoptera: Coccoidea). Bulletin of the British Museum (Natural History), Entomology, Supplement 7: 1-168.

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Soft scales as beneficial insects Gimpel, W.F., Miller, D.R. and Davidson, J.A., 1974. A systematic revision of the wax scales, genus Ceroplastes, in the United States (Homoptera; Coccoidea; Coccidae). Agricultural Experiment Station, University of Maryland, College Park, Maryland, Miscellaneous Publication 841: 1-85. Hashimoto, A. and Kitaoka, S. 1971. Scanning electron microscopic observation of the waxy substances secreted by some scale insects. Japanese Journal of Applied Entomology and Zoology, 15:76-86 (In Japanese with English summary). Hashimoto, A. and Mukai, K., 1967. Studies on the lipids of coccids Part X. Lipid composition of male larvae of Ericerus pela Chavannes as determined by Column Chromatography. Journal of the Agricultural Chemical Society of Japan, 41(10): 506-511 (in Japanese with English summary). Jiang, D.Q., Xia, M.Z. and Li, W.R., 1984. Studies on Microterys ericeri Ishii. Acta Entomologica Sinica, 27(1): 48-56 (In Chinese with English summary). Ke, Z.G., 1981. The distribution of Ericerus pela Chavannes and analysis of ecological factors. Insect Knowledge, 18(6): 257-259 (In Chinese). Kuwana, I., 1923. The Chinese white-wax scale, Ericeruspela Chavannes. The Philippine Journal of Science, 22(4): 393-405. Li, C.K., 1985. China wax and the China wax scale insect. World Animal Review, 55: 26-33. Li, S.Z., 1578. Chinese medicinal herbs [Chou (1990) translated the title as "The Great Pharmacopoeia'] (In Chinese, translated into English and researched by P. Smith and G.A. Stuart, 1973. San Francisco, Georgetown Press). * Naya, Y., Yoshihara, K., lwashita, T., Komura, H., Nakanishi, K. and Hata, Y., 1981. Unusual sesterterpenoids from the secretion of Ceroplastesfloridensis (Coccidae), an orchard pest. Application of the allylic benzozate method for determination of absolute configuration. Journal of the American Chemical Society, 103(23): 7009-7011. * Noirot, C. and Quennedey, A., 1974. Fine structure of insect epidermal glands. Annual Review of Entomology, 19: 61-80. Paik, W.H., 1978. Insecta VI. Coccoidea. Illustrated Flora and Fauna of Korea, 22 : 1-481 (in Korean). Pawlak, J.K., Tempesta, M.S., lwashita, T., Nakanishi, K. and Naya, Y., 1983. Structures of sesterterpenoids from the scale insect Ceroplastes ceriferus. Revision of the 14-membered ceriferene skeleton form 2-T/6C/10-T to 2-C/6-T/10-T. Chemistry Letters, No. 7: 1069-1072. Peng, X.L. and Zhong, Y.H., 1990. Morphological and histological studies on the neurosecretory system of Ericerus pela Chavannes. Journal of Sichuan University Natural Science Edition, 27(4): 486-491 (In Chinese with English summary). Rios, T. and Quijano, L. and Calder6n, J., 1974. Albolineol, a sesterterpene with a novel bicyclic skeleton. Journal of the Chemical Society, D. Chemical Communications, 10: 728-729. Sasaki, C., 1904. On the wax-producing coccid, Ericerus pe-la, Westwood [sic.]. Bulletin of Agricultural College [=College of Agriculture], Imperial University, Tokyo No. 16: 1-14. Shaanxi Province Biological Resource Survey Team, 1974. Pela wax scale and wax production. Shaanxi Press, Shaanxi, 69 pp (In Chinese). * Takahashi, S. and Nomura, Y., 1982. Wax composition of the soft scale Ericerus pela (Hemiptera: Coccidae). Entomologia Generalis, 7(4): 313-316. Tamald, Y., 1970. Studies on waxy coverings of Ceroplastes scale insects. Bulletin of the National Institute of Agricultural Science, Tokyo, 24:1-111. Tamaki, Y. and Kawai, S., 1968. Fatty acids, alcohols and hydrocarbons in the waxy covering of Ceroplastes pseudoceriferus Green, Ceroplastes japonicus Green, and Ceroplastes rubens Maskell (Homoptera: Coccidae). Japanese Journal of Applied Entomology and Zoology, 12:23-28 (in Japanese with English summary). Tamald, Y., Yushima, T. and Kawai, S., 1969. Wax secretion in a scale insect, Ceroplastes pseudoceriferus Green (Homoptera: Coccidae). Applied Entomology and Zoology, 4(3): 126-134. Tan, S.J. and Zhong, Y.H., 1989. Study on the wax glands in the male white-wax scale, Ericerus pela Chavannes. Journal of Sichuan University Natural Science Edition, 26(4): 489-493 (In Chinese with English summary). Tang, F.D. (Tang, Fang-teh), 1991. The Coccidae of China. Shanxi United Universities Press, Shanxi, 377 pp. (In Chinese with English summary). Waku, Y. and Foldi, I., 1984. The fine structure of insect glands secreting wax substances. In R.C. King and H. Akai (Editor) Insect Ultrastructure, Plenum Publishing Corporation, 2: 303-322. Wang, F., 1963. On the adaptability of the Chinese white wax scale Ericerus pela Chavannes to the ecological condition and its utilisation in production. Scientia Silvae Sinicae 8(2): 171-175 (In Chinese). Wang, F., 1978. The Breeding and Utilisation of E. pela. Sichuan Press, Chengdu, 123 pp. (In Chinese). Wang, J., 1566. A Collection of the Pharmaceutical Naturalists (In Chinese). * Wilson, E.H., 1913. A naturalist in western China, 2: 100-105. * Wu, C.B., 1980a. On the ecological adaptability of the Chinese white wax scale, Ericerus pela Chavannes. Journal of Sichuan University Natural Science Edition, 1980(3): 175-181 (In Chinese with English summary). Wu, C.B., 1980b. A discussion about some points in the paper "on the adaptability of the Chinese white wax scale Ericerus pela Chavannes to the ecological condition and its utilization in production". Scientia Silvae Sinicae 1980(4): 296-301 (In Chinese with English summary).

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Wu, C.B., 1980c. A preliminary study on ladybird beetle Chilocorus rubidus Hope. Journal of Sichuan University Natural Science Edition, 1980(4): 163-168 (In Chinese with English summary). Wu, C.B., 1981. Preliminary study on some measures to increase white wax production. Journal of Sichuan University Natural Science Edition, 21(3): 93-99 On Chinese with English summary). Wu, C.B., 1987. Preliminary study on using the hybrid vigor of white wax scale. Journal of Sichuan University Natural Science Edition, 24(2): 217-220 On Chinese with English summary). Wu, C.B., 1989. Pela Wax Scale and its Wax Production. China Forestry Press, Beijing, 155 pp. (In Chinese). Wu, C.B. and Gao, B., 1990. Studies on the structure and development of male reproductive system in the white wax scale, Ericerus pela. Journal of Sichuan University Natural Science Edition, 27(4): 495-497 on Chinese with English summary). Wu, C.B., Li, C.X. and Sun G.R., 1988. Comparative studies on some economic characters of the white wax scale "seed" produced in several different regions in provinces of Sichuan, Yurman and Guizhou. Journal of Sichuan University Natural Science Edition, 25(2): 230-235 on Chinese with English summary). Wu, C.B. and Zhong, Y.H., 1983. Study on the bionomics of white-wax scale Ericerus pela Chavarmes Part I. Journal of Sichuan University Natural Science Edition, 1983(3): 91-99 (In Chinese). Wu, C.B., Zu, W. and Ran, J.H., 1991. Inquisition on the arrangement of productive areas to produce white wax scale seed and white wax. Journal of Sichuan University Natural Science Edition, 28(3): 345-352 on Chinese with English summary). Xu, G.Q., 1639. Complete Treatise on Agriculture (In Chinese). Xu, S.G., 1959. White wax [=China wax]. China Forestry Press, Beijing, 69 pp. On Chinese). * Zhang, C.H., 1984. Successful introduction of pela insect, Ericerus pela Chavarmes, to a south subtropical area, Jingdong, Yunnan Province. Zoological Research, 5(3): 275-282 (In Chinese with English summary). Zhang, C.H., Yang, Y.G., Miao, Y.J. and Wu, G.Q., 1986. Occurrence of Ericerus pela Chavannes populations in Yonde county of Yunnan province south to 24" noah latitude. Acta Entomologica Sinica, 29(1): 108-109 on Chinese with English title). Zhang, Z.Y. and Shao, M.M., 1982. Observations on Ericerus pela Chavannes in Shaanxi. Insect Knowledge, 19(3): 34-36 fin Chinese). Zhang, Z.Y., Shao, M.M. and Qi, S.L., 1990. Study on fine varieties and sex ratio of the population of the white wax insect (Ericerus pela Chavannes). Scientia Silvae Sinicae 26(1): 46-52 on Chinese with English summary). Zhao, X.P. and Wu, C.B., 1990. The embryonic development of Ericerus pela (Chavarmes). Journal of Sichuan University Natural Science Edition, 27(2): 222-231 (In Chinese with English summary). Zou, S.W., 1981. The History of Chinese Entomology. Science Press, Beijing, 242 pp. On Chinese). *

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Sq[t Scale Insects - Their Biology, Natural Enemies and Control

Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.

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Chapter 1.3 Ecology 1.3.1

Effects on Host Plant

JOHN A. VRANJIC

INTRODUCTION Soft scales (Coccidae) feed on many vascular plants and are pests of major economic significance on various agricultural and ornamental crops (Hely et al., 1982; Johnson and Lyon, 1991). The damage by scale infestations to host plants includes both direct and indirect components. The direct components occur as a result of feeding activity and involve two processes: the penetration and damage of plant tissues by the insects' mouthparts, and the removal of resources needed for plant growth. Indirect damage to plants also occurs through two processes: the contamination of plant surfaces with honeydew and sooty moulds, and the transmission of arthropod-borne pathogens. Although these processes can be viewed separately, most studies do not determine their individual effects on plant growth. Despite the prominence of soft scales as pests, there are few studies quantifying their impact on plant growth. I will, therefore, broaden the scope of this review to include other families of Coccoidea, but will generally exclude the mealybugs (Pseudococcidae) and the armoured scales (Diaspididae), since these two families are important pests in their own fight and the impact of diaspidids on host plants has been reviewed in a previous volume (McClure, 1990). Family names are indicated in brackets on the first mention of genetic names to identify species not in the family Coccidae. Firstly, I shall review how scale insects inflict damage on their host plants and then I shall summarize the extent to which specific physiological and growth processes are disrupted; finally, some factors which modify plant responses to scale infestations are considered.

HOW SCALE INSECTS AFFECT PLANT GROWTH: DIRECT EFFECTS 1. Feeding damage The Coccidae and related families directly affect plant growth by their feeding, which involves the penetration of their mouthparts into the phloem and the uptake of sap as food (Raven, 1983). This feeding can disrupt plant tissues in the vicinity of the stylets through the toxic effects of saliva. In leaves, feeding can result in localized lesions involving both vascular tissues and the associated photosynthetic tissue, as shown by the degeneration of chloroplasts and subsequent discolouration around the feeding sites (Carter, 1973), thus reducing the functional photosynthetic area. Feexling by Eriococcus coriaceus Maskell (Eriococcidae) on Eucalyptus leaves causes a purple discolouration in the immediate vicinity of the insects, possibly from breakdown of chlorophyll (J. Vranjic, unpublished data). As well as discolouration, feeding by some scale insects can

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cause localizexl distortions of tissue. Cells surrounding the stylet punctures made by

Matsucoccusfeytaudi Ducasse (Margarodidae) on stems of Pinus pinaster Ait. increased both in size and number, producing a swelling around each puncture site (Carle et al., 1970). Although feeding by individual insects produces very localized effects, the extent of damage during heavy infestations can be considerable. The build-up of damaged tissues can cause the malfunctioning of the phloem and cambium, leading to stem dieback. In stems of ash (Fraxinus sp.), Kormirek (1946) observed that the stylets of Eulecanium tiliae (L.) (Coccidae) penetrated to the cambium and that cells adjoining the stylet track died. Proteinases and cellulases in the insect saliva broke down the dead cells, allowing the salivary secretions to penetrate into neighbouring cellular layers, eventually causing the necrosis of tissues within one to two millimetres around the stylet. During severe infestations, the phloem became completely interrupted by necrotic tissue, resulting in stem dieback. Feeding by high densities of Cryptococcus fagisuga Lindinger (Cryptococcidae) on beech (Fagus sp.) stems caused a wound response in the bark parenchyma: initially the feeding zone tissues became necrotic, then a secondary periderm developed to isolate the damage (Wainhouse et al., 1988). The subsequent distortions in stem growth led to fissuring of the bark, providing further points of attack by the beech scale, and aggravating the infestation. Heavy infestations of Matsucoccus species on pine (Pinus sp.) are characterized by branch deformation and an abnormally copious secretion of resin around the feeding sites (McKenzie, 1941; Carle et al., 1970), possibly as a defensive reaction against the scale. Despite any adverse effect of resinosis on scale insects, sugar pines (Pinus lambertiana Douglas) show progressive branch, and even tree, death following extensive attacks by Matsucoccus paucicicatrices Morrison (MeKenzie, 1941). 2. Resource removal The removal of sap represents a dram on resources intended for new growth, for translocation for use elsewhere within the plant and/or for storage. The extent to which plant function is disrupted depends upon several factors, notably the availability of resources to the plant and the density of the scale insect infestation (see Factors affecting Plant Responses, below). There are few data on the effects of scale insects on plant carbon and nitrogen economies, but those that are available suggest that the amount of photosynthate lost can be considerable. For instance, it has been estimated that forests of Nothofagus solandri (Hook. f.) Oerst. in New Zealand can lose up to 23 % of their photosynthate to the sooty beech scale, Ultracoelostoma assimile MaskeU (Margarodidae) under densities of 18.6 million insects per hectare (Belton, 1978, cited in Kelly, 1990). Populations of over 2000 ToumeyeUa liriodendri Gmelin (Coccidae) on tulip trees (Liriodendron tulipifera L.) with a leaf area of 60.2 m2 removed more carbon than was assimilated (Bums and Donley, 1970). Large infestations of T. liriodendri not only prevented growth but also depleted existing carbohydrate reserves (Bums and Donley, 1970), ultimately affecting the plant's capability to recover from the infestation. In addition to the loss of photosynthate, the loss of other essential nutrients may be of equal or greater significance. Measurements of nitrogen content and nitrogen export from senescing leaves of Euphorbia pyrifolia Lam. infested with lcerya seycheUarum (Westwood) (Margarodidae) suggest that this scale insect removed at least 25 % of the nitrogen exported (Newbery, 1980b). Losses of this magnitude are a significant drain on resources, limiting plant growth, reducing their competitiveness and affecting their response to subsequent environmental stress. In comparison, populations of the aphid, lllinoia liriodendri (Monell), removed only about 1% of the photosynthate and 17 % of the nitrogen annually from the foliage of a mature stand ofL. tulipifera (van Hook et al., 1980). Of the resources consumed by the aphid, about 65 % of the energy and 27 % of the nitrogen were lost in honeydew production. Further studies on the extent of

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resources lost to scale infestations are required to determine whether the quoted figures are truly representative or extreme. 3. Galls Gall formation by Coccoidea is mostly associated with certain taxa of Eriococcidae and Asterolecaniidae and, among the Coccidae, is confined to Cissococcus fulleri Cockerell which forms large galls on Cissus in South Africa (Beardsley, 1984). Gall formation is considered further in Section 1.3.2.

HOW SCALE INSECTS AFFECT PLANT GROVVFH: INDIRECT EFFECTS 1. Contamination with honeydew and sooty moulds In addition to the direct deleterious effects of feeding, plant growth is also effected indirectly by the excretion of honeydew. Phloem sap provides an unbalanced diet for scale insects, being typically limiting in nitrogenous compounds but with excess photosynthate, which is excreted as honeydew. The mixture of carbohydrates and trace amounts of nutrients in honeydew (Bums and Davidson, 1966; Basden, 1968) provides a favourable substrate for the growth of sooty moulds. The encrustations of sooty moulds on leaves and stems is responsible for the unsightly, blackened appearance of many homopterous-infested plants (Hughes, 1976; Meyer, 1978). Sooty moulds usually comprise a complex association of several fungal species, all saprophytic and therefore of no direct harm to the host plants (Fraser, 1933). They can take a variety of forms from thin hyphal networks to robust mycelial crusts (Hughes, 1976). The mycelia adhere closely to leaf and stem surfaces due to a mucilaginous base but do not penetrate into the host tissues, although hyphae occasionally enter and block stomata (Vranjic, 1993). Since mycelia adhere strongly to leaves, the mould is not washed off readily during rain (Tedders and Smith, 1976). Sooty moulds require a continuous supply of honeydew to thrive, and removal of the honeydew source usually causes their disappearance, as the crust eventually dries out and detaches from the leaf surface in flakes with the aid of rain and wind (McMaugh, 1985; J. Vranjic unpublished data). The rate of mould detachment and its interaction with weather have not been studied in detail. Development of sooty moulds is considered further in Section 1.2.2.2. Leaf contamination appears to disrupt light transmission rather than the photo-synthetic machinery (Brink and Hewitt, 1992). The impact of sooty moulds on whole plant growth depends upon the extent of leaf contamination, which itself is determined by the level of scale infestation (Newbery, 1980a; Brink and Hewitt, 1992), plant growth patterns (Vranjic and Gullan, 1990) and such external factors as weather and ant attendance (Arney, 1993). Contamination of leaves with honeydew and sooty moulds has been considered to have a far greater impact on host-plant growth than the actual feeding activity of scale insects (Hely et al., 1982). The economic impact is increased when sooty moulds occur on the fruit, rendering them unsalable unless cleaned (Hely et al., 1982). Currently, no studies are known in which the amount of sooty mould associated with scale insect infestation has been manipulated to quantify their impact on plant growth. However, field experiments involving the cereal aphid, Sitobion avenae F., on winter wheat (Triticum aestivum L.) have manipulated saprophytic yeast populations on the leaves. These experiments calculated that most of the yield loss was attributable to aphid feeding damage and only about 28 % of yield loss attributable to the negative effects of yeasts on photosynthesis and leaf aging (Rabbinge et al., 1981). In further studies, the saprophytic yeast flora was found to have no apparent effect in most years and even had a slightly beneficial effect in one year (Rabbinge et al., 1984). This beneficial effect

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occurred because the saprophytic yeast competitively interfered with necrotrophic fungal pathogens on the wheat leaves. The effects of scale insects and sooty moulds on photosynthesis are discussed further below under Impact on Physiological Processes. Evidence regarding the importance of sooty moulds also comes from ant manipulation experiments. Exclusion of ants from infestations of Coccus viridis (Green) (Coccidae) on Pluchea indica (L.) allowed honeydew and sooty mould to accumulate on the leaves; there was no such accretion on ant-attended plants (Bach, 1991). Ant-excluded plants consequently showed significantly higher abscission rates and leaf death than ant-attended plants with equivalent infestations of scale insects. Thus, the sooty moulds associated with C. viridis also increased leaf senescence and decreased leaf duration, as observed for aphids and yeast on wheat leaves, although the direct effect on photosynthesis was not measured. Arney (1993), however, observed that exclusion of ants from populations of Eriococcus confusus Maskell on Eucalyptus did not enhance sooty moulds, since antexcluded populations of scale insects were quickly controlled by predators. Nor did the differences in extent of contamination and scale insect survival translate into any significant effect on tree diameter or height. The impact of ants on plant responses to scale infestations are discussed further under Factors affecting Plant Responses below. More detailed studies are required to elucidate the relative contributions of leaf contaminants and insect feeding activity on plant growth responses to scale insect infestations.

2. Associations with plant pathogens With the exception of some species of mealybug, the Coccoidea are not important vectors of viruses (Carter, 1973), although Nixon (1951) mentioned the possible association of Saissetia species (Coccidae) with the sudden death disease of cloves (Syzygium aromaticum (L.) Merr. and Perry). However, there is one known instance of non-pseudococcid coccoids being associated with an important secondary pathogen. Beech bark disease arises because injury by the beech scale, Cryptococcus fagisuga, provides points of infection for the pathogenic fungus, Nectria coccinea Pets. ex Fr.) Fries., through the extensive fissuring of the bark (Houston et al., 1979). Once established, the fungus rapidly invades the bark, cambium and vascular system causing progressive dieback of branches. The infection is usually associated with heavy beech scale infestations (Carter, 1973). The disease has caused extensive dieback of beech in Europe and also resulted in the death of 85 % of beech trees in North America since 1890 when C. fagisuga was accidentally introduced (Houston et al., 1979).

IMPACT ON PLANT PHYSIOLOGICAL PROCESSES Given the varied ways in which scale infestations can affect plants, it is not surprising that several important physiological processes are disrupted. The damage caused by scale insects is not limited to specific tissues near the feeding sites but affects the entire plant because the insects drain and suppress the resources available within the host. This section discusses the impact of scale insects on photosynthesis, water relations and nutrition; these factors, of course, are not independent but interactive. Other physiological processes may well be affected, such as hormonal balance, but these have not been investigated.

1. Photosynthesis and gas exchange Scale insect infestations and the associated sooty moulds can affect gas exchange and assimilation rates by blocking stomata, reducing light transmission and by depleting the resources necessary to maintain photosynthesis. Resource removal was discussed above. Accretion of honeydew and sooty moulds can obscure stomata, while hyphae may even penetrate the stomatal opening, thus limiting the assimilation of carbon dioxide into the

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leaf (Fokkema, 1981). However, stomata tend to be prevalent on lower leaf surfaces and so the capacity for the undersides of leaves to become contaminated depends upon the distribution of the scale insects and on leaf orientation. Many coccid species preferentially inhabit leaf undersides (e.g., Newbery, 1980b) or stems and expel their honeydew downwards, so that leaf contamination is greatest on the upper leaf surfaces. In these situations, the problem of stomatal blockage is lessened by the relative escape of leaf undersurfaces from extensive contamination. The extent to which light transmission is reduced by sooty moulds has received little attention. Transmission of light through the leaves of pecan (Carya illinoensis (Wang) K. Koch) contaminated with sooty moulds following aphid infestations, was reduced by up to 25 %, depending upon aphid density and on the amount of mould on the leaves (Tedders and Smith, 1976). A heavy covering of sooty mould reduced the transmission of photosynthetically active radiation by over 90 % for leaves of Citrus paradisi Macf. (Brink and Hewitt, 1992) and by 57 to 81% for leaves of Eucalyptus blakelyi Maiden (Vranjic, 1993). The overall effect of light interference on assimilation rates is dependent upon growth conditions and the acclimation of leaves to particular light regimes. Bright light can induce photoinhibition, so that some reduction in light may have little effect or may even be beneficial, particularly under circumstances of light stress or a combination of light and other stresses (Osmond, 1987). As well as quantity, the quality of light reaching the chloroplasts may be affected by sooty moulds. The infra-red reflectance of Citrus leaves was altered by sooty mould (Hart and Myers, 1968), a factor that affects leaf temperature as well as photosynthetic characteristics. Quantitative changes in gas exchange and assimilation rates of mould-affected leaves have not been investigated widely. That extensive sooty mould can detrimentally affect photosynthesis is apparent from the severe chlorosis of leaf surfaces underneath the sooty mould (Carter, 1973). Thus, a light covering of sooty mould on the leaves of Citrus paradisi on trees infested with Cribrolecanium andersoni (Newstead) (Coccidae) caused almost 50% suppression in net photosynthesis, while heavy mould resulted in a 95 % decrease (Brink and Hewitt, 1992). Removal of the mould layer resulted in a considerable recovery of the rate of photosynthesis within a week, even with the heavily affected leaves, suggesting that the adverse effects of sooty mould are temporary and are mainly limited to blocking the transmission of light. Other studies have documented the impact of scale insect feeding on photosynthesis, as distinct from the effects due solely to sooty moulds. The feeding activity of some diaspidids, for example, is associated with a significant degree of leaf chlorosis. Infestation with the pine needle scale, Chionaspis pinifoliae (Fitch) (Diaspididae), reduced the photosynthetic rate of Pinus sylvestris L. by 30 % to 40% and chlorophyll content by 23% (Walstad et al., 1973). The euonymus scale, Unaspis euonymi (Comstock) (Diaspididae), reduced the assimilation rate of Euonymusfortunei (Turcz) Hand-Mazz. by 63 % and chlorophyll content by 49 % (Cockfield et al., 1987). However, scale infestations also influence the functioning of those leaves not directly affected by either insects or mould. Uninfested, newly developed leaves from saplings of Guaiacum sanctum L. infested with a Toumeyella species had less than one third the mean net assimilation rate of similar leaves from uninfested trees (Schaffer and Mason, 1990). The components of assimilation rate (i.e. stomatal conductance and internal partial pressure of CO2) were also lower for infested plants, but there was no significant difference in chlorophyll content as a result of infestation. Presumably, the Toumeyella sp. affected the new leaves by diverting the resources needed for growth and stomatal functioning. In terms of whole plant responses, there is an effective loss of functional photosynthetic leaf area due to premature leaf death, decreased production of new leaves and leaf contamination plus localized chlorosis, rendering the existing leaf area

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ineffective. Overall plant responses strongly influence which leaves are affected. Thus impairment of newly expanded leaves at the peak of their efficiency can cause significant reductions in plant growth, unlike the older leaves which contribute least to growth. Basal regeneration, such as occurs with some eucalypts, may be seriously affected, since these new leaves contribute significantly to the recovery of plants and yet are likely to be affected by sooty moulds on honeydew excreted by insects on the upper shoots.

2. Water relations Given that scale insects impose a continual drain of liquid sap and, in some instances, cause a marked decline in root production (Vranjic and Gullan, 1990), the effects on plant water uptake and balance are likely to be important. However, there have been few studies on changes in water relations caused by scale insect infestations. The average leaf-water content of iceplant (Carpobrotus sp.), a succulent, was not affected by an infestation ofPulvinariella mesembryanthemi (Vallot) (Coccidae) (Washburn et al., 1985). On the other hand, an infestation by ToumeyeUa sp. reduced the transpiration rate of Guaiacum sanctum, although the efficiency of water use did not generally differ between infested and uninfested plants (Schaffer and Mason, 1990). Leaves of Euonymus fortunei infested with the diaspidid, Unaspis euonymi, transpired less than uninfested leaves and had a lower conductance, suggesting that euonymus scale infestation affected stomatal function (Cockfield and Potter, 1986). Infested leaves also had a higher solute potential and lower pressure potential, indicating that they were more prone to wilting than uninfested leaves. 3. Nutrient content Plant nutrient content, especially nitrogen, has been measured to account for changes in scale insect growth and population density (e.g., McClure, 1980). The converse, that scale insects themselves can affect the uptake and distribution of nutrients within plants, has received scant attention, despite the implications that changes in nutrient transport and allocation have for future plant growth or subsequent infestations. The total foliar nitrogen content of Guaiacum sanctum was not affected by infestation with Toumeyella sp. (Schaffer and Mason, 1990). Soluble and total foliar nitrogen concentration did not differ significantly between bushes of Scaevola taccada (Gaertn.) Roxb. that were sprayed with insecticide to remove Icerya seychellarum and bushes that retained infestations (Newbery, 1980c). However, there was a positive correlation between the change in soluble nitrogen levels of senescing leaves and the level of scale insect infestation, implying that scale infestation could affect mobilization of soluble nitrogen.

IMPACT ON PLANT GROWTH The effects of scale insect infestation upon plant growth are complex and typically include blackening of shoots by sooty moulds (Hely et al., 1982), dieback of stems and apices (Meyer, 1978; Newbery, 1980b), leaf loss (Hill, 1980) and stunting of growth and altered patterns of resource allocation (Vranjic and Gullan, 1990). In extreme cases, scale insect infestations cause plant death, even of mature trees (McKenzie, 1941; Kom~rek, 1946).

1. Shoot growth Both the rate of leaf production and the rate of leaf loss are affected by scale insect infestation. Heavy infestations of Icerya seycheUarum reduced leaf production on the shrubs Euphorbia pyrifolia and Scaevola taccada by 40% and 39% respectively (Newbery, 1980b,c). On E. pyrifolia, the rate of leaf area production decreased and the proportion of leaves lost increased with the level of infestation (Newbery, 1980b). The gum tree scale, Eriococcus coriaceus, did not affect the total number of leaves produced

329

Effects on host plant

by seedling Eucalyptus blakelyi but did reduce total leaf area (Vranjic and Gullan, 1990). Infested plants generated more leaves from the basal epicormic buds and produced fewer leaves on the remainder of the plant than did uninfested plants. However, the smaller leaves produced by the basal regeneration did not fully compensate for the decrease in leaf area on other shoots. Cladophyll production on Opuntia species was markedly reduced byDactylopius confusus (Cockerell) (Dactylopiidae) (Gilreath and Smith, 1988): only 4 % of cladophylls produced new growth on plants with unchecked scale insect populations compared with 75 % of cladophylls on plants where the population was controlled by natural enemies. Scale insect infestations reduce the biomass of leaves and stems (Table 1.3.1.1), which is to be expected since these are the plant parts directly affected by infestations. Decreased biomass is a consequence of lower leaf production, higher leaf loss and stem dieback. On Guaiacum sanctum and Eucalyptus blakelyi, the shoot biomass of heavily infested plants was at least 50% lower than comparable uninfested plants (Schaffer and Mason, 1990; Vranjic and Gullan, 1990).

TABLE 1.3.1.1 Mean dry weights (g) of different plant parts in experiments assessing the influence of scale insects on whole plant growth. The ratio of the mean infested (Inf.) relative to mean uninfested control (Ctl) values are expressed as percentages. Scale insect

Host plant

Toumeyella sp.

Guaiacum Leaves sanctum Stems Roots

(Coccidae)

Plant part

Control Infested I n f . / C O (g) (g) %

Reference

35.400 121.700 65.300

9.900 46.100 18.600

28.0 37.9 28.5

Schafferand Mason (1990) Vranjic and Gullan (1990)

Eriococcus coriaceus (Eriococcidae)

Eucalyptus Leaves blakelyi Stems Lignotuber Roots

10.000 7.200 1.600 15.800

5.600 3.200 0.500 4.100

56.0 44.4 31.2 25.9

lcerya seychellarum (Margarodidae)

Scaevola taccada

New roots

0.063

0.002

3.2

Newbery(1980c)

2. Root growth The impact of shoot herbivores on root growth has been greatly underestimated and neglected, largely because of the difficulty in accurately measuring root growth, particularly in the field. Although changes to the root system are largely unseen, roots appear to be affected to an equivalent or even greater degree than shoots (Table 1.3.1.1). This effect appears to be consistent across different species. Young trees of sycamore (Acer pseudoplatanus L.), lime (Tilia cordata Miller) and horse chestnut (Aesculus hippocastanum L.) infested by the horse chestnut scale, Pulvinaria regalis Canard (Coccidae), all showed strong reductions in root growth, despite variable effects of the scale insect on shoot elongation (Speight, 1991). Vranjic and Gullan (1990) noted that the plant parts most affected by infestation of Eriococcus coriaceus on Eucalyptus blakelyi were the roots: infested plants had only a quarter the root dry weight of uninfested plants. In eucalypts, roots not only appear to be the most rapidly affected plant part, but are also the fastest to recover following eradication of scale insects (Vranjic, 1993). Similarly, manual removal of lcerya seychellarum markedly improved the production of new roots on potted seedlings of Scaevola taccada transplanted from

Section 1.3.1 references, p. 334

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Ecology

the wild, while infested plants barely showed any root growth (Newbery 1980c; Table 1.3.1.1). In addition, scale insect infestations may interact with mycorrhizal symbiosis in two main ways. Firstly, infestations may reduce the carbon available for mycorrhizal synthesis, which requires a large proportion of the photosynthate; secondly, increased nutrient availability, resulting from extensive mycorrhizal formation, may enhance the allocation of carbon to defensive compounds, thereby improving the potential for resistance. Del Vecchio et al. (1993) observed that juvenile Pinus edulis Englm., which were susceptible to infestation by Matsucoccus acalyptus Herbert (Margarodidae), had a significantly lower incidence of ectomycorrhizal formation than trees resistant to infestation. Mycorrhizal formation on susceptible trees, however, recovered almost completely after eradication of the infestation. This suggests that the decline in mycorrhizal synthesis resulted from scale insect herbivory. The interesting prospect that mycorrhizas might confer resistance against herbivores has yet to be fully explored. These severe effects on root growth and function would reduce the ability of plants to take up nutrients and water, thereby further limiting growth in addition to the direct drain on resources imposed by the insects. Any decrease in the extent of root production may also render a plant susceptible to additional stresses such as drought or to structural weakening.

3. Flower and fruit production Few studies consider the impact of scale insect infestations on plant reproduction because many host plants are perennial and woody and, consequently, longer term studies are required to assess this kind of impact. However, the reduction in yield of crops such as Citrus is a major reason why scale insects are economically important. It is to be expected that the diversion of resources by scale insects would have a negative impact on host reproduction because developing flowers and fruits are strong nutrient sinks that require a large proportion of the plant's resources. Field observations showed that the extent of flowering and fruiting by Scaevola taccada was negatively correlated with the degree of infestation by Icerya seychellarum (Newbery, 1980c), although no such correlations were found with two other host plants, Avicennia marina (Forsk.) Vierh. and Euphorbia pyrifolia (Newbery, 1980a,b). 4. Architecture and allocation Scale infestation can change the shape and architecture of the plant. This is due to altered patterns of allocation at the level of the entire plant (e. g., root-shoot ratio) or of individual modules (i.e. relative sink strength and dominance of meristems). Changes in root-shoot ratio were noted by Speight (1991) and Vranjic and Gullan (1990), who observed that host plants had lower root-shoot ratios when infested with scale insects. The impact of scale insects on biomass allocation was similar to the changes associated with low light stress (Mooney et al., 1988). The mechanisms underlying control of the root-shoot ratio are not fully understood, although available evidence supports an hypothesis involving the supply and demand of both carbon and nitrogen between the plant parts (Wilson, 1988). The changes in root-shoot ratio arise because photosynthetic sources supply the carbohydrate demands of the shoot and, therefore, the insect population, prior to meeting the demands of below-ground sinks. Consequently, the drain caused by scale insect feeding activity results in less assimilate becoming available for root growth. Scale insect infestations can be considered as sink analogues; i.e. the effects of their feeding are analogous to adding extra within-plant sinks. The partitioning of resources among shoot modules depends upon demands exerted by competing meristems and the relative strengths of plant and insect "sinks'. The strength of plant sinks on infested shoots progressively weakens as an infestation (i.e. insect sinks) develop because a higher proportion of resources is diverted from the shoot to the insect population. When scale insects divert sufficient resources to cause death of a leading apex, the removal of

Effects on host plant

331

apical dominance encourages lower branches or regenerative shoots to grow (resources permitting). Distortions in the shape of young trees have a detrimental effect on the later value of trees as timber. Apical death and/or regenerative growth are symptomatic of severe infestations by several species of scale insects (McKenzie, 1941; Burns and Donley, 1970; Vranjic and Gullan, 1990). Bums and Donley (1970) identified four different types of architectural changes to Liriodendron tulipifera trees infested with scale insects, based on the regrowth pattern following apical death: 1) death of the leading shoot with a subsequent lateral becoming dominant, 2) death of the leader with no new dominant, resulting in generally increased bushiness, 3) reduced vigour showing sparse foliage and high branch death, and 4) death of the main stem followed by basal sprouting. Such changes in the pattern of resource allocation have consequences not only for the shape of the plant but also for the subsequent survival and distribution of localized scale insect populations. Damage from scale insects and subsequent changes in the within-tree distribution of infestations has not been studied in the context of plant modularity and source-sink relationships.

FACTORS AFFECTING PLANT RESPONSES Numerous factors, both genetic and environmental, influence the responses of plants to scale insect infestation. The species of plant and scale insect involved in the interaction are but one source of variation. For instance, young sycamore, lime and horse chestnut trees responded in different ways when infested by the same species of scale insect (Pulvinaria regalis) (Speight, 1991). Shoot elongation of sycamore and horse chestnut decreased as a result of infestation, although only the former was significant; in contrast, the shoot elongation of lime trees increased slightly (but not significantly) with infestation. However, even within a plant species there can be genotypes differing in susceptibility to infestation (McClure, 1985; Schvester, 1988). Plants vary both spatially and temporally in susceptibility to scale infestations, showing outbreaks in some regions or years but not others. It has been suggested that environmental factors can alter plant physiology to render the host temporarily resistant to scale, a phenomenon termed pheno-immunity (Flanders, 1970). The sources of variation for scale insect infestations are multiplied when the numerous and interesting interactions between scale insects and their associated organisms are considered. Few of these possibilities have been studied with respect to plant responses and only some major influences that have received attention are discussed below.

1. Host plant condition A plant's response to infestation is influenced by its current status (e.g., age, size, health), which is partly determined by the growth conditions which it is currently experiencing (e.g., seasonality, availability of nutrients, water, light, herbivores)or has previously experienced (e.g., stored resources) (Washburn et al., 1985). Older, larger plants generally appear to be more tolerant of infestations. Thus, although small bushes of Atriplex vesicaria Hew. ex Benth. were attacked by the coccid, Megapulvinaria maskelli (Olliff) (Coccidae) less frequently than large bushes, they showed a greater incidence of branch death (Briese, 1982). Also, it took less time and a smaller population of coccids to inflict noticeable damage on smaller bushes. A prolonged infestation presumably increases the risk of predation, so that the larger populations needed to inflict damage to larger plants are less likely to be maintained. Older ash (Fraxinus sp.) trees survived attack by Eulecanium tiliae better than younger trees, unless the attack was accompanied by adverse environmental conditions such as drought

Section 1.3.1 references, p. 334

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332

or extreme cold (Kom,~rek, 1946). Field surveys showed that larger, older mangrove (Avicennia marina) trees supported larger populations of Icerya seychellarum (Newbery, 1980a). However, there were no correlations between growth and age (except for shoot vigour), growth and infestation, or nutrient status and age. It was also noted that larger trees were subjected to poorer drainage and that leaves of young mangroves retained a film of salt solution, both of which may have affected their susceptibility to attack. The ways in which certain environmental factors affect scale insect populations have been examined more widely than how they influence plant responses to the scales. Scale insects generally respond positively to an improvement in plant nitrogen content, for example, after added fertilizer. Addition of nitrogenous fertilizer to Citrus increased the size of female Ceroplastes sinensis Del Guercio and Ceroplastes destructor Newstead (Coccidae) (Beattie et al., 1990). Populations of Toumeyella parvicornis (Cockerell) increased when host trees (Pinus banksiana Lamb.) were given urea but declined on trees given potassium (Smimoff and Valero, 1975). Moderate host plant stress is thought to particularly affect the performance of sap sucking insects because this feeding guild may be more sensitive to slight changes in nutritive and defensive compounds in the phloem (Larsson, 1989). However, the survivorship of Pseudaulacaspis pentagona (Targioni Tozzetti) (Diaspididae) on urban mulberry (Morus alba L.) trees was positively correlated with shoot water potential; i.e. the armoured scale insects survived best on unstressed trees (Hanks and Denno, 1993). Furthermore, the wide variation in water potential among trees spaced less than ten metres apart suggested that environmental stress was a strong factor influencing the small-scale distribution of scale insects. The impact of additional nutrients or of stress on scale insects presumably has a concomitant effect on plant growth, as larger scale insects remove more resources and produce more offspring. Changes in growth conditions, however, also affect plant growth directly. If additional nutrition leads to rapid growth, as occurs with eucalypts, the improved vigour may temporarily enhance tolerance to the infestation; conversely, stressing the host may prevent such a response and worsen the impact of infestation (Vranjic, 1993). The correct timing and application of fertilizers or water to plants could be incorporated into cultural control schemes to minimise the impact of insect damage. Interactions between scale insects and plant secondary compounds are rarely studied. Despite notions that phloem-feeders can avoid defensive compounds, particularly if they are compartmentalized (Raven, 1983), some studies have detected secondary compounds in the honeydew of aphids (Molyneux et al., 1990). McClure and Hare (1984) observed that the fecundity of two diaspidid species (Fiorinia externa Ferris and Nuculaspis tsugae (Marlatt)) was related to the composition of foliar terpenoids in two species of hemlock (Tsuga spp.). Variation in secondary chemistry, therefore, should not be ignored when differential susceptibility of trees to infestation is being investigated.

2. Insect population density Another important factor affecting plant response is the size and duration of the insect infestation. This can determine whether a plant continues to grow, reduces growth, stops growing or begins to show dieback. Measures of plant growth often show a negative correlation or a negatively asymptotic decline as the size of the infestation increases (Newbery, 1980a,b,c; Washburn et al., 1985; Speight, 1991; Vranjic, 1993). A greater insect load on host plants presumably constitutes a larger drain of resources from feeding as well as producing more widespread accretions of sooty moulds. Insect population density has been positively correlated with the extent of sooty mould contamination on leaves (Newbery, 1980a,c; Brink and Hewitt, 1992). However, dense populations that lower host quality can exert a negative feedback on the insect population in several ways. Direct mortality of sedentary insects, such as coccoids, can occur by stem dieback and leaf abscission (Faeth et al., 1981). Death or decline of plant parts reduces the availability of suitable feeding sites for subsequent generations (Washburn

Effects on host plant

333

et al., 1985), and higher population densities increase the possibility of their being smothered under sooty mould or honeydew excreted by other nearby individuals (Collins and Scott, 1982; Washburn et al., 1985).

3. Ant attendance The presence of ants can affect host plants indirectly in several ways (Buckley, 1987). Ants can enhance scale insect growth and survival by stimulating feeding rates and by deterring the natural enemies of scale insects, and thus potentially increase the detrimental effects on plant growth. This appears to have been the case with Eriococcus coriaceus and E. confusus on eucalypts (Amey, 1993), although some natural enemies of these scale insects did circumvent antagonism by ants through behavioural or morphological adaptations. Ants can also indirectly benefit plants by reducing the incidence of sooty moulds through feeding on the honeydew (Bach, 1991), and by deterring other herbivores. Ants, therefore, exert a combination of detrimental and beneficial effects on plant growth. Identifying which of these influences is the most important and determining the balance of these effects on plant growth, requires experimentation but few such studies have been undertaken using scale insects. The overall effect of ant attendance on Coccus viridis was indirectly beneficial to the plant Pluchea indica (Bach, 1991), the main effects of the ants being to deter herbivores and to lower the incidence of sooty moulds. The potential benefits of ants to plant growth suggests an important role for ants in pest management (Way and Khoo, 1992; Arney, 1993). Ant-coccid interactions are discussed further in Section 1.3.5.

SUMMARY AND RECOMMENDATIONS FOR FUTURE RESEARCH

The major effects of scale insects on plant growth occur by the depletion of resources and by the suppression of photosynthesis. It is, perhaps, because scale insects affect plants physiologically at such a fundamental level that their damage is not limited to particular tissues but influences the whole plant, including the roots. There is no doubt that scale insects can seriously reduce host plant growth: heavy infestations are severely detrimental and may even cause death. Whilst this is recognized, the impact of recurrent, low-level, scale infestations has been ignored, despite studies that demonstrate the negative effects of chronic herbivory (e.g., Morrow and LaMarche, 1978). The full extent to which scale insects affect physiology is poorly understood. In particular, their effects on plant carbon and nitrogen economies and the impact of sooty moulds on photosynthesis and gas exchange need to be quantified further, in order to accurately assess the economic value of scale insect infestations. As well as their physiological impact, scale insects also affect the ecological interactions of their host plants. The loss of vigour and reduced capability of infested plants to recover renders them more susceptible to subsequent stresses, such as drought and competition. Plant responses to scale insect infestation are modified by plant genotype and growth condition. These factors have implications for potential cultural control of scale insects and also for the fitness and composition of future plant populations. Scale insect - host plant interactions are complicated by the association of scale insects with other organisms, chiefly natural enemies, ants and sooty moulds. These agents may exert a modifying influence on plant growth responses to scale insect feeding activities. Sooty mould can cause considerable detriment to plant growth, while ants on the other hand, may benefit plants by deterring other herbivores and the accumulation of sooty mould. Further experimentation examining coccoid-ant-fungal interactions from the

Section 1.3.1 references, p. 334

Ecology

334

viewpoint of plant growth is required to demonstrate the validity and generality of the ecological relationships pertaining to honeydew-producing Coccoidea.

ACKNOWLEDGEMENTS I am grateful to Dr Julian Ash for his useful criticisms of the draft manuscript, to Dr Penny Gullan for checking the validity of scale insect names and comments on the manuscript, and to Dr Mary Carver for checking the validity of some aphid names.

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Variations in susceptibility of Pinus pinaster to Matsucoccus feytaudi (Homoptera: Margarodidae). In: W.J. Mattson, J. Levieux and C. Bernard-Dagan (Editors), Mechanisms of Woody Plant Defenses against Insects, Search for Pattern. Springer-Verlag, New York, pp. 267-275.

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Ecology Smirnoff, W.A. and Valero, J., 1975. Effets h moyen terme de la fertilisation par urde ou par potassium sur Pinus bankm'ana L. et le comportement de ses insectes ddvastateurs: tel que Neodiprion swainei (Hymenoptera: Tenthredinidae) et Toumeyella numismaticum (Homoptera: Coccidae). Canadian Journal of Forest Research, 5: 236-244. Speight, M.R., 1991. The impact of leaf feeding nymphs of the horse chestnut scale, Pulvinaria regalis Canard (Hem., Coccidae), on young host trees. Journal of Applied Entomology, 69:551-553. Tedders, W.L. and Smith, J.S., 1976. Shading effect on pecan by sooty mould growth. Journal of Economic Entomology, 69: 551-553. van Hook, R.I., Nielsen, M.G. and Shugart, H.H., 1980. Energy and nitrogen relations for a Macrosiphum liriodendri (Homoptera: Aphididae) population in an east Tennessee Liriodendron tulipifera stand. Ecology, 61 : 960-975. Vranjic, J.A., 1993. Whole Plant Responses of Eucalypt Seedlings to Infestation by Scale Insects. Ph.D. Thesis, Division of Botany and Zoology, Australian National University, Canberra. Vranjic, J.A. and Gullan, P.J., 1990. The effect of a sap-sucking herbivore, Eriococcus coriaceus (Homoptera: Eriococcidae), on seedling growth and architecture in Eucalyptus blakelyi. Oikos, 59: 157-162. Wainhouse, D., Gate, I.M. and Lonsdale, D., 1988. Beech resistance to the beech scale: a variety of defenses. In: W.J. Mattson, J. Levieux and C. Bernard-Dagan (Editors), Mechanisms of Woody Plant Defenses against Insects, Search for Pattern. Springer-Verlag, New York, pp. 277-293. Walstad, J.D., Nielsen, D.G. and Johnson, N.E., 1973. Effects of the pine needle scale on photosynthesis of Scots pine. Forest Science, 19:109-111. Washburn, J.O., Frankie, G.W. and Grace, J.K., 1985. Effects of density on survival, development and fecundity of the sot~ scale, Pulvinaria mesembryanthemi (Homoptera: Coccidae) and its host plant. Environmental Entomology, 14: 755-761. Way, M.J. and Khoo, K.C., 1992. Role of ants in pest management. Annual Review of Entomology, 37: 479-503. Wilson, J.B., 1988. A review of evidence on the control of shoot: root ratio, in relation to models. Annals of Botany, 61 : 433-449.

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Gall Formation

JOHN W. BEARDSLEY

INTRODUCTION Within the superfamily Coccoidea, gall-forming species have been described in eight major family level taxa: Margarodidae, Pseudococcidae, Kermesidae, Lecanodiaspididae, Eriococcidae, Coccidae, Asterolecaniidae, and Diaspididae. However, of the more than 160 species of obligatory gallicolus Coccoidea known, only a single species of Coccidae, the African Cissococcus fulleri Cockerell, produces plant galls (Beardsley, 1984).

Cissococcus fulled Cockerell Cockerell's (1902) brief description of C. fulleri was supplemented by a relatively detailed redescription by Brain (1918), based upon a second collection from South Africa. Ferris (1919), apparently before seeing Brain's work, gave descriptive notes on the adult female and first stage nymph, based on part of the type material. Apart from Steinweden's (1929) brief reference, no mention of C. fulleri is made until 1994, when Hodgson provided a detailed description of the adult female. Cissococcus fulleri forms large globular pear- or urn-shaped galls on stems, tendrils and leaf stalks of a vine, Cissus cuneifolia (Vitaceae). The female insect develops enclosed within the gall, and the caudal end of the adult female is modified and sclerotized to form an operculum which closes the gall aperture. The operculum bears the anal plates which, presumably, permit the coccid to void honeydew into the outside environment. Regarding the galls, Brain (1918) stated "The normal gall averages 12 mm long, is broad pear-shaped, almost as broad as long, broadly rounded at the base and slightly tapering to the end where the orifice is situated. The galls are usually fixed by one side, so that the long axis of the gall is parallel with the stem or tendril to which it is attached. The galls apparently grow very rapidly from June to August, for in the material just received (8th August 1916) Mr. Fuller writes that the galls have all developed in the last six weeks." Brain (1918) stated further that "the orifice of the gall is conical, the thin outer edge being brown and hard in texture, the inside appearing sorer and green." (See Fig. 1.1.3.1 in Section 1.1.3.1). Apparently, C. fulleri is bisexual, although the males are not gallicolus. Brain described the male puparium as "delicate, glass-like, not divided into def'mite plates as in the 8' LECANIINAE." His description and the accompanying figure indicate the presence of long curled white glassy wax filaments over the dorsal surface of the male puparium. He did not describe the adult male. In his original description, Cockerell (1902) placed C. fulleri with the eriococcids, stating "Belongs to the Eriococcini. Larva typically Eriococcine, with rows of dorsal

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Ecology spines..." Brain (1918) placed the species in a new subfamily, the Cissococinae, within the Coccidae (= Coccoidea of present authors). Ferris (1919) redescribed and illustrated the first-stage nymph, showing that there are no dorsal spines, although a marginal series of spines is present. Ferris assigned the species to the Coccinae (=Coccidae as presently defined) on the basis of larval and adult female morphology. Steinweden (1929) concurred with Ferris's placement of the genus in the Coccidae. Hodgson (1994) also considered C. fulleri to belong to the Coccidae, but suggested that some of the features which had evolved (presumably in relation to its gall-forming habit)justified its separation into the monogeneric subfamily Cissococcinae. The phylogenetic analysis in Section 1.1.3.7, which is based on characters of the lst-instar nymph, adult male as well as the adult female, confirms the placement of Cissococcus in the Coccidae. The unusual features noted by Hodgson (1994) were (i) lack of an anal cleft, (ii) complete lack of antennae, (iii) reduction of the dorsum to a very small area around the anal plates, (iv) displacement of the rudimentary legs, mouthparts and spiracles onto the upper surface, so that (v) the labium is more anterior than the clypeolabial shield. Cockerell's type material was taken from Umquahumbi Valley, South Africa, while the material that Brain received from Fuller was collected on the Natal Coast near Durban. Brain's description is relatively detailed and includes a figure of the female operculum as well as photographs of the galls. Hodgson's (1994) description was based on two lots of material, one from wild grape in Natal, but collected in 1935, while the second lot had no collection data. Aside from these collections, there appears to be little information available about the distribution of this unusual species. That there is but a single known gallicolus coccid species seems anomalous, in view of the relatively common occurrence of gall formation among the Eriococcidae and Asterolecaniidae, families which appear to be closely related to the Coccidae. Possibly, additional collecting, particularly in Africa, may turn up additional gallicolus forms. However, our present knowledge of the World's coccoid fauna seems sufficient to rule out the likelihood that many gall-forming Coccidae remain undiscovered.

REFERENCES Beardsley, J.W., 1984. Gall-forming Coccoidea. In: T.N. Ananthakrishnan (Editor), The Biology of Gall Insects. Oxford and IBH Pubs, New Delhi. pp. 79-106. Brain, C.K., 1918. Coccidae of South Africa - II. Bulletin of Entomological Research, 9: 131-163, pls. XIV-XVIII. Cockerell, T.D.A., 1902. New genera and species of Coccidae, with notes on known species. Annales and Magazine of Natural History (Ser. 7), 9: 20-26. Ferris, G.F., 1919. Notes on Coccidae -III, (Hemiptera). Canadian Entomologist, 51: 108-113. Hodgson, C.J., 1994. The Scale Insect Family Coccidae: an Identification Manual to Genera. CAB International, Wallingford, UK, vi+639 pp. Steinweden, J.B., 1929. Basis for the generic classification of the coccoid family Coccidae. Annales of the Emomological Society of America, 22: 197-245.

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1.3.3 Crawler Behaviour and Dispersal DAVID J. GREATHEAD

INTRODUCTION Many important pest species of Coccoidea have been spread by man through the movement of cuttings, nursery stock and produce, to the extent that they are now virtually cosmopolitan (Simmonds and Greathead, 1977). Consequently, natural dispersal mechanisms have been a largely neglected topic for research. Because most crawlers settle close to the parent female (e.g. Bodenheimer, 1935) and because coccids, except males, lack any obvious means of movement over greater distances, there has been a widespread belief that their powers of dispersal are poor. Phoretic transfer of crawlers and gravid females on human clothing, in the hair of mammals and on the plumage of birds is commonly believed to be an important means of dispersal, but Washburn and Frankie (1981), working in California, showed that, whilst crawlers and ovisacs of the iceplant scale, Pulvinariella mesembryanthemi (Vallot), could adhere to clothing and the hair of dogs and could survive long enough for transport to another site, laboratory tests indicated that survival on mice was less than one hour and on parakeets only 15 minutes. Thus, they concluded that this means of dispersal is probably less important than wind. Studies on this and other species of soft scales, using sticky traps, have shown that crawlers can be dispersed over considerable distances on wind currents, as was first demonstrated by Quayle (1916) for the black scale, Saissetia oleae (Olivier), in Californian citrus groves. Experimental results demonstrating the importance of wind in the dispersal of crawlers of armored scales (Diaspididae), principally Aulacaspis tegalensis (Zehntner) and Aonidiella aurantii (Maskell), has been reviewed in an accompanying volume in this series (Greathead, 1989). Information is also available on the dispersal of representatives of other families, notably mealybugs on cocoa in Ghana (Comwell, 1958, 1960); margarodids Icerya seychellarum Westwood on Aldabra Atoll in the Indian Ocean (Hill, 1980) and Matsucoccus resinosae Bean and Godwin on red pine in Connecticut (Stephens and Aylor, 1978); an eriococcid, Cryptococcus fagisuga Lindinger, on beech trees in England (Wainhouse, 1980) and a dactylopiid, Dactylopius austrinus De Lotto, on Opuntia aurantiaca Lindley in South Africa (Moran et al., 1982). These studies have all shown that dispersal by wind currents is a common feature among Coccoidea but there is less information on the behaviour associated with this phenomenon. The most comprehensive study of dispersal of soft scale crawlers has been made on P. mesembryanthemi and Pulvinaria delottoi (Gill) in California (Washburn and Frankie, 1981, 1985; Washburn and Washburn, 1984). Other relevant observations have been made on the citrus scale, Coccus hesperidum L. in Texas (Hoelscher, 1967; Reed et al., 1970), the pine tortoise scale, Toumeyella numismaticum (Pettit and McDaniel) [ = Toumeyella parvicornis (Cockerell] in Manitoba (Rabkin and Lejeune, 1954), S. oleae (Mendel et al., 1984) and the Florida wax scale, Ceroplastes floridensis Comstock

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(Yardeni, 1987), the latter two species on citrus in Israel. Because of the similarity in behaviour and dispersal mechanisms exhibited by the crawlers of the investigated species from the various families, this review draws on these observations to supplement the meagre information on dispersal by soft scale crawlers.

CRAWLER BEHAVIOUR Under alternating light:dark regimes, crawlers of S. oleae emerge from beneath the female at the onset of the light phase in laboratory tests (Mendel et al., 1984) and so would emerge shortly after dawn in the field, as do the crawlers of armored scales (Greathead, 1989), lcerya seychellarum (Hill, 1980) and presumably most scale insects. Survival of S. oleae crawlers depends on temperature and humidity, varying from over twelve days at 23~ at 100% RH to less than a day at 29~ at any humidity (Mendel et al., 1984). Pulvinariella mesembryanthemi crawlers appear to be more robust and survive about four days in dry air and eight days in moist air (Washburn and Frankie, 1981). The majority of crawlers of all the species studied wander for less than a day before settling near the female - 80% of those of S. oleae settled within 24 hours (Mendel et al., 1984). Washburn and Frankie (1981) measured the speed ofwalking of P. mesembryanthemi crawlers as 0.72-1-0.22 mm sec ~ in a greenhouse experiment (but Greathead (1975) had shown that the speext of movement of Aulacaspis tegalensis crawlers was strongly affected by humidity). They also demonstrated that there was little movement between plants laid out on a grid in the greenhouse. The crawlers move upwards on the plant which has the effect of bringing them to younger leaves which are the preferred feexling sites (Washburn and Frankie, 1985). In laboratory tests, 80% of the crawlers moved into the illuminated areas of a test arena (Washburn and Frankie, 1981) and thus were positively phototropic and negatively geotropic, as are those of armored scales (Greathead, 1989). Evidently not all scale insects respond to gravity because Wainhouse (1980) was only able to demonstrate phototaxis in Cryptococcus fagisuga. These behaviours bring crawlers to young tissue which is preferred and also to the tops of plants where those that have not settled can be dislodged by air currents. Wind tunnel experiments with P. mesembryanthemi showed that the crawlers exhibit take-off behaviour (Washburn and Washburn, 1984) (as did the white sugarcane scale, Aulacaspis tegalensis) but apparently not in another armored scale, the citrus red scale, Aonidiella aurantii (Greathead, 1989) and so this behaviour may not be present in all species. Crawlers submitted to wind strengths of between 1.8 and 4.0 m sec ~ take up a characteristic position which facilitates removal from the substrate. They rise, facing away from the air current, on their second and third pairs of legs, or on the third pair only, with the antennae and free legs outstretched. This position appears to facilitate dislodgement by increasing drag and reducing the grip of the tarsal claws on the substrate. This behaviour is only exhibited by crawlers over 76 hours old, i.e. those which have not settled during the first 24 hours. In the field, crawlers accumulate at the tips of leaves at the tops of the host plants from which they are carried away by the wind.

DISPERSAL BY AIR CURRENTS Washburn and Frankie (1981) used sticky boards on 1 m poles and 3.5 m towers to demonstrate wind dispersal of P. mesembryanthemi and measured a maximum interception rate 10 cm above the canopy of 225 crawlers h ~ over their 48 hour sampling period, when the average wind speed was 13.4 km h ~. Crawler density decreased with height and was highest on boards facing into the wind. Crawlers were captured up to a maximum of 50 m above the ground (Washburn and Frankie, 1985). From these

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observations, and from the results of laboratory experiments indicating a sinking speeA of 26.2 cm see ~ for live crawlers in still air, Washburn and Washburn (1984) concluded that crawlers could be transported well over 190 km in 24 hours at a wind speed of 8 km h ~ Other investigators have measured downwind dispersal with traps laid out at distances from source populations of scales. Thus, Rabkin and Lejeune (1954) found crawlers of Toumeyella numismaticum (Pettit & McDaniel) [= Toumeyella parvicornis (Cockerell] up to 4.8 km (3 miles) downwind and Hoelscher (1967) trapped Coccus hesperidum crawlers 55 m from the source. Reed et al. (1970) observed infestations near windbreaks and noted that they were lower on the lee side, where catches on sticky boards were also less, confirming that airborne crawlers are an important source of infestation (see Greathead, 1972, for similar observations on Aulacaspis tegalensis and explanation of the effect of windbreaks on the distribution of air-borne insects). Yardeni (1987), working with Ceroplastesfloridensis in Israel, found that 79% of crawlers on sticky traps were captured downwind of infested trees and that clean trees downwind of the source developed infestations more frequently on the upwind side (26 %) than on the downwind side (8 %).

DISCUSSION These observations on soft scales are consistent with those obtained with the crawlers of armored scale insects (Greathead, 1989), namely that the principal natural means of dispersal from host plant to host plant within an area and over greater distances between suitable habitats is by transport on air currents. However, there is no proof that dispersal over distances of tens or hundreds of kilometres actually takes place although there is strong circumstantial evidence that this happened in eastern Africa with A. tegalensis, which feeds only on sugarcane. The longest observed distance travelled by airborne crawlers relates to Icerya seychellarum which was trapped over water 3.5 km downwind of an infestation (Hill, 1980). Wainhouse (1980) quotes evidence that Cryptococcus fagisuga spread at a rate of 6-8 km yr m following its introduction into North America in 1890. Both A. tegalensis, which feeds on sugarcane, and P. mesembryanthemi, which feeds on the iceplant Carpobrotus edulis (L.), have been shown to exhibit take-off behaviour which indicates that, in these species at least, dispersal on air currents is not accidental. They are also unusually fecund; P. mesembryanthemi produces up to 2,400 crawlers (Washburn and Frankie, 1985) whereas Toumeyella parvicornis, feeding on pine trees, produces only 534 +50 eggs. Another scale insect which exhibits take-off behaviour is Dactylopius austrinus. The crawlers of this species are sexually dimorphic, the female crawlers developing long wax threads which aid dispersal. The males do not develop these waxy threads but are able to disperse as winged adults, unlike the females (Moran et al., 1982). In keeping with the ecological explanation of migratory behaviour put forward by Southwood (1962) and Johnson (1969), Greathead (1972) suggested that take-off behaviour is an adaptation to short-lived host plants which constitute temporary habitats, whereas the majority of scale insects feed on trees which can be regarded as permanent habitats. These authors propose that migrant species occupy temporary or unstable habitats. Thus, it would also be expected that the majority of pest species, feeding on tree crops, will be less adapted for dispersal and less fecund. However, even if they do not disperse as readily, the observations reviewed here do indicate that movement between trees is predominantly on air currents and that transport on the bodies of animals is likely to be less important. Gunn (1979) attempted to verify this hypothesis by collecting information from the literature on the fecundity of scale insects but he was

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u n a b l e to fred clear e v i d e n c e to substantiate it. H o w e v e r , as p o i n t e d out by W i l l i a m s ( 1 9 7 0 ) , m a n y p u b l i s h e d estimates o f fecundity are serious u n d e r e s t i m a t e s , so that such c o m p a r i s o n s are unreliable.

REFERENCES Bodenheimer, F.S., 1935. Citrus Entomology in the Middle East. Dr W. Junk, The Hague, 663 pp. Cornwell, P.B., 1958. Movement of the vectors of virus diseases of cocoa in Ghana. I. Canopy movement in and between trees. Bulletin of Entomological Research, 49: 613-630. Cornwell, P.B., 1960. Movement of the vectors of virus diseases of cocoa in Ghana. II. Wind movement and aerial dispersal. Bulletin of Entomological Research, 51: 175-201. Greathead, D.J., 1972. Dispersal of the sugar-cane scale Aulacaspis tegalensis (Zhnt.) (Hem., Diaspididae) by air currents. Bulletin of Entomological Research, 61: 54%558. Greathead, D.J., 1975. The ecology of a scale insect, Aulacaspis tegalensis, on sugar cane in East Africa. Transactions of the Royal Entomological Society of London, 127:104-114. Greathead, D.J., 1989. Crawler behaviour and dispersal. In: D. Rosen (Editor), Armored Scale Insects. Their Biology, Natural Enemies and Control. Vol. A. Elsevier Scientific Publishers, Amsterdam, pp. 305-308. Gunn, B.H., 1979. Dispersal of the cochineal insect Dactylopius austrinus De Lotto (Homoptera: Dactylopiidae). Ph.D. Thesis, Rhodes University, Grahamstown, South Africa. Hill, M.G., 1980. Wind dispersal of the coccid lcerya seychellarum (Margarodidae: Homoptera) on Aldabra Atoll. Journal of Animal Ecology, 49: 939-957. Hoelscher, C. L., 1967. Wind dispersal of brown soR scale crawlers, Coccus hesperidum (Homoptera: Coccidae), and Texas citrus mites, Eutetranychus banksi (Acarina: Tetranychidae) from Texas citrus. Annals of the Entomological Society of America, 60: 673-678. Johnson, C.G., 1969. Migration and Dispersal of Insects by Flight. Methuen, London, 763 pp. Mendel, Z., Podoler, H. and Rosen, D., 1984. Population dynamics of the Mediterranean black scale, Saissetia oleae (Olivier), on citrus in Israel. 5. The crawlers. Journal of the Entomological Society of Southern Africa, 47: 23-34. Moran, V.C., Gunn, B.H. and Walter, G.H., 1982. Wind dispersal and settling of first-instar crawlers of the cochineal insect Dactylopius austrinus (Homoptera: Coccoidea: Dactylopiidae). Ecological Entomology, 7: 409-419. Quayle, H.J., 1916. Dispersion of scale insects by the wind. Journal of Economic Entomology, 9: 486-493. Rabkin, F.B. and Lejeune, R.R., 1954. Some aspects of the biology and dispersal of the pine tortoise scale, Toumeyella numismaticum (Pettit and McDaniel) (Homoptera: Coccidae). Canadian Entomologist, 86: 570-575. Reed, D.K., Hart, W.G. and Ingle, S.J., 1970. Influence of windbreaks on distribution and abundance of brown sot~ scale in citrus groves. Annals of the Entomological Society of America, 63: 792-794. Simmonds, F.J. and Greathead, D.J., 1977. Introductions and pest and weed problems. In: J.M. Cherrett and G.R. Sagar (F.,ditors). Origins of Pest, Parasite, Disease and Weed Problems. Blackwell Scientific Publications, Oxford, pp. 109-124. Southwood, T.R.E., 1962. Migration of terrestrial arthropods with particular reference to the study of insect populations. Biological Reviews, 37: 171-214. Stephens, G.R. and Aylor, D.E., 1978. Aerial dispersal of red pine scale, Matsucoccus resinosae (Homoptera: Margarodidae). Environmental Entomology, 7: 556-563. Wainhouse, D., 1980. Dispersal of first instar larvae of the felted beech scale, Cryptococcus fagisuga. Journal of Applied Ecology, 17: 523-532. Washburn, J.O. and Frankie, G.W., 1981. Dispersal of a scale insect, Pulvinariella mesembryanthemi (Homoptera: Coccoidea) on iceplant in California. Environmental Entomology, 10: 724-727. Washburn, J.O. and Frankie, G.W., 1985. Biological studies of iceplant scales, Pulvinariella mesembryanthemi and Pulvinaria delonoi (Homoptera: Coccidae), in California. Hilgardia, 53(2): 1-27. Washburn, J.O. and Washburn, L., 1984. Active aerial dispersal of minute wingless arthropods: exploitation of boundary-layer velocity gradients. Science, 223: 1088-1089. Williams, J.R., 1970. Studies on the biology, ecology and economic importance of the sugar-cane scale insect, Aulacaspis tegalensis (Zhnt.) (Diaspididae), in Mauritius. Bulletin of Entomological Research, 60:61-95. Yardeni, A., 1987. Evaluation of wind dispersed sot~ scale crawlers (Homoptera: Coccidae), in the infestation of a citrus grove in Israel. Israel Journal of Entomology, 21: 25-31.

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1.3.4. Seasonal History; Diapause SALVATORE MAROTTA and ANTONIO TRANFAGLIA

INTRODUCTION Soft scales are all phytophagous insects, with the adult females usually spending a large part of their life firmly fixed to their host plants at the point where the crawlers originally settled. Consequently, the immature stages and adult female have a close relationship with their host plant and its immediate environment. It is, therefore, not surprising that their voltinism and rate of growth and development are influenced both directly and indirectly by many environmental factors. Temperature, humidity, rainfall, wind, edaphic conditions, use of insecticides, host plant nutrition and physiology, agricultural practices and other factors are often cited as the most common influences which interact and/or control scale insect populations. An understanding of these complex factors is essential in the assessment and successful control of soft scale insects. A substantial literature about these aspects is available and, because of the previously mentioned diversity, it is difficult to generalize about them. This Section will discuss only the principal and most interesting physical and biotic factors which appear to affect soft scale populations, including their influence on the seasonal history.

VOLTINISM The seasonal history of several economically important soft scale insects has been studied in detail throughout the world. The number of generations per year and their rates of development can vary considerably, both between countries with different climatic regimes and between different host plants. For example, the brown soft scale, Coccus hesperidum Linnaeus, one of the most polyphagous Coccidae, has six to seven generations per year in greenhouses in the USSR (Saakyan-Baranova, 1964), six outdoors in Israel (Avidov and Harpaz, 1969), three to five in southern California (USA) (Ebeling, 1959), three in South Africa (Annecke, 1966), two to three in both western Sicily (Monastero, 1962) and southern France (Panis, 1977a) and one in both Sardinia (Crovetti, 1962) and eastern Sicily (Longo and Benfatto, 1982). On the other hand, for other species, the number of generations per year is relatively constant throughout their range, apparently being unaffected by environmental factors. For example, Coccus p s e u d o m a g n o l i a r u m (Kuwana) has only one generation in Greece (Argyriou and Ioannides, 1975), Israel (Ben-Dov, 1980), southern Italy (Barbagallo, 1974), Turkey ((~Sncfier and TuncS~ureck, 1975) and in California (USA) (Flanders, 1942a; Ebeling, 1959); Ceroplastes sinensis Del Guercio has only a single generation in Italy (Silvestri, 1939; Monastero and Zaami, 1959), Virginia (USA) (Williams and Kosztarab, 1972) and in New South Wales (Australia) (Snowball, 1970), while the

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Ecology

Florida wax scale, Ceroplastesfloridensis Comstock, has two generations both in Greece and Israel (Ben-Dov, 1976; Argyriou and Kourmadas, 1980; Podoler et al., 1981) and two or three in different regions of Egypt (Habib et al., 1971; Salem and Hamdy, 1985; Helmy and El-Imery, 1986). However, there are also species whose voltinism varies even within the same country. Thus, in Italy, Sphaerolecanium prunastri (Fonscolombe) has only one generation per year at high altitude but has two on the southern plains (Silvestri, 1939). The Mediterranean black scale, Saissetia oleae (Olivier), usually has only one generation per year in the Mediterranean basin (Bibolini, 1958; Argyriou, 1963; Viggiani et al., 1973; Jarraya, 1974; Tuncyurek, 1975; Panis, 1977b; Podoler et al., 1979) and in California (USA) (Ebeling, 1959), although on olive trees along the coast in Greece and Italy, it may develop a partial second generation (Argyriou, 1963; Nuzzaci, 1969; Viggiani et al., 1973). Similarly in Israel, S. oleae can develop a second generation on orange and on irrigated olive trees (Peleg, 1965; Rosen et al., 1971; Blumberg et al., 1975) while, in certain coastal regions of California (USA), it can have two generations annually on citrus (Ebeling, 1959). The seasonal history and the spatial distribution of most univoltine species of soft scales which overwinter as second-instar nymphs on the woody parts of trees (such as Parthenolecanium corni (Bouchr), P. persicae (F.) and Eulecanium tiliae (L.)), has the following general pattern (Fig. 1.3.4.1). After hatching, the first-instar nymphs or crawlers move from beneath the female cover onto the plant surface where they disperse, usually settling in clusters on the tips and along the outer margins on the topmost leaves. Greatest crawler activity is during this period and this can last several hours or even a few days. After settling and undergoing their first moult, the nymphs move less frequently. However, in the autumn, after a further moult and prior to leaf-fall, the second-instar nymphs move to the twigs and branches of the host plant, where they overwinter. However, in those species of soft scales which overwinter as the adult female, i.e. C. floridensis, C. pseudoceriferus Green and Neopulvinaria innumerabilis (Rathvon), it is the young, preovipositional female which returns to the woody parts of the plant in the autumn. This sequence of events, from emergence of the crawlers to the return of the second-instar nymphs or young females to the woody parts of the tree, is synchronized with the phenology of the host plant, probably as a result of genetically determined behavior patterns and environmental factors. The most important factors affecting these population redistributions are light, gravity, temperature, humidity or a combination of these. After hatching, the initial migration of the crawlers produces a population which is concentrated on either the upper or lower leaf surfaces, often near the canopy periphery. An initial positive phototactic dispersal has been observed in many species of different genera, for example in C. floridensis (Schneider et al., 1987a), C. hesperidum (Saakyan-Baranova, 1964), Pulvinaria vitis L. (Phillips, 1963), P. corni (Habib, 1955) and Physokermes hemichryphus (Dalman) (Pechhacker, 1971). However, the crawlers of P. corni appear not to react to a direct light source but rather to changes in light intensity (Komeili Birjandi, 1981). This reaction of the crawlers to light decreases after a period of time, suggesting that this response is affected by crawler age. Crawler establishment can also be affected by gravity (geotaxis). However, P. corni crawlers are indifferent to gravity and it is the second-instar nymphs which are positively geotactic (Habib, 1955). The crawlers of C. floridensis have a slight negative geotaxis (Schneider et al., 1987a; Komeili Birjandi, 1981), while those of C. hesperidum are strongly negatively geotactic (Bodenheimer, 1951). In the first two days after hatching, the first instars of P. vitis tend to settle initially on the upper parts of the plant but, subsequently, many move downwards, so that the distribution on the plant canopy becomes more uniform in a week (Phillips, 1963).

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Fig. 1.3.4.1. Diagrammatic illustration of the annual life cycle of Parthenolecanium corni (Bouch6). The species overwinters as second-instar nymphs (A) on woody parts of the hostplant. In the spring, these nymphs move onto branches or twigs where they moult into adult females (B). The females lay the eggs in a brood chamber beneath her abdomen. After hatching, the first-instar nymphs emerge and move onto the new leaves, where they settle (C). At the end of summer, the second-instar nymphs (D) are mostly located on the lower surface of the leaves, stems or underside of the twigs. In the autumn, before leaf-fall, the second-instar nymphs migrate (E) from the leaves to the woody parts of the plant to overwinter.

The migration of later nymphal instars towards the woody parts of the host plant seems to be synchronized to the host plant phenology. The second instars of P. corni and the adult females of C. pseudoceriferus, C. rusci L. and P. vitis migrate from the leaves to branches before leaf-fall, probably in response to a gradual reduction in sap circulation (Kawecki, 1958; Sankaran, 1959; Phillips, 1963; Benassy and Franco, 1974). The movement of C. floridensis preovipositing females, from leaves to the twigs coincides with the annual leaf-drop in citrus (Schneider et al., 1987a). The possible role of ethylene (which increases in concentration prior to leaf dehiscence) upon these scale movements has been partially investigated by Schneider et al. (1987a), who showed that, by artificially increasing the ethylene concentration in the leaf tissue of citrus, they were able to induce a significantly increased movement of C. floridensis. Temperature and relative humidity have also been shown to have important effects on crawler longevity, survival and establishment. Temperature is considered to be the main factor affecting development rate and generation time. For example, Washburn and Frankie (1985) found extensive latitudinal variation in the development state of populations of the iceplant scale, Pulvinariella mesembryanthemi (Vallot). They compared the phenology of populations of this scale inhabiting several field sites in north and south California (USA) and found that the more southerly populations were progressively more advanced than those in the north, so that this soft scale had three generations annually in the south but only two in the north. Washburn and Frankie

Section 1.3.4 references, p. 348

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Eco/ogy

(1985) attributed these differences to the warmer temperatures in the more southern areas.

In the laboratory, the duration of each generation has been found to be significantly affected by temperature. Thus, Washburn and Frankie (1985) found that laboratoryreared P. mesembryanthemi completed each generation in 10 weeks at 24.5~ whereas it took 30 weeks at 14.5~ Similarly, Schneider et al. (1987b), working with C. floridensis, found that it took only 99 days to complete a generation at 26~ but 146 days at 21~ However, some species have the same seasonal history in the field and in the greenhouse. Thus Habib (1955), who studied the life cycle of P. corni on Rubus fruticosus and Prunus persica in England, found that this species developed only a single generation per year under both conditions and that its duration was almost the same. He concluded that the differences in temperature and humidity under greenhouse conditions and those in the field were not sufficiently different to cause a change in the number of generations in England. The importance of seasonal fluctuations in temperature and humidity for the growth, development and generation time of other soft scales is also well documented (Saakyan-Baranova, 1964; Hafez et al., 1971; EI-Minshawy and Moursi, 1976; von KShler, 1978). In some cases, there is a synchronization between the seasonal history and voltinism of the scale and its host. Saakyan-Baranova (1964) studied the relationship between the seasonal history of C. hesperidum and the phenology of its host plant, Pittosporum undulatum. She found that periods of intensive activity by the soft scale, as revealed by mass emergence of progeny in the greenhouse, usually coincided with an active growth period of the host plant, particularly with the appearance of young shoots. Thus, three of the generations coincided with three periods of new shoot growth, while further generations were associated with the flowering and fruit bearing periods of P. undulatum. The quality of the host plant may greatly affect soft scale phenology. Modification of voltinism in uniparental, normally univoltine, soft scale insects can be phenologically induced through changes in the physiology of their host plants (Flanders, 1970). Thus, the Mediterranean black scale, S. oleae, is generally univoltine when developing on olive trees but becomes multivoltine on insectary-grown potato sprouts and on oleander (Flanders, 1942b; Blumberg and Swirski, 1977). The citricola scale, C. pseudomagnoliarum, is usually univoltine when growing on citrus in the field but is multivoltine under greenhouse conditions on potted hackberry (Celtis sp.), when the life cycle can be as short as 8 weeks at 26.5~ and 60% relative humidity (Flanders, 1942a). Another example is the effect of the host plant on P. corni in the Krasnodar region of Russia, where it has one generation on plum, two on peach and three on Robinia pseudoacacia (Borchsenius, 1957). Another important phenomenon is pheno-immunity. This is often ignored or underestimated in scale insect-host plant interactions. Pheno-immunity is a particular and variably induced resistance of the host plant to the attack and development of a particular species of scale insect and can affect reproduction, survivorship, development, voltinism and host-parasite relationships. Thus, host plants can often show varying degrees of susceptibility to a particular species of scale insect. For example, Citrus may be heavily infested by S. oleae in one area but appear to be immune to attack or is only lightly infested in other areas (Compere 1939, 1940). It is not uncommon to find a heavy infestation on only one of two plants of the same species growing side by side. Similarly, a plant may be susceptible to scale infestation one year and apparently immune the next. According to Flanders (1970), some plants appear to be permanently genetically immune, others are always susceptible whilst still others can fluctuate between being immune and susceptible. Plants in the latter category have "pheno-immunity", i.e. they have an environmentally induced physiological resistance to particular scale insects. For

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example, unfavourable conditions such as drought, which can lead to a reduction of the available water in the soil, can result in an increase in the osmotic pressure of plant tissues which become less susceptible to scale insect attack, especially by young instars. Flanders (1970) presented numerous examples in support of his hypothesis that environmental and meteorological changes, edaphic factors and the application of fertilizers could modify the physiology and the phenology of the plant, thus altering or inducing changes in the plant's susceptibility or immunity when attacked by scale insects. He summarizeA the literature on the subject as it related to S. oleae, P. corni and E. tiliae. Some recent work on soft scales supports this hypothesis. Research on the biology of pine tortoise scale, Toumeyella parvicornis (Cockerell), indicates that a mild winter, unseasonably warm spring or mild autumn can accelerate development of soft scale populations and provide an extended growth period, thus increasing the number of generations produced during a growing season (Sheffer and Williams, 1987). Smirnoff and Valero (1975), working with jack pine, Pinus banksiana, found that populations of T. parvicornis increased 2, 7 and 9 times in plots fertilized with 100, 200 and 400 kg of ureic N/ha respectively. On the other hand, scale populations on plants grown in potassium-treated plots were reduced from 42 % to 21%, while in non-fertilized plots, infestations actually increased from 38% to 80%. In addition, Beattie et al. (1990) found that the growth and maturity of Ceroplastes destructor Newstead and C. sinensis were influenced by nitrogen but not by other nutrients. They also noted that scales living on Citrus sinensis planted on Poncirus trifoliata rootstock with high levels of nitrogen were larger and matured earlier than scales on trees with low levels of nitrogen (Beattie et al., 1990). The host plant can also influence the relationship of soft scales with their natural enemies. Studies on the bio-ecology of S. oleae in Corfa (Greece) revealed that wild host plants, such as Carduus pycnocephalus L., Carlina corymbosa L. and Eryngium campestre L., growing near or under olive trees, affected the age distribution of the scale populations and their interaction with two hymenopterous parasitoids, Metaphycus lounsburyi (Howard)and Scutellista caerulea Motschulsky (Viggiani et al., 1975). In olive growing areas where these wild host plants were present, host stages of S. oleae suitable for parasitoid development were available from spring to autumn but, in olive growing areas without or with only a few of these wild host plants, the host stages of S. oleae were only available in the spring and summer and, consequently, the parasitoids overwintered more consistently in areas with abundant weeAs. In addition, field observations in southern California suggest that S. oleae on citrus is only suitable as a host for the endoparasitoid Coccophagus rusti Compere when the scale is growing rapidly on new plant tissue formed over pruning wounds (Flanders, 1952).

DIAPAUSE Voltinism is often limited by interruptions in scale insect activity induced by unfavourable seasonal changes in their environment because physical and biological factors suitable for growth, development and reproduction are present only during particular periods of the year. In order to synchronize these activities with favourable conditions and in order to increase survival during unfavourable periods, soft scales (as with other insects) enter a state of dormancy. Summer and winter diapauses are common forms of dormancy. Although soft scale insects offer a great opportunity to investigate diapause, information on their physiological, biochemical and behavioural features of diapause is rather scanty compared with that for other scale insect groups (see McClure, 1990) and with that for insects in general (see Tauber and Tauber, 1976; Hodek and Hodkova, 1988). However, information on the overwintering

Section 1.3.4 references, p. 348

348

Ecology b i o - m o r p h o l o g i c a l stage for many soft scales is available. Generally, in genera w h e r e the adult females lack waxy coverings or eggsacks and live in the Nearctic and Palearctic regions, i.e. species in the genera Eulecanium, Coccus, Sphaerolecanium, Saissetia, Parthenolecanium, Eucalymnatus, Physokermes and Toumeyella, the o v e r w i n t e r i n g stage is the second-instar nymph. An exception to this phenological rule is Palaeolecanium bituberculatum (Signoret), which overwinters in the egg stage (Goidanich, 1962; Vashchinskaya, 1969). Other soft scales that overwinter in the egg stage are Luzulaspis

luzulae (Dufour) and Parafairmairia gracilis Green. W i n t e r diapause in the adult stage occurs in only a few species o f Pulvinaria Targioni Tozzetti and Rhizopulvinaria Borchsenius (see Kosztarab and K o ~ r , 1988). F u r t h e r studies, similar to those mentioned above, could p r o v i d e the basis for a greater understanding o f the influence o f environmental and biotic factors on d e v e l o p m e n t , generation time and seasonal history o f soft scale populations and w o u l d p r o v i d e useful data for planning control procedures for soft scale species o f e c o n o m i c importance.

REFERENCES Annecke, D.P., 1966. Biological studies on the immature stages of sot~ brown scale, Coccus hesperidum Linnaeus (Homoptera: Coccidae). South African Journal of Agricultural Science, 9: 205-227. Argyriou, L.C., 1963. Studies on the morphology and biology of the black scale, Saissetia oleae (Olivier), in Greece. Annales de l'Institut Phytopatologique Benaki, n.s., 5: 353-377. Argyriou, L.C. and loannides, A.G., 1975. Coccus aegaeus (Homoptera, Coccoidea, Coccidae) De Lotto: nouvelle esp~ce de 16canine des citrus en Grace. Fruits, 30 (3): 161-162. Argyriou, L.C. and Kourmadas, A.L., 1980. Ceroplastesfloridensis Comstock, an important pest of citrus trees in Aegean islands. Fruits, 35 (11): 705-708. Avidov, Z. and Harpaz, I., 1969. Plant Pests of Israel. Israel Universities Press, Jerusalem, 549 pp. Barbagallo, S., 1974. Notizie sulla presenza in Sicilia di una nuova cocciniglia degli agrumi: Coccus pseudomagnoliarum (Kuwana) (Homoptera, Coccidae). Osservazioni biologiche preliminari. Entomologica, 10: 121-139. Beattie, G.A., Weir, R.G., Cliff, A.D. and Jiang, L., 1990. Effect of nutrients on the growth and phenology of Guscardia destructor (Newstead) and Ceroplastessinensis Del Guercio (Hemiptera: Coccidae) infesting citrus. Journal of the Australian Entomological Society, 29: 199-203. Brnassy, C. and Franco, E., 1974. Sur l'rcologie de Ceroplastes rusci L. (Homoptera, Lecanoidae) dans les Alpes-Maritimes. Annales de Zoologie et d'Ecologie Animale, 6(1): 11-39. Ben-Dov, Y., 1976. Phenology of the Florida wax scale, Ceroplastesfloridensis Comstock (Homoptera: Coccidae) on citrus in Israel. Phytoparasitica, 4 (1): 3-7. Ben-Dov, Y., 1980. Observations on scale insects (Homoptera: Coccoidea) of the Middle East. Bulletin of Entomological Research, 70:261-271. Bibolini, C., 1958. Contributo alia conoscenza delle cocciniglie dell'olivo. II. Saissetia oleae Bern. (Homoptera: Cocc.). Frustula Entomologica, 1 (4): 3-95. Blumberg, D. and Swirski, E., 1977. Mass breeding of two species of Saissetia (Horn.: Coccidae) for propagation of their parasitoids. Entomophaga, 22 (2): 147-150. Blumberg, D., Swirski, E. and Greenberg, S., 1975. Evidence for a bivoltine populations of the Mediterranean black scale Saissetia oleae (Olivier) on citrus in Israel. Israel Journal of Entomology, 10: 19-24. Bodenheimer, F.S., 1951. Citrus entomology in the Middle East. W. Junk, The Hague, 663 pp. Borchsenius, N.S., 1957. Sucking insects, Vol. IX. Suborder mealybugs and scale insects (Coccoidea). Family cushion and false scale insects (Coccidae). Fauna USSR, Novaya Seriya 66,493 pp. (In Russian). Compere, H., 1939. The insect enemies of the black scale, Saissetia oleae (Bern.) in South Africa. University of California Publications in Entomology, 7 (5): 75-90 Compere, H., 1940. Parasites of the black scale, Saissetia oleae, in Africa. Hilgardia, 13: 387-425. Crovetti, A., 1962. I1 Ceroplastes sinensis Del Guercio in Sardegna (Segnalazione e brevi note etologiche). Studi Sassaresi, ser. III, 10: 3-8. Ebeling, W., 1959. Subtropical Fruit Pests. University of California, Division of Agricultural Sciences, 436 pp. EI-Minshawy, A.M. and Moursi, K., 1976. Biologicalstudies on some soft scale insects (Hom., Coccidae) attacking guava trees in Egypt. Zeitschrift fiir Angewandte Entomologie, 81: 363-371. Flanders, S.E., 1942a. Biological observations on the citricola scale and its parasites. Journal of Economic Entomology, 35: 830-833.

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Flanders, S.E., 1942b. Propagation of black scale on potato sprouts. Journal of Economic Entomology, 35: 690-698. Flanders, S.E., 1952. Biological observations on parasites of the black scale. Annals of Entomological Society of America, 45: 543-549. Flanders, S.E., 1970. Observations on host plant induced behavior of scale insects and their endoparasites. The Canadian Entomologist, 102 (8): 913-926. Goidanich, A., 1962. Ciclo fenologico abnorme di un genere di Lecaniidae gimnosoma paleartico (Hemiptera Homoptera Coccoidea). Atti della Accademia delle Scienze di Torino, 96: 269-284. Habib, A., 1955. Some biological aspects of the Eulecanium corni Bouch6 group. Bulletin de la Socirt6 Entomologique d'Egypte, 39: 217-249. Habib, A., Salama, H.S. and Amin, A.H., 1971. Population studies on scale insects infesting citrus tree in Egypt. Zeitschrifl tiir Angewandte Entomologie, 69:318-330. Hafez, M., Salama, H.S. and Saleh, M.R., 1971. Survival and development ofLecanium acuminatum Sign. (Coccoidea) on a host plant and artificial diets. Zeitschrifl fiJr Angewandte Entomologie, 69:182-186. Helmy, E.I. and El-Imery, S.M., 1986. Ecological studies on the Florida wax scale Ceroplastesfloridensis Comstock (Homoptera: Coccidae) on citrus in Egypt. Bulletin de la Socirt6 Entomologique d'Egypte, 66: 155-166. Hodek, I. and Hodkova, M., 1988. Multiple role of temperature during insect diapause: a review. Entomologia Experimentalis et Applicata, 49 (1-2): 153-165. Jarraya, A., 1974. Observations biorcologiques sur une cochenille citricole dans la rrgion de Tunis Saissetia oleae (Bernard) 0tomoptera, Coccoidea, Coccidae). Bulletin SROP, 1974/3: 135-158. Kawecki, Z., 1958. Studies on the genus Lecanium Burm. IV. Materials to a monograph of the brown scale Lecanium corni Bouch6 (Homoptera, Coccoidea, Lecaniidae). Annales Zoologici, 4 (9): 135-230. Krhler, G., 1978. On the biology and autoecology of the green scale of coffee, Coccus viridis (Green) (Hemiptera: Coccinea-Coccidae). Zoologische Jahrbficher, Abteilung fiir Systematiek, Jena, 105 (4): 561:572. Komeili Birjandi, A., 1981. Biology and ecology of Parthenolecanium spp. (Hem., Coccidae). Entomologist's Monthly Magazine, 117: 47-58. Kosztarab, M. and Koz~r, F., 1988. Scale Insects of Central Europe. Akadrmiai Kiadb, Budapest, 456 pp. Longo, S. and Benfatto, D., 1982. Note biologiche su Coccus hesperidum L. (Rhynchota, Coccidae) e risultati di prove di lotta. Atti Giornale Fitopatologiche, Sanremo, 137-146. McClure, M.S., 1990. Seasonal history. In: D. Rosen (Editor). Armored Scale Insects, Their Biology, Natural Enemies and Control, Vol. A, Elsevier, Amsterdam, pp. 315-318. Monastero, S., 1962. Le cocciniglie degli agrumi in Sicilia (Mytilococcus beckii New., Parlatoria ziziphus Lucas, Coccus hesperidum L., Pseudococcus adonidum L., Coccus oleae Bern., Ceroplastes rusci L.). II nota. Bollettino Istituto di Entomologia Agraria di Palermo, 4 (28):65-151. Monastero, S. and Zaami, V., 1959. Le cocciniglie degli agrumi in Sicilia (Ceroplastes sinensis Del Guercio, Pseudococcus cirri Risso, Icerya purchasi Maskell). Bollettino Istituto Entomologia Agraria di Palermo, 3:1-82 Nuzzaci, G., 1969. Osservazioni condotte in Puglia sulla Saissetia oleae Bern. (Homoptera-Coccidae) e i suoi simbionti. Entomologica, 5: 127-138. Onciier, C. and Tuncyrureck, M., 1975. Observations sur la biologic et les ennemis naturels de Coccus pseudomagnoliarum Kuw. dans les vergers d'agrumes de la rrgion 6grenne. Fruits, 30: 255-257. Panis, A., 1977a. Bioecologia de la cochinilla comun de los agrios en la region Mediterranea (Homoptera, Coccoidea, Coccidae). Boletin Servicio de Defensa Contra Plagas y Ispeccion Fitopatologica, 3" 157-160. Panis, A., 1977b. Contribucion al conocimiento de la biologia de la cochinilla nigra de los agrios (Saissetia oleae Oliv.). Boletin Servicio de Defensa Contra Plagas y Ispeccion Fitopatologica, 3:199-207. Pechhacker, H., 1971. Uber die Ausbreitung der Larven der Physokermesarten, speziell von Physokermes hemicryphus Dalm. (Kleine Fichtenquirlschildlaus oder kleine Lecanie). Apidologie, 2 (4): 289-301. Peleg, B.A., 1965. Observations on the life cycle of the black scale, Saissetia oleae Bern., on citrus and olive trees in Israel. Israel Journal of Agricultural Research, 15: 21-26. Phillips, J.H.H., 1963. Life history and ecology of Pulvinaria vitis (L.) (Hemiptera: Coccoidea), the cottony scale attacking peach in Ontario. The Canadian Entomologist, 95: 372-407. Podoler, H., Bar-Zacay, I. and Rosen, D., 1979. Population dynamics of the Mediterranean black scale, Saissetia oleae (Olivier), on citrus in Israel. 1. A partial life-table. Journal of Entomological Society of South Africa, 42 (2): 257-266. Podoler, H., Dreishpoun, Y. and Rosen, D., 1981. Population dynamics of the Florida wax scale Ceroplastes floridensis (Homoptera: Coccidae) on citrus in Israel. 1. A partial life-table. Acta Oecologica, Oecologia Applicata, 2 (1): 81-91. Rosen, D., Harpaz, I. and Samish, M., 1971. Two species of Saissetia (Homoptera: Coccidae) injurious to olive in Israel and their natural enemies. Israel Journal of Entomology, 6: 35-53. Saakyan-Baranova, A.A., 1964. On the biology of the soft scale Coccus hesperidum L. (Homoptera, Coccoidea). Entomological Review, 43" 135-147. Salem, S.A. and Hamdy, M.K., 1985. On the population dynamics of Ceroplastesfloridensis Comstock on guava trees in Egypt. Bulletin de la Socirt6 Entomologique d'Egypte, 65: 227-237.

350

Ecology Sankaran, T., 1959. The life history and biology of the wax scale Ceroplastes pseudoceriferus Green (Coccidae: Homoptera). Journal of the Bombay Natural History Society, 56: 39-59. Schneider, B., Podoler, H. and Rosen, D., 1987a. Population dynamics of the Florida wax scale, Ceroplastes floridensis (Homoptera: Coccidae), on citrus in Israel. 2. Spatial distribution. Acta Oecologica, Oocologia Applicata, 8 (1): 67-78. Schneider, B., Podoler, H. and Rosen, D., 1987b. Population dynamics of the Florida wax scale, Ceroplastes floridensis (Homoptera: Coccidae) on citrus in Israel. 3. Developmental rate and progression of mean age. Acta Oecologica, Oecologia Applicata, 8 (2): 95-103. ShelTer, B.J. and Williams, M.L., 1987. Factors influencing scale insect populations in southern pine monocultures. Florida Entomologist, 70 (1): 65-70. Silvestri, F., 1939. Compendio di Entomologia Applicata. Tipografia Bellavista, Portici, Vol. 1 (2), 527 pp. Smirnoff, W.A. and Valero, J., 1975. Effects au moyen de la fertilisation par urre ou par potassium sur P/nus banksiana L. et le comportement de ses insectes d6vastateurs: tel que Neodiprion swainei et Toumeyella numismaticum. Canadian Journal of Forest Research, 5: 236-244. Snowball, G.J., 1970. Ceroplastes sinensis Del Guercio (Homoptera: Coccidae), a wax scale new to Australia. Journal of the Australian Entomological Society, 9: 57-64. Tauber, M.J. and Tauber, C.A., 1976. Insect seasonality: diapause maintenance, termination, and postdiapause development. Annual Review of Entomology, 21" 81-107. Tuncyurek, M., 1975. Observations sur la bio-6cologie de Saissetia oleae Bern. dans les vergers de la r6gion ~g6enne. Fruits, 30 (3): 163-165. Vashchinskaya, N.V., 1969. On the biology of the soft scale Palaeolecanium bituberculatum (Targ.) (Homoptera, Coccoidea) from Armenia. Entomological Review, 48: 472-476. Viggiani, G., Fimiani, P. and Bianco, M., 1973. Ricerca di un metodo di lotta integrata per il controllo della Saissetia oleae (Oliv.). Atti Giornate Fitopatologiche, Bologna: 251-259. Viggiani, G., Pappas, S. and Tzoras, A., 1975. Osservazioni su Saissetia oleae (Oliv.) e i suoi entomofagi nell'isola di Corl~. Bollettino del Laboratorio di Entomologia Agraria, 'Filippo Silvestri', 32: 156-167. Washburn, J.O. and Frankie, G.W., 1985. Biological studies of iceplant scales, PulvinarieUa mesembryanthemi and Pulvinaria delonoi (Homoptera: Coccidae), in California. Hilgardia, 53(2): 1-27. Williams, M.L. and Kosztarab, M., 1972. Morphology and systematics of the Coccidae of Virginia with notes on their biology (Homoptera: Coccoidea). Virginia Polytechnic Institute and State University, Research Division Bullettin, 74:1-215.

Soft Scale Insects - Their Biology, Natural Enemies and Control

Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.

1.3.5

351

Relationships with Ants

PENNY J. GULLAN

INTRODUCTION Ant attendance of homopterans, especially aphids, coccoids and leafhoppers, is a well known phenomenon (e.g., Flanders, 1951; Nixon, 1951; Strickland, 1950; Way, 1954a, 1963; Buckley, 1987a,b; Fig. 1.3.5.1) to the extent that the presence of ants is often a useful means of locating relatively inconspicuous homopterans. Honeydew, the sugary

Fig. 1.3.5.1. Wax-covered coccids of Austrolichtensia hakearum (FulleO on Hakea sp. attended by ants of Camponotus sp. in south-west Western Australia. The anal area of the coccids is at the wide end of the dark stripe visible on each coccid.

excreta produced by many homopterans, provides ants of numerous species with a stable source of energy (Way and Khoo, 1992). Ants of three of the 11 extant subfamilies, namely the Dolichoderinae, Formicinae and Myrmicinae, commonly attend homopterans

Section 1.3.5 references, p. 371

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Ecology

to some extent (Wheeler, 1910; Nixon, 1951; Evans and Leston 1971; Samways et al., 1982; H611dobler and Wilson, 1990) and these three ant subfamilies are species-rich (Hblldobler and Wilson, 1990). Much of the literature on ant-homopteran interactions documents the associations of ants with aphids (reviewed by Sudd, 1987), mealybugs or homopterans in general (e.g., Nixon, 1951; Way, 1963; Buckley, 1987a,b). The discussion that follows is restricted to information on the interactions of ants with coccids or soft scale insects (family Coccidae) and emphasises two types of studies - those that deal with ant-coccid relationships with a view to control populations of the latter on economically important plants such as citrus or coffee, and those seeking to answer evolutionary and ecological questions concerning the intimate associations that exist between certain tropical and subtropical ants, coccids and plants. Although most ants are predatory or scavenge on animal matter (Carroll and Janzen, 1973), and coccids may form part of their diet, this review emphasises those relationships between ants and coccids that involve reciprocal benefits. Most associations are facultative for both partners but some associations are apparently obligate (Tho, 1978; Ward, 1991) and many ants that tend coccids to obtain honeydew also may prey on coccids, either regularly or only under particular circumstances (see section on Benefits of Coccids to Ants). The coccids may be referred to as trophobionts (a term deriving from the work of Wasmann; see Wheeler, 1910; H611dobler and Wilson, 1990) in that they supply honeydew for ants which, in turn, provide protection from natural enemies or sanitary benefits or both (see section on Benefits of Ants to Coccids). The most important of the world's pest ants, such as Linepithema humile (Mayr) (the Argentine ant), Pheidole megacephala (Fabricius) and Solenopsis species (fire ants) (Fig. 1.3.5.2), attend coccids and other homopterans (Compere, 1940; Nixon, 1951; Samways et al., 1982), often enhancing the pest status of both the ants and

Fig. 1.3.5.2. A coffee branch with an aggregation of Coccus celatus De Lotto attended by the fire ant Solenopsis geminata (Fabricius) in Papua New Guinea, near Madang.

the attended coccids. Ants, whether regarded as pest species or not, frequently affect plant health and reproductive output indirectly via the coccids that they tend and defend. The soft scales remove plant sap, may damage plant tissues or inject toxins (Nixon, 1951; Steyn, 1954; Briese, 1982; see also Section 1.3.1), and generally contaminate fruit and foliage with honeydew that becomes blackened with sooty moulds which may impair photosynthesis and sometimes lead to leaf abscission (Fig. 1.3.5.3; see Sections 1.2.2.2 and 1.3.1). The ants may increase the magnitude of such debilitation by improving the survival and hence reproductive capacity of the coccids (see section on Benefits of Ants

Relationships with ants

353

to Coccids). Furthermore, the ants may incidentally increase populations of non-tended armoured scale insects (Diaspididae) due to protection afforded to nearby soft scales (Flanders, 1945; Steyn, 1954). Most honeydew-seeking ants will visit several or all species of Coccidae, and often all suitable homopterans, present in an area (Samways et al., 1982; Adenuga and Adeboyeku, 1987), but some ant species are more specific in their attendance (Way, 1963; Leston, 1973). For example, the coccid Saissetia zanzibarensis Williams is intimately associated with the African weaver ant Oecophylla longinoda (Latreille) and not other ant species that occur in eastern Africa (Way, 1954b). Similarly, in tea plantations in north-east India, three coccid species, including Coccus hesperidum L., are attended by the green tree ant Oecophylla smaragdina (Fabricius), whereas a fourth coccid species is associated almost exclusively with Crematogaster dohrni Mayr and never with O. smaragdina (Das, 1959). The degree of coccid-ant specificity may depend on the habits and habitat requirements of both partners and on the duration of association of the taxa. The production of honeydew by coccids corresponds to the ingestion of phloem sap which, after at least partial digestion during passage through the gut, is eliminated via the everted anus and either actively ejected or imbibed by ants. The presence of ants changes the elimination behaviour so that the honeydew droplet is held stationary between the splayed anal ring setae rather than propelled away from the coccid's body by sudden withdrawal of the anus and bunching of the setae (Bedford, 1968; Williams and Williams, 1980). The frequency of discharge of honeydew droplets may be increased (Andrews, 1930) or decreased (Smith, 1942) in the presence of ants, but it is not known whether frequency and droplet size are related. Ants induce scale insects to eliminate honeydew by palpitating or caressing them with their antennae (Smith, 1942; Evans and Leston, 1971; Bums, 1973; Williams and Williams, 1980; Collins and Scott, 1982), a behaviour referred to as solicitation (Wheeler, 1910; H611dobler and Wilson, 1990). In the absence of ants, many soft scales actively expel honeydew droplets away from their body, for example to a distance of 6-12 mm for the third-instar nymphs of Ceroplastes sinoiae Hall (Bedford, 1968) and to about 5 mm for Pulvinariella mesembryanthemi (Vallot) (Collins and Scott, 1982). In some coccids, such as S. zanzibarensis, the mechanism for ejection of the honeydew droplet is inefficient and rapid body contamination occurs when ants are excluded (Way, 1954b, 1963). For some coccids, however, it is possible that the quantity of honeydew produced may be less in the absence of ants than in their presence (Bradley, 1973), as has been demonstrated for ant-tended aphids (reviewed by Way, 1963).

BENEFITS OF ANTS TO COCCIDS The presence of tending ants may be beneficial to coccids in one or more ways (Fig. 1.3.5.3). Removal of honeydew improves the sanitation of scale insect aggregations by reducing physical fouling caused by both the sugary excreta and the sooty moulds which grow on it (Flanders, 1951; Way, 1954b; Das, 1959; see also Section 1.2.2.2). If ants are excluded, coccids may become engulfed in their own honeydew and die (Flanders, 1951; Way, 1954b; Bess, 1958; Das, 1959). It is unclear whether death results from asphyxiation or from some effect of the fungal growth which usually follows honeydew contamination. There is unequivocal evidence that ants can protect scale insects from their natural enemies, especially parasitic wasps (Bartlett, 1961; Buckley and Gullan, 1991; Bach, 1991; Fig. 1.3.5.4A) and predatory beetles (Das, 1959; Bartlett, 1961; Bums, 1973; Bradley, 1973; Hanks and Sadof, 1990; Bach, 1991). Ants interfere with

Section 1.3.5 references, p. 371

354

Ecology

the activities of coccid natural enemies either by direct attack (including consumption of adults, larvae or eggs) or incidental disturbance, both of which may prevent oviposition or feeding by parasitoids and predators. The likelihood of ant reaction to natural enemies may vary depending on the distance of the coccids from the ant nest and the abundance of the coccids or availability of other food for the ants (Way, 1963). Furthermore, the degree of protection afforded to coccids can vary depending on

Fig. 1.3.5.3. Summary diagram of possible interactions present in coccid-ant-plant associations. Direct positive (+) and negative (-) influences are shown. Not all of these effects may operate in any given coccid-ant-plant association and the overall effect of the interactions on each participant will depend on the relative magnitude of each individual effect. FN = floral nectary; EFN = extrafloral nectary.

the innate behavioural characteristics of the associated ant species (see section on Coccid Protection and Ant Aggression). Some predators may gain immunity from ant attention by chemical protection or camouflage and slow movements (Nixon, 1951; Das, 1959; Bartlett, 1961; Bums, 1973). Two other factors may explain the differing levels of susceptibility to ant interference found among various species of parasitic wasps. Ant-induced disturbance may be greater if wasp oviposition time is long (a minute or more rather than a few seconds) and/or if the wasps' inherent sensitivity to nearby moving objects is high (Bartlett, 1961). Another idea which has not been tested is that ants may remove dead scale insects from aggregations, perhaps reducing the spread of parasitoids into the remainder (Buckley, 1987a). Certain ant species are known to transport coccids to new feeding sites on the same plants or to uninfested plants, thus greatly facilitating the spread of soft scale populations (Way, 1963; H611dobler and Wilson, 1990; Maschwitz et al., 1991b). Records ofcoccid transport by ants include: Coccus hesperidum by O. smaragdina (Das, 1959),

355

Relationships with ants

Coccus viridis (Green) by Crematogaster brevispinosa Mayr and Solenopsis geminata (Fabricius) (Edwards, 1935, cited by Nixon, 1951), Coccus formicarii (Green) by Crematogaster species (Das, 1959) and S. zanzibarensis by O. longinoda (Way, 1954b). In contrast, experiments by Steyn (1954) produced no evidence that ants of Anoplolepis custodiens (F. Smith) transported C. hesperidum and observations by Smith (1942) indicated no transport of Saissetia coffeae (Walker) by S. geminata or by Brachymyrmex heeri Forel.

A

6 II

.)

4

o $

3

Ants present

it

l~J Ants removed

J~

E :3 z

2

0

i

I

0

8

15

29

7

41 --.-

6 5

m

4

~ a Z

2 1

0

0

8

15

29

41

Days after commencement of experiment

Fig. 1.3.5.4. Number of s c a l e s of Coccus viridis (Green) per leaf of Pluchea indica (L.) Less., with and without ants of Pheidole megacephala (Fabricius), that were: (A) parasitised and (B) dead from other c a u s e s . Bars represent the mean plus one standard error for per-plant values (with six plants per treatment). Modified from Bach (1991).

Ants frequently build protective covers or nests over coccid aggregations on plants (Wheeler, 1910; Nixon, 1951; Strickland, 1950; Way, 1954b; Clarke et al., 1989) and nest sites and shelters may be altered or selected to accommodate the coccids (Das, 1959; Way, 1963; Benzie, 1985) but there seem to be no records of coccids being taken into underground ant nests to overwinter in temperate or colder regions. Shelters may benefit the coccids by providing protection from the weather (Briese, 1982; but see Way, 1954b), excluding predators and parasitoids (Nixon, 1951; Das, 1959; Way, 1963;

Section 1.3.5 references, p. 371

Ecology

356

Sugonyayev, 1995) and reducing the incidence of disease. Coccids may be less susceptible to fungal attack within rather than outside ant nests due to the antibiotic action of the metapleural gland secretions produced by most ants and apparently disseminated diffusely through their nests to kill fungi and other micro-organisms (Hblldobler and Engel-Siegel, 1984; Beattie, 1985). However, there is indication that some ants, such as Anoplolepis longipes (Jerdon) and O. smaragdina, may disseminate the spores of entomopathogenic fungi which kill coccids (Nixon, 1951; Das, 1959; Haines and Haines, 1978). Some observations suggest that entomopathogenic fungi of tropical coccids flourish in shady, humid conditions and in certain places may be the principal factors regulating coffee scales, especially S. coffeae (Smith, 1942). Smith found that scales were less abundant in shady locations in coffee plantations than in sunny ones and were most abundant in dry weather. It is noteworthy that the tropical, arboreal weaver ants Oecophylla longinoda and O. smaragdina, which commonly build silk shelters over scale insects on exposed foliage in open habitats (e.g., Way, 1954a; Buckley and Gullan, 1991), lack metapleural glands (H611dobler and Engel-Siegel, 1984). In contrast, ants that live with coccids in very humid tropical microhabitats, such as nest chambers inside live plants (see section on Coccids, Ants and Ant-plants), would be expected to have especially well developed metapleural glands or very effective antibiotics. Anatomical and/or pharmacological studies of the metapleural glands of most of the specialist plant-ants have yet to be done. Ant attendance may enhance coccid survival and reproductive success in one or more of the ways outlined above. In practice, it is difficult to determine experimentally which of the many possible benefits of attendance by a particular ant species is most important for the survival of a given coccid species at a particular place and time on a given host plant, and certainly it is very difficult to make generalisations about the benefits to Coccidae of relationships with ants. Given this reservation, the following section will attempt to summarise the experimental data derived from studies in which attendant ants have been deliberately excluded from coccid populations.

THE EFFECT OF ANT EXCLUSION ON COCCIDS Most experimental studies of the effects of ant exclusion on soft scales have concentrated on coccids of one pest species attended by ants of a single species (Table 1.3.5.1). In both agricultural and horticultural systems, the majority of ant exclusion studies have reported increased parasitisation and/or predation as the main factors controlling coccid populations in the absence of ants (Table 1.3.5.1), although a number of studies (Flanders, 1945; Way, 1954b; Bess, 1958; Das, 1959; Collins and Scott, 1982; Jutsum et al., 1981; Bach, 1991) have found that honeydew and sooty mould contamination and/or fungal disease have a deleterious effect on the coccids. Sometimes the latter factors have been claimed to account for most coccid mortality in the absence of ants (Miller, 1931; Bess, 1958). However, it is unclear whether honeydew contamination per se is a major cause of coccid mortality. Laboratory experiments (in the absence of natural enemies) with C. hesperidum reared on melons failed to f'md evidence that honeydew removal, by either Argentine ants or mechanical means, increased coccid growth rate or survival compared to contaminated, ant-excluded cultures (Bartlett, 1961). This finding is contrary to that of Way (1954b, fig. 3) who maintained populations of S. zanzibarensis on caged clove seedlings (to exclude natural

;?TABLE 1.3 5 . 1 The relationships of Coccidae with ants: the results of ant exclusion studies

Coccid species

Ant species

Plant species

country (habitat)

Effects on cocci& of ant exclusion

References

Coccus viridis (Green)

Azfeca sp.

orange

Increased predation, honeydew contamination & fungal disease; virtual elimination in 1 month

Jutsum et al., 1981

records may be misidentifications of C . celaius De Lotto (see Williams 1982)

Trinidad, West Indies (orchard)

mostly Cremafogaster sp .

coffee

Venezuela (plantation)

Increased predation (ants chased coccinellid adults)

Hanks and Sadof, 1990

Oecophylla smaragdina (Fabricius) Technomyma albipes (F. Smith)

coffee

Sri Lanka (experimental plot 1 tree)

Increased mortality due to honeydew and sooty mould contamination, not predators & parasitoids

Bess, 1958

Pheidole megacephala (Fabricius)

Pluchea indica (L.)Less. (introd. weed)

Hawaii (in field)

Increased parasitisation, predation, honeydew contamination & sooty mould

Bach, 1991

(NB. some

Coccus fomicarii (Green)

orange

Anoplokpis longipes (Jerdon) (formerly Plagiokpis longipes)

coffee

Java

Increased parasitisation, decreased excretion and developmental rate

Van der Goot, 1916

Dolichodem rhoracicus (F. Smith) (= D . biiuberculaius

cacao?

Java

Little effect

Van der Goot, 1916

NE India

Disappeared within 3 months after ant removal (never outside ant nests)

Das, 1959

Cremarogasier dohrni Mayr and Crcmaiogasier sp .

tea bushes

(plantations)

TABLE 1.3.5.1 (continued)

Coccid species

Ant species

Han! SDeCles

Coccus hesperidum L.

Country habitat)

Effects on cocci& of ant exclusion

References

Anoplolepis custodiens (F. Smith)

orange

South Africa (orchards)

Virtual elimination due to increased predation and parasitisation

Steyn, 1954

Linepirhema humile (Mayr) (formerly Iridomynncx humilis)

citron melon (Cirrullus sp .)

USA California (laboratory study)

No effect on rate of development and survival

Bartlett, 1961

L. hurnile

citrus

USA California (laboratory & field

Increased parasitisation and predation

Badett, 1961

L . humile

orange

USA California (street trees)

Increased parasitisation or honeydew suffocation

Flanders, 1945

Oecophylla smaragdina

tea and shade trees

N E India (plantations)

Increased predation by coccinellids, honeydew suffocation and sooty mould, slightly increased parasitisation

Das, 1959

Ceroplasres rusci (L.)

with many ant spp., esp. Ckmarogasrer spp.

Ochna pulchra Hook

South Africa (savanna woodland trees)

Significantly fewer coccids but reasons not determined

Grant and Moran, 1986

Milviscuhtlus rnangiferae (Green)

0 .smaragdina

Eucalyprus deglupra Blume

Papua New Guinea (garden)

Increased parasitisation

Buckley and Gullan, 1991

0 .smaragdina

Psidium auaiava L.

Papua New Guinea harden)

Increased parasitisation and Dredation

Buckley and Gullan, 1991

Parasaisseria nigra (Nietner)

with many ant spp., esp. Cremarogasrer spp.

Tenninalia sericea Burch.

South Africa (savanna woodland trees)

Significantly fewer coccids but reasons not determined

Grant and Moran, 1986

Pulvinariella mesembryanthemi (vallot)

Cremarogasrer sp. and Iridomynnex sp.

Carpubrotus edulis (L.) L. Bolus

Australia (in field)

Increased sooty mould bredator removal had little effect; parasitoids not controlled for)

Collins and Scott, 1982

TABLE 1.3 5 . 1 (continued) Coccid species

Ant species

Plant species

country (habitat)

Effects on cocci& of ant exclusion

References

Saissetia mironda

Tapinoma sp.

Eryrhrina sp.

Papua New Guinea (garden)

Increased parasitisation

Buckley and Gullan, 1991

Saissetia oleae

L. humile

citrus

USA California (laboratory & field)

& predation

Increased parasitisation

Bartlett, 1961

Saissetia zanzibarensis

Oecophylla longinoda

clove tree

Williams

(Latreille)

Zanzibar (field & shade-house)

Increased parasitisation, predation, honeydew & sooty mould contamination

Way, 1954b

(Jambosa caryophyllus)

Tourneyella liriodendri

Crematogaster lineolara (Say)

tuliptree

USA

Reduced survival from 28% to 856, but only a small number of scales normally attended

Bums, 1973

Reduced survival from 47% to 8% by increasing predation, especially by adult coccinellids

Bums, 1973

Cockerell & Parrott

(Olivier)

(Gmelin)

(Liriodendturn tulipiJcra L.)

(regeneration in abandoned pastures)

tuliptree

USA

Formica exsectoides Forel

tuliptree

USA

Formica obscuripes Forel

jack pine

Dolichodem taschenbergi (Mayr)

Tourneyella panicomis

(Cockerell)

Tourneyella sp .

(as previous)

Reduced survival from 5 8 % to 8 % ; F. exsecroides had greater effect on predators than D. raschcnbergi

Bums, 1973

Canada (forest)

Increased predation, esp. by adult coccinellids, but possible pest resurgence if remove all ant nests since predators too efficient

Bradley, 1973

Trinidad, West Indies (orchard)

Collapse of their caflon shelters; increased predation and virtual elimination in one month

Jutsum et al., 1981

(as previous)

(Pinus bankF iana

Lamb.) Azteca sp.

orange

360

Ecology

enemies of the scales) with or without weaver ants (O. longinoda). Scales and plants in half of the cages without ants were washed twice a day to reduce honeydew levels. The total numbers of coccids increased dramatically in the presence of ants, increased to a lesser extent in the cages where the plants were washed, but declined to a low, relatively constant number in the unwashed, ant-excluded treatment. Way (1954b) found that extensive sooty mould growth occurred on the unwashed, ant-excluded plants, whereas it was slight or absent in the other two treatments. In contrast, in Bartlett's (1961) laboratory study, no fungi developed upon honeydew of C. hesperidum. Thus, the opposite conclusions reached by Bartlett (1961)and Way (1954b) might result from differences in fungal contamination, in levels of crowding or in tolerances to honeydew contamination in the two species of coccids. Possible deleterious effects of sooty moulds and entomopathogenic fungi are probably aggravated by warm humid conditions that occur in the tropics (as discussed in the preceding section), where Way's study was carried out. Thus, the relative effects on coccid populations of natural enemies versus honeydew and fungal contamination may depend on temperature and humidity. In natural systems, it is almost impossible to ascertain the exact factors responsible for death of all coccids after ant attendance is prevented. For example, in the populations of Coccus viridis studied by Bach (1991), some individuals died (as evidenced by their brown colouration) for unknown reasons and these dead scales were more numerous on

Fig. 1.3.5.5. The effects of removing ants ofAzteca sp. on populations of two coccid species, where 9 9 Azteca sp. killed with toxic bait; o---o living Azteca sp. control; 10 trees in each treatment. (A) Mean Azteca sp. activity score: 0, ants absent; 1, 5 ants ml trunk; 3, ants abundant; 4, ants swarming everywhere; (B) number of trees with living Azteca sp. nests; (C) number of trees with Coccus viridis where the majority on marked leaves were dead; (D) number of trees with Toumeyella sp. where the majority on marked branches were dead. Modified from Jutsum et al. (1981).

Relationships with ants

361

ant-excluded plants (Fig. 1.3.5.4B). Egg parasitoids and some pathogens of coccids may be difficult to detect and certain predators, such as spiders, may be elusive due to nocturnal habits. However, in laboratory experiments designed to test the effect of single factors, for example, honeydew contamination or coccinellid predators, the results may have little reality for field conditions. In the field, the effects of different factors will be subject to climatic limitations and may not be additive; for example, predators may interfere with parasitic wasps. Regardless of the causes of coccid mortality in the absence of ants, their population decline is typically dramatic, often resulting in virtual elimination (Table 1.3.5.1; Fig. 1.3.5.5). About a third of all ant exclusion studies have involved the green scale, C. viridis, although some experiments on C. viridis actually may have been carried out on or included specimens of C. celatus De Lotto, which is readily confused with C. viridis in the field (Williams, 1982). Nevertheless, the effects of ant attendance on populations of these two Coccus species are likely to be similar. Indeed, the ant removal study of Jutsum et al. (1981) showed similar effects on C. viridis and on an unrelated ToumeyeUa species on citrus trees (Fig. 1.3.5.5). Only one study of ant exclusion involving soft scales has been carried out in a natural ecosystem, undisturbed by human activity. This research (Grant and Moran, 1986) assessed the effects of foraging ants on arboreal insect herbivores in woodland savanna in South Africa. Two soft scale species were identified among the herbivores and ant exclusion significantly reduced populations of these coccids (Table 1.3.5.1), although the causative factors were not ascertained. Coccid populations in native vegetation may be regulated by a diverse community of ants, parasitoids and predators. A better understanding of why soft scales are not pests in natural habitats may aid the management of pest coccids in agricultural and horticultural systems.

COCCID PROTECTION AND ANT AGGRESSION Not all ants are equally effective in protecting coccids from their natural enemies. Soft scale outbreaks may be precipitated by certain species, such as the pest ants Linepithema humile, Anoplolepis custodiens and A. longipes (Compere, 1940; Steyn, 1954; Haines and Haines, 1978; Samways et al., 1982). Only a few studies, however, have compared directly the protection afforded to soft scales by different species of ants. Burns (1973) estimated the survival of ant-attended and untended tuliptree scales (Toumeyella liriodendri (Gmelin)) on tuliptree (Table 1.3.5.1). He found that the ants increased the survival of the coccids and that the three ant species could be ranked from most to least effective as follows: Formica exsectoides Forel, Dolichoderus taschenbergi (Mayr) and Crematogaster lineolata (Say). Formica exsectoides was much larger and more aggressive than D. taschenbergi and had a greater disruptive effect on predators, whereas C. lineolata was the smallest of the three species and protected its scales by building a shelter over them. Similarly, Buckley and Gullan (1991), who studied coccoid-ant associations on cultivated plants in Papua New Guinea, found that soft scales attended by relatively inoffensive ants (Papyrius nitidus (Mayr) and Tapinoma sp.) were significantly more heavily parasitised than those attended by more aggressive ants (0. smaragdina and Solenopsis geminata) (Table 1.3.5.2). A third study, which reported substantial differences among ant species in their capacity to promote populations of Coccidae and other homopterans was a survey by Samways et al. (1982) of ants foraging on citrus trees in South Africa. They recorded 25 ant species attending honeydew-producing homopterans or collecting droplets of fallen honeydew. Of these, only two species, A. custodiens and Pheidole megacephala, were serious widespread pests, precipitating outbreaks of soft scales, mealybugs and, indirectly, California red

Section 1.3.5 references, p. 371

362

Ecology

scale (Aonidiella aurantii (Maskell)), although at some localities Pheidole sculpturata Mayr rivalled P. megacephala in causing soft scale and California red scale outbreaks. A. custodiens and P. megacephala apparently ran erratically over the fruit and perhaps this behaviour greatly disturbed natural enemies of the scale insects. Samways et al. (1982) emphasised that most tree-foraging ants were relatively harmless or caused only localised outbreaks of scale insects, or could even be beneficial predators feeding on citrus pests. A fourth study by Van der Goot (1916) compared populations of C. viridis attended by either A. longipes or Dolichoderus thoracicus (F. Smith) and found that the scales flourished in the presence of A. longipes with an average of 1,057 scales per bush, compared to 403 on bushes with D. thoracicus and 70 on ant-free bushes. This difference in numbers of coccids attended by the two ant species was attributed to differences in their behaviour, such as the faster movement of A. longipes over the scales. The above differences in ant ability to foster coccid infestations presumably relate both to ant diet and to differences in behaviour, including aggressiveness (Nixon, 1951; Strickland, 1950), which have led to the recognition of "dominance', a complex concept

TABLE 1.3.5.2 Parasitisation in ant-tended Coccidae in Papua New Guinea, near Madang" species associations, incidence of parasitisation of the coccids and ant aggressiveness rank. Data extracted from Buckley and Gullan (1991). Coccid species

Host plant

Parasitisation of coccids No. individ. Mean % examined parasit.

Saissetia miranda

Erythrina sp.

>400

> 70

Ant Aggressiveness rank (1 = least 4 = most)

1

Attendant ant species

Tapinoma sp.

~ho~rhm)

(Cockerell & Parrott)

Coccus longulus

Gliricidia sepium

(Douglas)

(Jacq.) Walp.

20

20

2

Papyrius nitidus (Mayo

~hodemm) Drepanococcus chiton (Green)

G. sepium

30

Oecophylla smaragdina

20

(Fabricius) (Formicinae)

Thespesia populnea

20

0

44