World Crop Pests, 7A
SOFT SCALE INSECTS T H E I R BIOLOGY, NATURAL ENEMIES AND C O N T R O L
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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
This Page Intentionally Left Blank
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
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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
This Page Intentionally Left Blank
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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Fig. 1.1.2.1.5. E u ' e n n e a v i l l i e r s i Matile-Ferrero, adult female, Senegal, on A p h a n i a senegaler~is. A Dorsum and venter. B-J: ventral structures. B - Quinquelocular disc-pores, normal and aberrant types. C - Area of stigmatic furrow and marginal setae (note absence of differentiated stigmatic setae). D - Tubular duct. E - Minute duct. F - Body seta. G - Seta of the submarginal row. J - Multilocular disc-pore. K - R : dorsal structures. K - Preopercular pore. L - Anal plates. M - Dorsal microduct. N - Marginal ~ t a . O Body seta. P - Cone-like tubular duct. Q - Glandular tubercle with satellite tubular ducts. R - Pocket-like tubercle. (From Matile-Ferrero, 1984).
External morphologyof the adultfemale
13
Setae The ventral surface is covered with scattered setae, randomly distributed, except for the characteristic interantennal setae, submarginal setae and prevulvar setae, which are often similar throughout the family. The interantennal setae are slender, usually long, varying on most species from one to six pairs, although Poaspis jahandiezi (Balachowsky) has about 20 pairs. The submarginal setae, if present, are in a more or less regular row around the body. They are usually short and slender and about the same shape on all species. Usually one pair of large prevulvar setae lie on each abdominal segment V, VI and VII. On species belonging to such genera as Ceroplastes and Kilifia, a pair of prevulvar setae is present on segment VII only, while prevulvar setae are entirely absent on species of Pseudopulvinaria and Vinsonia. Microspines, spinules or spicules occur on most of the Coccidae. These are minute transverse tooth-like projections of the derm, common on insects (Snodgrass, 1935). They are concentrated on the mid-region of the abdomen and thorax and on the anal cleft area.
Pores The ventral surface of the Coccidae bears large locular disc-pores and minute simple pores. The two main types of disc-pores are the quinquelocular disc-pores and the multilocular disc-pores, which are present on the whole family (Fig. 1.1.2.1.4,D, H). The quinquelocular disc-pores (with a few aberrant quadrilocular, trilocular or bilocular pores as in Fig. 1.1.2.1.5,B) are present in all instars and are associated with the spiracles. They are usually restricted to the stigmatic furrow in a more or less narrow band from the spiracles to the margin and to the stigmatic setae, when the latter are present. On Toumeyella cerifera Ferris, the stigmatic furrows are lined with quinquelocular pores, mixed with multilocular disc-pores, either similar to or different from the abdominal multilocular disc-pores (Williams & Kosztarab, 1972). Rarely, quinquelocular disc-pores may be present along the submargins, as on Psilococcus and on Pseudopulvinaria sikkimensis Atkinson (Hodgson, 1991b). Multilocular disc-pores are present only on the adult female and each usually possesses 10 loculi but on some species the loeuli are fewer. They occur at least around the vulva and often also in transverse rows on preceding abdominal segments. They are sometimes present on the mid-region of the thorax, on the head, between the antennae and also lateral to the coxae, as on Chloropulvinaria psidii (Maskell). Rarely, multilocular disc-pores may be present conspicuously along the submargins, as on Melanesicoccus myrmecariae Williams & Watson. Their presence or absence and their distribution are of taxonomic importance. In some genera, the multilocular disc-pores are replaced by quinquelocular disc-pores around the vulva, such as on Pseudophilippia quaintancii Cockerell and on several species of Toumeyella, and they may also be present on other abdominal segments, as on Messinea conica De Lotto. Minute simple pores, with round or oval orifices, are occasionally present, particularly near the margin. Frontal tubercles are minute raised spots located antero-medially to each antennal base. They have been observed on many species of Coccidae and are probably homologous to similar structures in the family Eriococcidae.
Ducts Tubular ducts and microducts occur on the ventral surface of many species, while several species are devoid of both of these ducts. A tubular duct is composed of a simple sessile orifice, from which a duct (the outer ductule) extends inwards; the inner
Section 1.1.2.1 references, p. 20
14
Morphology end of the duct is cup-shaped with an inner ductule arising from the rim of the cup (Figs 1.1.2.1.3,F ; 1.1.2.1.9,E). The shape and arrangement of the tubular ducts differ between genera and also between species. They may be very few, near the mouthparts and the attachment of each leg, as on several species of Coccus, or they may be in a broad submarginal band, as on species of Saissetia; in a broad submarginal band and in transverse rows on each segment, as on some Pulvinaria spp., or they may be present densely throughout the whole surface, as on species of Exaeretopus. Tubular ducts are structures normally associated with the adult female but they also occur, in particular patterns, on second-instar males. In adult females which produce an ovisac, such as species of Pulvinaria, the ventral tubular ducts are believed to be the organs which secrete the waxy ovisac. The function of the ducts of adult females which lack an ovisac but which possess ventral tubular ducts (e.g., species of Saissetia) has not yet been fully explained, although they are normally present on oviparous species and absent on viviparous species. Microducts are scattered all over the ventral surface but are mainly concentrated on the submarginal area. The microducts usually open through sclerotized pores which may have oval, square-shaped, 8-shaped or cruciform orifices (Fig. 1.1.2.1.9,B). Microducts are invaginated, with a short, thick inner ductule (Fig. 1.1.2.1.4,B).
DORSAL SURFACE The dorsal surface of the adult female is usually plain but on several species it may form projections or processes, while on others the surface may be distorted, with several irregular pits or hollows, as on species of Umwinsia and Couturierina. In the genus Saissetia, several species are provided with dorsal H-shaped ridges (Fig. 1.1.2.1.1,E).
Fig. 1.1.2.1.6. SEM micrographs of Etiennea villiersi Matile-Ferrero, adult female, Senegal, on Aphania senegalensis. A - Dorsum showing concentric ridges, length 4.5 mm. B - Dorsal submarginal tubercles with satellite tubular ducts and marginal spiniform setae. C - Dorsal submarginal tubercle and its satellite tubular "ducts (diameter 20 #m). D - Dorsal submarginal pocket-like tubercle (diameter 8 #m). (From Matile-Ferrero, 1984).
External morphology of the adultfemale
15
The dorsal cuticle of young adult females is usually membranous and may have, at most, a slightly sclerotized cuticle, provided with numerous areolations, plate-like areas or tessellations, as on Eucalymnatus tessellatus (Signoret). On fully-grown adult females, the dorsal cuticle may become heavily sclerotized, masking most of the taxonomic characters.
Anal plates The presence of two anal plates is one of the striking characters of the family, except in the aberrant genus Physokermes, where they are absent on the adult female. The anal plates are situated at the base of the anal cleft, which may be very deep and extend to half the length of the body, as with Protopulvinaria spp. The anal plates cover the anal opening and function as an operculum. They are sclerotized and consist of two plates, each of which articulates along its anterior margin. They are usually triangular in shape with lateral margins rounded and inner margins contiguous (Fig. 1.1.2.1.4,J) although, in a few genera, they may be reniform or bean-shaped. In some genera they are elongate with the antero-lateral margin shorter than the postero-lateral one (Fig. 1.1.2.1.8,L) or with the antero-lateral margin longer than the postero-lateral margin, as with Neolecanium silveirai (Hempel) (Fig. 1.1.2.1.7,10, Udinia and Protopuh,inaria spp. The dorsal surface of each plate usually bears a few setae known as apical setae, subdiscal setae and discal setae. The position and the shape of the anal plate setae differ according to genera and species and are of significant taxonomic value. In some genera, each plate bears numerous setae; thus Houardia troglodytes has about 38 setae on each plate and H. mozambiquensis has about 70 (Hodgson, 1990). In other genera, several stout spiniform setae may be present along the inner and posterior margin of each plate, as with Ceronema africana and Vitrococcus conchiformis (Newstead). Under the plate is a transverse ano-genital fold with a varying number of fringe setae (Fig. 1.1.2.1.5,G). Laterally there are two ventral thickenings (Fig. 1.1.2.1.7,B,F), each usually bearing a number of subapical setae (Fig. 1.1.2.1.4,j). In some genera, such as Ceroplastes, the anal plates are surrounded by a sclerotized area which may be produced into a dorsal caudal process.
Anal ring The anal ring, surrounding the anal orifice, is usually situated at the inner base of an anal invagination or anal tube. The anal ring is an incomplete, sclerotized ring which usually bears numerous wax pores and six to 12 long setae (Fig. 1.1.2.1.7,B). Rarely, the anal ring may be devoid of pores and have only short setae, as with species of Rhodococcus. The anal tube is eversible and extends past the anal plates to eject the liquid excrement or honeydew away from the body to avoid contamination (Williams and Williams, 1980; Foldi and Pearce, 1985) (Fig. 1.1.2.1.7,B,C). Some ant-attended species have lost this ability and, when ants are excluded, the species become severely contaminated with honeydew.
Setae and glandular structures The dorsal surface of the female is provided with setae and with numerous, welldefined glandular structures of high taxonomic significance. The diversity of the glandular structures is remarkable when compared with other scale insect families. There are three main types: pores, ducts and glandular tubercles. On the dorsum of species of Ceroplastes and Vinsonia, there are clear areas which lack large pores and setae when observed under the light microscope but these areas were found to be dotted with orifices of primary wax pores by Gimpel et al. (1974).
Section I. 1.2. I references, p. 20
16
Morphology
Fig. 1.1.2.1.7. A - Stictolecanium ornatum (Hempel), adult female, Brazil, on Eugeniajaboticaba: dorsal surface of abdomen, showing reticulated pattern of cribriform pores; (a) - individual cribriform pore (diameter 20 #m). B - Ceroplastes brevicauda Hall, adult female, Gabon, on Dacryodes edulis: anal plates, extended anal tube, anal ring and anal setae. C - Ceroplastodes zavanarii Bellio, adult female, Guinea Bissau, on unidentified plant: anal plates, extended anal tube, anal ring and anal setae. D- Eriopeltis festucae (Fonscolombe), adult female, France, on grass: last abdominal segments showing dorsal truncate cone-like setae. E- Eriopeltisfestucae, adult female: truncate cone-like setae on anal area. F- Neolecanium silveirai (Hempel), adult female, Ecuador, on roots of Elaeis guineen~is: last dorsal abdominal segments covered with cupule-shaped pores. G - Neolecanium silveirai: cupule-shaped pores (diameter 20 #m). (Photographs by D. Matile-Ferrero).
Setae Dorsal setae may be short and thick, lanceolate, cylindrical or conical, pointed, rounded, fringed or knobbed apically, and inserted in basal-sockets of different types. Dorsal setae are usually randomly scattered over the surface. On Tillancoccus spp., they are spine-like and arranged in single transverse rows. Rarely they are long and hair-like and are arranged in transverse bands (as on Houardia troglodytes), in medio-longitudinal lines (as on Trijuba oculata (Brain)), in clusters (as on Richardiella taiensis MatileFerrero & Le Ruyet (Fig. 1.1.2.1.4,A)) or fairly scattered over the entire d o r s u m (as on Melanesicoccus myrmecariae). An unusual type of stout, truncate, cone-like seta occurs on species of Eriopeltis, Mallococcus and some other genera, where they partly or entirely cover the surface (Fig. 1 . 1 . 2 . 1 . 7 , D , E ) .
External morphology of the adultfemale
17
Fig. 1.1.2.1.8. Mametia louisieae Matile-Ferrero, adult female, Comoro Is., on Eugenia caryophyUata. A - Dorsal and lateral view of female and ovisac. B - Adult female, dorsum and venter. C-J: ventral structures. C - Antenna. D - Quinquelocular disc-pore. E - Tubular ducts. F - Marginal setae. G - Body seta. H - Multilocular disc-pore. J - Hind tarsus, tarsal digitules, claw and claw digitules (note tibio-tarsal articulatory sclerosis). K-O: dorsal structures. K - Minute discoidal pore. L - Anal plates. M - Stigmatic clet~s and stigmatic setae, variation. N - Body seta. O - Tubular duct. (From Matile-Ferrero, 1978).
Section 1.1.2.1 references, p. 20
18
Morphology
Pores Dorsal pores may occur over the whole surface, while preopercular pores are generally restricted to the preopercular region (Figs 1.1.2.1.3,It,J; 1.1.2.1.5,K). Dorsal pores are most often disc-like and of three main types: the locular, cribriform and minute simple types. The first two types show many variations. Locular pores are frequent on species producing waxy tests, as on all Ceroplastes species and some related genera where the dorsal surface is densely covered with pores possessing up to five loculi. These pores are termed: unilocular, bilocular, trilocular, quadrilocular and quinquelocular pores. All or some of these five types may be found on the same species. The loculi of these pores may be circular, subcircular or oval and of different sizes. They can be of some importance for the separation of species. Large
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Ceroplasteshodgsoni (Matile-Ferrero & Le Ruyet), adult female, Ivory Coast, on Cleistanthus A - D o r s u m and venter. B-G: ventral structures. B - Cruciform minute duct. C - Marginal stigmatic seize. D - Quinquelocular disc-pore. E - Tubular duct. F - Marginal seiz. G - Multilocular discpore. H - L : dorsal structures. H - Body seta. J - Filamentous unilocular duct. K - Filamentous bilocular duct. L - Stigmatic seize. (From Matile-Ferrero and Le Ruyet, 1985). Fig. 1 . 1 . 2 . 1 . 9 .
polystachyus.
External mGrphology of the adultfemale
19
sclerotizext bilocular pores may also cover the entire dorsum, as on Neolecanium cornuparvum (Thro) and Pseudophilippia quaintancii Cockerell. These pores may be invaginated, as on the latter species. Cribriform pores (Fig. 1.1.2.1.4,K) occur on a few species. On species of Hemilecanium there are two pairs but they may be more numerous, as on species of Cribrolecanium (where they also differ in size) or they may form a reticulate pattern, as on Stictolecanium ornatum (Hempel) (Fig. 1.1.2.1.7,A,Aa). Large sclerotized cupule-shaped pores occur on a few species. These are the tubercular pores of Qin & Gullan (1989) and the compound pores of Williams & Watson (1990). They may cover the whole dorsum, as on Cryptostigma spp. and on Neolecanium silveirai (Fig. 1.1.2.1.7,F,G). Minute simple pores are often randomly scattered over the dorsum, as on Mametia louisieae (Fig. 1.1.2.1.8,K). Preopercular pores, although usually restricted to a group just anterior to the anal plates, may extend in a longitudinal band anteriorly as far as the head and laterally to several times the width of the anal plates. They are usually convex with a granular surface (Fig. 1.1.2.1.5,K) but may be conical or, less often, acorn-shaped.
Ducts Different types of tubular ducts and microducts may occur on the dorsum. The largest type is the tubular duct with a stout outer ductule and an slimmer inner ductule, similar to those on the venter (Fig. 1.1.2.1.8,O). The presence or absence of tubular ducts on the dorsal surface is a significant taxonomic character. Dorsal tubular ducts are lacking on many species of Coccidae, but they densely cover both surfaces on species of several genera, such as Exaeretopus, Luzulaspis, Philephedra and Mametia (Fig. 1.1.2.1.8,B). On a few species, the tubular ducts are only occasionally present and in small numbers, as on Coccus hesperidum (L.) and C. moestus De Lotto, where some individuals bear up to 31 tubular ducts on the submargin (Gill et al., 1977). On species of Parafairmairia, some of the dorsal tubular ducts are arranged in longitudinal and transverse rows. An unusual, small, tubular duct with a cone-like pore, observed recently on several species of Etiennea, may be scattered over the dorsum (Fig. 1.1.2.1.5,P). Small ducts, with a long branched inner filament called filamentous ducts, are present on several species of Ceroplastes, such as Ceroplastes hodgsoni (Matile-Ferrero and Le Ruyet) and on Vinsonia spp. (Fig. 1.1.2.1.9,J,K). Dorsal microducts are present on most Coccidae, usually scattered over the surface but sometimes arranged in bands, clusters or lines. They are different in structure from the ventral microducts and are more varied. These microducts may be slightly sunken or deeply invaginated, each with a slightly to heavily sclerotizeA unilocular or bilocular opening, with or without an inner ductule (Figs 1.1.2.1.3,M; 1.1.2.1.4,L; 1.1.2.1.5,M). Glandular tubercles Glandular tubercles are very complex, large structures with a sclerotizeA round domeshaped opening. Sometimes they are crateriform and named "inverted duct tubercles" as on Philephedra (Nakahara & Gill, 1985). Two types of glandular tubercles can be distinguished: submarginal tubercles and dorsal tubercles. Submarginal tubercles occur on more than half of the species of the family. They range in number from one to about 30 pairs, as on Hemilecanium imbricans (Green) (Hodgson, 1969) and Etiennea multituberculatum Hodgson. They are arranged in one, rarely two, rows along the submargins (Fig. 1.1.2.1.3,A). There are two primary types of submarginal tubercle: the first type has only one wide central tubular duct (Fig. 1.1.2.1.3,L); the second type has a wide central tubular duct
Section 1.1.2.1 references, p. 20
Morphology
20
surrounded by small satellite tubular ducts (Figs 1.1.2.1.5,Q; 1.1.2.1.6,B,C). The most commonly observed type is the first, which shows a wide range of patterns between species. The second type is unusual and is known only on three species of Etiennea (Hodgson, 1991a) and on Anopulvinaria cephalocarinata Fonseca. Submarginal tubercles may be present or absent on any single colony of the same species, as was reported by Williams & Kosztarab (1972) for Parthenolecanium corni (Bouchr). Dorsal tubercles occur only on a few species of Philephedra (Nakahara & Gill, 1985), Lagosinia (Hodgson, 1968) and Hemilecanium coriaceum Hall (Hodgson, 1969). Dorsal tubercles are similar in size and structure to the first type of submarginal tubercle and are arranged in longitudinal, irregular rows. On Lagosinia strachani (Cockerell), each dorsal tubercle is surrounded by small dome-shaped pores, termed knobules by Hodgson (1968). Dorsal tubercles of the second, uncommon, type occur on Etiennea villiersi Matile-Ferrero (Fig. 1.1.2.1.5,A). Another type of unusual tubercle is the pocket-like tubercle or sclerotized gland as found on Platysaissetiaferina De Lotto (De Lotto, 1978), Parasaissetia nigra (Nietner) (Ben-Dov, 1978) and more recently on the submargins among the submarginal tubercles on Etiennea (Figs. 1.1.2.1.5,R; 1.1.2.1.6,D) (Matile-Ferrero, 1984; Hodgson, 1991). Pocket-like tubercles are also present on the dorsal submargins of Ceroplastodes gowdeyi Newstead, termed "submarginal barely sclerotized ridged pores" by Hodgson (1971). The present author has observed a similar structure on Parthenolecanium persicae (Fabricius), mainly among the posterior submarginal tubercles.
REFERENCES Beardsley, J.W., 1966. Homoptera: Coccoidea. Insects of Micronesia, 6: 377-562. Ben-Dov, Y., 1978. Taxonomy of the nigra scale, Parasaissetia nigra (Nietner) (Homoptera: Coccoidea: Coccidae), with observations on mass rearing and parasites of an Israeli strain. Phytoparasitica, 6:115-127. 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). De Lotto, G., 1978. The soft scales (Homoptera: Coccidae) of South Africa, HI. Journal of the Entomological Society of Southern Africa, 41: 135-147. 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). International Journal of Insect Morphology and Embryology, 14: 259-271. Gill, R.J., 1988. The Scale Insects of California. Part 1. The Soft Scales (Homoptera: Coccoidea: Coccidae). Technical Series in Agricultural Systematics and Plant Pathology, California Department of Food and Agriculture, No. 1: xi + 132 pp. Gill, R.J., Nakahara, S. and Williams, M.L., 1977. A review of the genus Coccus Linnaeus in America north of Panama (Homoptera: Coccoidea: Coccidae). Occasional Papers in Entomology, State of California, Department of Food and Agriculture No. 24: 1-44. 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, College Park, Maryland, 841: 1-85. Hamon, A.B. and Williams, M.L., 1984. Arthropods of Florida and neighboring land areas. Vol. 11. The soft scale insects of Florida (Homoptera: Coccoidea: Coccidae). Florida Department of Agriculture & Consumer Services. Contribution No. 600. Florida Department of Agriculture, GainesviUe. 194 pp. Hodgson, C.J., 1967. Notes on Rhodesian Coccidae (Homoptera Coccoidea): Part 1: the genera Coccus, Parasaissen'a, Saissetia and a new genus Mashona. Arnoldia (Rhodesia), 3 (5): 1-24. Hodgson, C.J., 1968. Further notes on the genus Pulvinaria Targ. (Homoptera: Coccoidea) from the Ethiopian region. Journal of the Entomological Society of Southern Africa, 31: 141-174. Hodgson, C.J., 1969. The status of Hemilecanium imbricans (Green) (Homoptera: Coccoidea) in Africa south of the Sahara. Journal of Natural History, 3: 321-327. Hodgson, C.J., 1971. The species assigned to the genus Ceroplastodes (Homoptera: Coccoidea) in the Ethiopian Region. Journal of Entomology (B), 40:49-61. Hodgson, C.J., 1990. The scale insect genus Houardia Marchal (l-lomoptera: Coccidae). Systematic Entomology, 15: 219-226. Hodgson, C.J., 1991a. A revision of the scale insect genera Etiennea and Platysaissetia (Homoptera: Coccidae) with particular reference to Africa. Systematic Entomology, 16: 173-221.
External morphology of the adult female
21
Hodgson, C.J., 1991b. A redescription of Pseudopulvinaria sikla'mensis Atkinson (Homoptera, Coccoidea), with a discussion of its affinities. Journal of Natural History, 25: 1513-1529. Hodgson, C.J., 1994. The Scale Insect Family Coccidae. An Identification Manual to Genera. CAB International, Wallingford, 639 pp. Kawai, S., 1972. Diagnostic notes and biology of the coccid-species occurring on cultivated or wild trees and shrubs in Japan. Bulletin of the Tokyo-To Agricultural Experiment Station, 6 : 5 4 pp. + 48 plates. (in Japanese) Kawai, S., 1980. Scale Insects of Japan in Colors. National Agricultural Education Association, Tokyo, 455 pp. (in Japanese). Koteja, J., 1974. Comparative studies of the labium in the Coccinea (Homoptera). Scientific Papers of the Agricultural University in Krakow, 89: 1-162. Koteja, J., 1980. Campaniform, basiconic, coeloconic, and intersegmental sensilla on the antennae in the Coccinea (Homoptera). Acta Biologica Cracoviensia, series Zoologia, 22: 73-88. Koteja, J., Liniowska, E. and Lubowiedzka, A., 1976. On some changes of the cuticle in the female Saissetia hemisphaerica Targioni-Tozzetti (Homoptera, Coccinea). Acta Biologica Cracoviensia, series Zoologia, 19: 71-7. Matile-Ferrero, D., 1978. Homopt~res Coccoidea de l'Archipel des Comores. Mrmoires du Musrum National d'Histoire Naturelle (N.S.), Srrie A, Zoologic, 109: 39-70. Matile-Ferrero, D., 1984. Etiennea villiersi n.g., n.sp., du Srnrgal mrridional. Revue Franqaise d'Entomologie, 6: 99-103. Matile-Ferrero, D. and Le Ruyet, H., 1985. Cochenilles nouvelles du massif forestier de Ta'i, en Crte d'Ivoire (l-lomoptera, Coccoidea). Revue Franqaise d'Entomologie, 7: 273-286. Nakahara, S., and Gill, R.J., 1985. Revision of Philephedra, including a review of Lichtensia in North America and description of a new genus, Metapulvinaria. Entomography, 3" 1-42. Qin, T.K. and Gullan, P.J., 1989. Cryptostigma Fen,is: a coccoid genus with a strikingly disjunct distribution (l-lomoptera: Coccidae). Systematic Entomology, 14: 221-232. Rosciszewska, M., 1989. Structure and sense organs of antennae in females of Coccoidea (Homoptera, Coccinea). Scientific Papers of the Agricultural University in Krakow, 129:1-126 (in Polish). Snodgrass, R.E., 1935. Principles of Insect Morphology. McGraw-Hill Co., New-York and London, 667 pp. Steinweden, J.B., 1929. Bases for the generic classification of the coccoid family Coccidae. Annals of the Entomological Society of America, 12: 197-245. Williams, D.J. and Watson, G.W., 1990. The Scale Insects of the Tropical South Pacific Region, Part 3. The Soft Scales (Coccidae) and Other Families. CAB International, Wallingford, 267 pp. Williams, J.R. and Williams, D.J., 1980. Excretory behaviour in sof~ scales (Hemiptera: Coccidae). Bulletin of Entomological Research, 70: 253-257. Williams, M.L. and Kosztarab, M., 1972. The insects of Virginia: No. 5. Morphology and systematics of the Coccidae of Virginia with notes on their biology 0tomoptera: Coccoidea). Virginia Polytechnic Institute and State University, Research Division Bulletin, 74: 1-215.
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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.
23
1 . 1 . 2 . 2 The Adult Male JAN H. GILIOMEE
INTRODUCTION The morphology of male Coccidae (Fig. 1.1.2.2.1) has been the subject of extensive studies by Giliomee (1967) and Miller (1991). These two authors have described males of about 50 species and expanded our knowledge of the male morphology and taxonomy of this family, which had been previously based mostly on the detailed morphological study of just one species (Theron, 1958). Using the terminology of Giliomee (1967), a few further species have been described by Gimpel et al. (1974), Ray & Williams (1980, 1983), Manawadu (1986), Farrel (1990) and Hodgson (1991, 1993). These studies on the male do not corroborate the classifications of the Coccidae suggested by workers such as Bodenheimer (1953) and Borchsenius (1957), who used only female characters. Giliomee (1967) proposed four species-groups, i.e. Eulecanium-, Eriopeltis-, Inglisia- and Coccus-groups. Later, Ray & Williams (1983) added the Toumeyella-group for the males of the genera Neolecanium, Pseudophilippia and Toumeyella studied by them. Miller (1991) in general supported these groupings. He redefined the Eulecanium-, Eriopeltis-, Coccus- and Toumeyella-groups and added the Philephedra-, Sphaerolecanium- and Protopulvinaria-groups. The f'mdings from studies on the male were ignored in the classification proposed by Tang Fang-teh et al. (1990) and Tang Fang-teh (1991). However, Hodgson (1994) made a courageous attempt to end the schism by taking the relationships indicated by the studies of the male into consideration when he proposed the division of the Coccidae into 10 subfamilies. The description that follows is mainly based on Giliomee (1967) and Miller (1991). The abbreviations refer to Fig. 1.1.2.2.2.
GENERAL APPEARANCE In contrast to the female, adult male Coccidae have a typical insect shape, with a clearly defined head, thorax and abdomen. The front wings and three pairs of legs are well developed. The antennae are long and filiform and the elongated penial sheath is conspicuous, forming the tip of the abdomen. A long wax filament is produced by a glandular pouch on each side of the VIII abdominal segment. The total length of the male varies between 1 and 3 mm, depending on the species.
HEAD The rounded head capsule is partly sclerotizexl. Dorsomedially, a reticulated median crest (me) is found, which extends anteriorly over the apex of the head. In some species, it carries vestiges of the midcranial ridge (mcr) dorsally or anteriorly. The large, reticulated ocular sclerite (oes) covers most of the ventral and part of the lateral surface of the head capsule. It is partly bounded anteriorly by the preocular ridge (procr), which bears a process for articulation with the scape, and posteriorly by the prominent postocular ridge (pocr). In some cases the latter surrounds or partly
Section 1.1.2.2 references, p. 30
24
Morphology
U Fig. 1.1.2.2.1. Dorsal view of an adult male soft scale insect.
surrounds the ocellus. The two ridges are sometimes joined together below the ocellus by an interocular ridge (ior). Ventrally, the ventral part of the midcranial ridge (vmer) extends anteriorly from the ocular sclerite and forks into the lateral arms of the midcranial ridge (liner), which may also bifurcate. Sometimes a linear vestigial ridge is present dorsally on the median crest, representing the dorsomedial part of the mideranial ridge (diner). On the posterior edge of the ocular sclerite, a narrow preoral ridge (WoO links the two postocular ridges and supports a scoop-like cranial apophysis (ca). Behind this structure a vestigial mouth opening (mo) is found, surrounded by two tendon-like apodemes (t), and two or four tentorial pits (atp, ptp). The ocular sclerite bears a pair of lateral ocelli (o) and a variable number of simple eyes. Some species only have large pairs of dorsal simple eyes (dse) and ventral simple eyes (vse), but others also possess 1 to 3 pairs of smaller lateral simple eyes
(Ise). Behind the postocular ridge, the gena (g) is found in the form of a reticulated bulge. The antennae are inserted on the anterolateral margin of the head. They are usually 10-segmented, but antennae with 9 or fewer segments are found in some groups. The scape (scp) is short and broad, the pedicel (pdc) subglobular and the flagellar segments (Fro-t,,) tubular.
THORAX Prothorax. A deep cervical constriction separates the head from the largely membranous prothorax. Just posterior to the constriction, the collar-like pronotal ridge (prnr), with the associated pronotal sderite (prn) on each side, is very distinct. Posterolaterally a small, weakly sclerotized, sometimes striated posttergite (pt) is found. Pleurally, a ridge-like pro-episternum + cervical sclerite (pepcv) stretches from the postocular ridge anteriorly to the short propleural ridge (plr~), which articulates with the coxa of the front leg; posteriorly, an invagination of the pleural ridge forms a small propleural apophysis (plal). The prosternum (stnl) consists of a triangular or oval
The adult male
25
sclerite, bounded posteriorly by a transverse ridge and traversed medially by a longitudinal ridge which shows varying degrees of inter- and intraspecific development. Mesothorax. As principal wing-bearing segment, this part of the body is heavily sclerotized, with strong ridges and sutures. The notum is widely separated from the postnotum by a membranous area and is subdivided into a prescutum, scutum and scutellum. The prescutum (prsc) has the shape of a subrectangular, reticulated bulge, which bears an internal mesoprephragma anteriorly. Laterally and posteriorly it is separated from the scutum by strong prescutal ridges (pscr) and a prescutal suture (pscs) respectively. The scutum (set) is characterized by a large, median, membranous area and two lateral parts which extend along the prescutum anteriorly and the scutellum posteriorly. Anterolateral to the scutum, a semitubular prealare (pra) and convex triangular plate (tp) extend to the epistemum. Posteriorly, along the lateral margin of the scutum, an anterior notal wing process (anp) and a posterior notai wing process (pnp) can be discerned. The scuteilum (scl) has a transversely rectangular shape and is usually semi tubular with an internal scuteilar foramen (sclf). Behind the scutellum a large membranous area separates it from the mesopostnotum (pnz), which curves deeply into the metathoracic cavity. The postnotum bears a mesopostphragma on its posterior margin and a deep postnotal apophysis (pna) on each side. Anterolaterally it is produced into a strong postalare (pa) which articulates with the mesopleural ridge and bears the anterior and posterior postalar ridges (apar, ppar) on its margins. Pleurally, the large episternum (epsz) is divided into dorsal and ventral parts by a membranous cleft. The dorsal part is convex and bounded anteriorly by a subepisternal ridge (ser) which extends across the cleft. The ventral part is a narrow sclerite which extends from the mesopleural ridge (plr2) posteriorly to the lateropleurite (lpi) anteriorly. The mesopleural ridge (plrz) is a broadly sclerotized ridge which stretches obliquely across the pleuron from the large, rounded mesopleural wing process (pwpz) dorsally to the coxa ventrally. The mesopleural apophysis (plaz) is invaginated, where it is overlapped by the postalare. On the lower anterior margin, a small, tendon-like apodeme (t) is found and posterodorsally a small subalare (sa). The pleural wing process is usually connected with the epistemum by means of a narrow sclerite, the basalare (bas); in some species, such as Coccus hesperidum L., it is vestigial. Posterior to the lower extremity of the pleural wing process, a small sclerite represents the mesepimeron (epmz). The mesothoracic spiracle (sp,.), supported by a peritreme (ptrz), is situated behind the pleural apophysis of the prothorax. The mesosternum consists almost entirely of the large basisternum (stnz), of which the anterior part is bounded by a short marginal ridge (mr) and the posterior part by a precoxal ridge (pcrz). A longitudinal median ridge (mdr), which is sometimes interrupted or vestigial, divides the basistemum into two parts. On the posterior margin of the basistemum, a transverse furcal pit (fp) with a large internal furca (f) is situated.
Metathorax. The metathorax is largely membranous. However, a well developed, invaginated metanotum closely overlaps the mesopostnotum, with its posterior margin usually forming a ridge-like structure dorsally. On each side, a suspensorial sclerite (ss) anchors the haltere when the latter is present, while further posteriorly a small transverse sclerite represents the metapostnotum (pn3). Pleurally, the metapleural ridge (pir 3) extends dorsally from the coxal articulation towards the base of the haltere where it expands into a small metapleurai wing process (pwp3). About half-way from the coxa, the metapleurai apophysis (pla3) is represented by a shallow depression. When the halteres are absent, the ridge only extends for a short distance above the coxal articulation. From the ridge, the metepisternurn (epss) extends anteroventrally and the metepimeron (epm3) posteriorly. A vestigial precoxal ridge (pcr3) sometimes extends anteriorly from the pleural ridge along the margin of the episternum.
Section 1.1.2.2 references, p. 30
26
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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
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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
O I II
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Fig. 1.1.2.3.1. Pseudophilippia quaintancii Cockerell, 1st instar (From Ray and Williams, 1980).
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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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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Pseudophilippia quaintancii Cockerell, 2nd-instar ~ (From Ray and Williams, 1980).
Mouthparts: well developed, similar to first instar. Legs: usually well developed, without tibio-tarsal sclerosis or free articulation, but may be reduced. Each tarsus and claw with a pair of digitules, usually knobbed, but when legs reduced, may become setiform. Claw digitules usually unequal, with one broad and the other slender. Claw denticle present or absent. Spiracles: two pairs of thoracic spiracles present. Spiracular furrows with quinquelocular disc-pores in bands 1-3 pores wide. Occasionally disc-pores with 4-6 loculi may occur mixed with quinquelocular pores.
The immature stages
39
Spiraeular setae: usually present in groups of 3, with median seta longest, rarely absent or undifferentiated from marginal setae. Stigmatic sclerotisations occasionally present. Anal plates: each plate usually triangular, cephalolateral (anterior) margin normally longer than caudolateral (posterior) margin. Most often with 4 apical setae and 1 subapical seta. Anal fold with 1 or 2 pairs of fringe setae. Anal ring: with pores and 6 setae. Pores: bilocular pores (dorsal microductules) and simple pores are scattered over the dorsum. Occasionally pores of unique structure, which are particular to a species, may occur on the dorsum. A single conical, simple pore (preantennal pore) is usually found ventrally just anterior to the antennal scape. Various types of multilocular disc-pores occur in the spiracular furrows (spiracular disc-pores). Preopercular pores absent. Ducts: tubular ducts disposed along margin on dorsum of second-instar males. Sometimes these ducts are also arranged in patterns similar to the suture pattern of the male test, which is produced by the second-instar male. Tubular ducts usually absent in the female, but occur dorsally around margin in Eulecanium cerasorum, and ventrally around margin in Pseudopulvinaria sikkimensis Atkinson. Microducts with square, oval or cruciform openings scattered over venter, more numerous in submarginal areas, often absent in mid-ventral region. Setae: dorsal body setae present or absent, when present usually few in number. Marginal setae variable in structure and number, more numerous than in first instar, longest on posterior of body near anal cleft. Ventral body setae short, slender and pointed, but may be straight or curved; generally located in a submarginal row and scattered sparsely on other parts of body. Usually with 2 pairs of interantennal setae, rarely 1 pair. Usually with 3 pairs of ventral submedian setae on pregenital segments of abdomen, but with 2 pairs in Eucalymnatus tessellatus (Signoret), Protopulvinaria pyriformis and Milviscutulus mangiferae (Green) and only 1 pair in species of Ceroplastes and Vinsonia. Submarginal tubercles" present or absent; if present, few in number, generally only 1 dorsally on each side of body between anterior and posterior spiracular setae groups.
THIRD-INSTAR FEMALE (Figs 1.1.2.3.6, 1.1.2.3.7) In some Coccidae this stage is the adult female, but it seems that most species have three immature instars in the female. The immature third-instar female is very similar in appearance to the adult and can very easily be overlooked or mistaken for young adult females if not examined microscopically. The third-instar female can usually be recognized because it has fewer pores, setae and other dermal structures. It may also have fewer antennal segments and anal ring setae, while tubular ducts and multilocular disc-pores are absent or few in number on the venter of the abdomen. The immature third instar is intermediate between the second instar and adult female, and basically differs from each in the number of dermal structures, having more than the second instar and less than the adult.
Section 1.1.2.3 references, p. 46
40
Morphology
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1.1.2.3.6.
Pseudophilippia quaintancii Cockerell,
3rd-instar ~? (From Ray and Williams, 1 9 8 0 ) .
In the immature third-instar female, the body outline is oval to nearly circular, with a well-developed anal cleft; antennae well developed or reduced, six-or seven-segmented' with one to three pairs of interantennal setae; legs may be well developed, without tibiotarsal sclerosis or free articulation, or reduced; tarsal claws each with paired digitules which may be equal or unequal in shape; spiracular setae generally differentiated from marginal setae; dorsal body setae present or absent; anal plates always present, with one to three pairs of fringe setae; anal ring most often with eight setae, but sometimes six; multilocular disc-pores and tubular ducts usually absent from venter of abdomen; preopercular and discoidal (dorsal simple) pores absent; submarginal tubercles, when present, usually located on head, thorax and abdomen in lesser numbers than in the adult.
41
The immature stages
'~ L
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THIRD-INSTAR MALE (PREPUPA) (Fig. 1.1.2.3.8) The third-instar male or "prepupa" is enclosed within a glassy wax test produced by the second-instar male. This stage begins a transformation of the body into a form quite different from that seen in the female. In the prepupal stage, the body is elongate, narrowest anteriorly, widest at the wingbuds or abdomen; derm membranous; segmentation indistinct; antennae usually elongate, but may be reduced
Section 1.1.2.3 references, p. 46
Morphology
42
Fig. 1.1.2.3.8. Williams, 1980).
Pseudophilippia quaintancii Cockerell, 3rd-instar ~ (prepupa) (From Ray and
(e.g., Pseudophilippia quaintancii), with eight to nine poorly defined segments; legs somewhat lobe-like with five segments and reduced claws and digitules; wingbuds arising laterally on thorax between pro- and mesothoracic legs and usually extending back to base of metathoracic leg; thoracic spiracles with zero to eleven disc-pores near atrium, these pores may have three to eight loculi; a few marginal setae located on anterior of head and on abdomen; body setae sparse, generally with a pair on dorsum of head and a few scattered posteriorly on abdomen; ventrally, usually with a few scattered near each coxa and medially and laterally on abdomen; with two pairs of interantennal setae; posterior of body with a well-sclerotised median penial lobe which is usually rounded and not extending past caudal lobes; anal opening near base of penial lobe and genital opening near apex; usually two sclerotised caudal extensions lateral to penial lobe but these are absent in Pseudopulvinaria sikkimensis (Hodgson, 1991). In the prepupal male, anal plates, eyes, submarginal tubercles, dorsal pores, spiracular setae and tubular ducts are absent.
43
The immature stages
FOURTH-INSTAR MALE (PUPA) (Fig. 1.1.2.3.9) In the pupal stage, the body remains largely membranous, but tagmata are more clearly expressed, and the appendages are more strongly developed. Other characteristics are similar to the prepupa. Differences from the prepupa include: antennae and legs more sclerotised and greater in length; antennae directed posteriorly
,,,o
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A
Fig. 1.1.2.3.9. Pseudophilippia quaintancii Cockerell, 4th-instarg (pupa) (FromRay and Williams, 1980).
and nine- or ten-segmented; prothoracic legs directed anteriorly and usually C-shaped, with tibia and tarsus curved toward midline of body; wing buds extending as far back as anterior abdominal segments; disc-pores associated with spiracular atrium numbering zero to nineteen, each pore with four to twenty loculi; penial lobe or sheath triangular in shape and usually extending past caudal lobes of abdomen.
Section 1.1.2.3 references, p. 46
44
Morphology TABLE 1.1.2.3.1 List of descriptions and/or illustrations of immature stages of Coccidae in literature Species
Immature stage/s
References
Bodenheimera rachelae (Bodenheimer) Ceronema banksiae Maskell Ceronema koebeli Green Ceroplastes actiniformis Green Ceroplastes brevicauda Hall Ceroplastes ceriferus Fabricius Ceroplastes destructor Newstead Ceroplastes floridensis Comstock Ceroplastes japonicus Green Ceroplastes pseudoceriferus Green
1st, 2ndg, 2ndd' 1st 1st I st nymphal instars 1st, 2ndg, 3rd9 nymphal instars 1st, 2ndg, 3rd9 1st, 2ndg, 3rd9 1st, 2ndg, 3rdg, 2ndd', 3rdd', 4thd' 1st
Ben-Dov, 1969; Hodgson, 1994 Morrison & Morrison, 1922 Green 1909 Green 1909 Cilliers, 1967 Green, 1909; Pollet, 1972 Cilliers, 1967 Green, 1909; Ben-Dov, 1970; Pollet, 1972 Camporese and Pellizzari, 1994
nymphal instars 1 st 1st, 3rd? 1 st 1st 1st, 3rd?, 3rdr 4thS'
Marchal, 1909 Green, 1909 Ezzat & Hussein, 1967 Hodgson, 1971 Hodgson, 1970 Leonardi, 1920; Ben-Dov, 1975; l~eh~i~ek, 1960 [as F. viburni (Signoret)]; Borchsenius, 1957 [asF. rosemar/n/Goux];
Ceroplastes rusci (Linnaeus) Ceroplastes sinensis Del Guercio Chloropulvinaria psidii (Maskell) Coccus acutissimus (Green) Coccus asiaticus (Green) Coccus hesperidum Linnaeus
Coccus pseudomagnoliarum (Kuwana) Coccus viridis (Green) Cryptes baccatus (Maskell) Cryptostigma endoeucalyptus Qin & Gullan Ctenochiton viridis Maskell Didesmococcus koreanus Borchsenius Drepanococcus cajani (Maskell) Ericerus pela (Chavannes) Eriopeltis festucae (Fonscolombe) Eriopeltis lichtensteini Signoret Eriopeltis stammeri Schmutterer Eriopeltis varleyi Manawadu Etiennea ferox (Newstead) Etiennea gouligouli Hodgson Etiennea montrichardiae (Newstead) Etiennea muMturberculum Hodgson Etiennea petasus Hodgson Etiennea sinetuberculum Hodgson Eucalymnatus tesseUatus (SignoreO
Eulecanium caraganae Borchsenius Eulecanium ciliatum (Douglas) Euleeanium franconicum (Lindinger) Euleeanium kunoense (Kuwana) Eulecanium sericeum (Lindinger) Eulecanium tiliae (Linnaeus) Filippia follicularis (Targioni Tozzeui) Gascardia madagascariensis Targioni Tozzetti Houardia troglodytes (Marchal) Inglisia chelonoides Green Kilifia acuminata (Signoret) Kozaricoccus bituberculatus (Brain) Lagosinia vayssierei (Castel-Branco) Lichtensia viburni Signoret
Sankaran, 1962; Kawai & Tamaki, 1967 Leonardi, 1920; G6mez-Menor Ortega, 1937; Vilar, 1951, 1952 1st, 2ndg, 3rd9 Pollet, 1972; Snowball, 1970 1st, 2nd 9 Green, 1909 1st Green, 1909 [as L. acutissimus (Green)] 1st Green, 1909 [as L. caudatum Green] 1st, 2ndg, nymphal Green, 1909 [as L. signiferum Green]; instars G6mez-Menor Ortega, 1937, 1958; Borchsenius, 1957; Fonseca, 1973; l~eh~ek, 1960 Fonseca, 1953 1st [as Lecanium viride Green]: Green, 1904 1st,2nd 9 Morrison & Morrison, 1922 1st Qin & Gullan, 1989 1st Morrison & Morrison, 1922 1st Borchsenius, 1957 1st Green, 1909 [as Ceroplastodes cajani 1st Maskell] Kuwana, 1923; Ferris, 1950; Danzig, 1965 1st, 2nd 9 Leonardi, 1920; G6mez-Menor Ortega, 1 st 1937; l~eh~i~ek, 1960 l~eMi~ek, 1960 1 st Schmutterer, 1952 1 st Manawadu, 1986 I st, 2ndd' Hodgson, 1993 1st, 2nd9 Hodgson, 1993 3rdg, 2ndd Hodgson, 1993 1st, 2nd9 & d', 4thd' Hodgson, 1993 1st, 3rdg, 2nd~ Hodgson, 1993 1st, 2nd9 & d', 3rdg, 4thd' Hodgson, 1993 1st, 2rid9 & c~, 3rdg, 4thd' Green, 1904 [as L. tessellatum var. 1st, 2ndg, 3rd9 perforatum (Newstead)]; G6mez-Menor Ortega, 1937, 1958; Reh~i~ek, 1960; Ray & Williams, 1981 Borchsenius, 1957; Tereznikova, 1981 1st, 3rd? l~ehti~ek, 1960 1st l~eh~i~ek, 1960 1st Husseiny & Madsen, 1962 1st, 2ndg, 4thd' Reh~i~ek, 1960 1 st Silvestri, 1919; Silvestri, 1920 [as 1st, 2ndg,3rdd', Eulecanium coryli (L.)]; Kawecki, 1958b 4th~ and l~eh~i~ek, 1960 [as L. coryli (L.)] Leonardi, 1920; G6mez-Menor Ortega, 1 st 1937; Ben-Dov, 1973 Targioni Tozzetti, 1895 nymphal instars
45
The immature stages TABLE 1.1.2.3.1 (continued) Species
Immature stage/s
References
Luzulaspis frontalis Green Luzulaspis luzulae (Dufou0 Luzulaspis scotica Green Mallococcus sinensis (Maskell) Marsipococcus marsupialis (Green) Milviscutulus mangiferae (Green)
1st 1 st 1 st 1st, 2nd9 2nd~? 1st, 2nd?, 3rd9
Neolecanium cornuparvum (Thro)
1st, 2ndg, 3rdg, 2nd~', 3rdd', 4the' 1 st 1st, 2rid9
l~eh~i~ek, 1960; Koteja, 1966 l~eh~i~ek, 1960 l~eh~i~ek, 1960 Lambdin & Kosztarab, 1973 Green, 1904 [as L. marsupiale Green] Green, 1904 [as P. mangiferae Green]; Ben-Dov et al., 1975 Ray & Williams, 1983
Neolecanium silveirai (Hempel) Neopulvinaria innumerabilis (Rathvon) Paracardiococcus actinodaphnis Takahashi Parafairmairia biparu'ta (Signoret) Parafairmairia gracilis Green Paralecanium expansum (Green) Paralecanium marginatum (Green) Paralecanium planum (Green) Paralecanopsis festucae (Borchsenius) Paralecanopsis fallax (Giard) Paralecanopsis formicarum (Newstead) Paralecanopsis Paralecanopsis Paralecanopsis Paralecanopsis Paralecanopsis
iridis (Borchsenius) shutovae (Borchsenius) taurica (Borchsenius) terrestris (Borchsenius) turcica Bodenheimer
Parasaissetia nigra (Nietne0 Panhenolecanium cerasifex (Fitch) Parthenolecanium corni (Bouch6) Parthenolecanium fletcheri (Cockerell) Parthenolecanium persicae (Fabricius) Parthenolecanium pomeranicum (Kawecki) Parthenolecanium rufulum (Cockerell) PhyUostroma myrfflli (Kaltenbach) Physokermes hemicryphus (Dalman) Physokermes piceae (Schrank) Protopulvinaria pyriformis Cockerell Pseudophilippia quaintancii Cockerell Pseudopulvinaria sikkimensis Atkinson Psilococcus tuber Borchsenius Pulvinaria delottoi Gill Pulvinaria flavescens Brethes Pulvinaria horii Kuwana Pulvinaria hydrangeae Steinweden
Lepage & Piza, 1941 Phillips, 1962; Canard, 1965, 1966 [as N. imeretina (Hadzibeji)] Hodgson, 1994 2ndg, 2ndd' G6mez-Menor Ortega, 1948 1st Schmutterer, 1952;Reh~ek, 1960; 1st, 2nd 9, 2ndd, 3rdd, 4thd Koteja & Rosciszewska, 1970 2ndg, 2ndd' Green, 1904 [as L. expansum Green] 2nd<~ Green, 1904 [as L. marginatum Green] 1st Green, 1904 [as L. planum Green] 2ndg, 3rd9 Borchsenius, 1957; Tereznikova, 1981 1st Borchsenius, 1957 1st, d'9 nymphal Schmutterer, 1952; l~eh~ek, 1960; instars Boratynski et al., 1982 1st, 2nd9 Borchsenius, 1957; Danzig, 1980 1st, 2nd9 Borchsenius, 1957 2ndg, 3rd9 Borchsenius, 1957 3rd9 Borchsenius, 1957 1st, 2ndg, 2ndd' Hodgson, 1994; Tereznikova, 1981 and Borchsenius, 1957 [as L. porifera Borchsenius] I st, 2nd ~?, 2nd d', Green, 1904 [as L. n/grum Nietner]; Smith, 3rd9 1944; Ben-Dov, 1978 1st, 2nd9 Richards, 1958 1st, 2nd~? Bielenin,v1958; Canard, 1968; Kawecki, 1958a; Reh~i~ek, 1960; Dziedzicka & Sermak, 1967; Gonzalez, 1989 1st, 2 n d ~ ? Schmutterer, 1954; Borchsenius, 1957; l~eh~i~ek, 1960; Dziedzicka, 1968 2nd9 Green, 1928; Boratynski, 1970 1st, 2rid9 l~ehti~ek, 1960; Dziedzicka, 1968 1st, 2nd9 Schmutterer, 1954; G6mez-Menor Ortega, 1960 [as Eu. pulchrum (King)]; l~eh~i~ek, 1960; Dziedzicka, 1968 1st l~eh~i~ek, 1960 1st Schmutterer, 1956; Tereznikova, 1981 1st Schmutterer, 1956;Reh~ifiek, 1960 1st, 2ndg, 3rd9 G6mez-Menor Ortega, 1948, 1958; Ray & Williams, 1982 1st, 2nd?, 3rdg, Ray & Williams, 1980; Hamon & 2nd~, 3rdd', 4the' Williams, 1984 1st, 2ndd', 2ndg, Hodgson, 1991 3rd~?, 4the' Koteja, 1969 [as P. parvus Borchsenius] nymphal instars Gill, 1979 1st, 2ndg, 3rd9 Ringuelet, 1924; l~ehti~ek, 1960; 1st Canard, 1965 Canard, 1994 1 st 1st, 2ndg, 2ndd', Canard, 1965, 1969 3rd9
Pulvinaria salicicola Borchsenius Pulvinaria vitis (Linnaeus)
nymphal instars 1st, 2nd?
PulvinarieUa mesembryanthemi (Vallot)
1st
Section 1.1.2.3 references, p. 46
Shmelev, 1975 l~eh~ek, 1960 [as P. betulae (L.)]; Phillips, 1962; Canard, 1965 [as P. oxyacanthae (L.)] G6mez-Menor Ortega, 1937; Quintana, 1956; Canard, 1965
46
Morphology TABLE 1.1.2.3.1 (continued) Species
Immature stage/s
References
Rhizopulvinaria arenaria Canard Rhizopulvinaria artemisiae (Signoret) Rhizopulvinaria grassei (Balachowsky) Rhizopulvinaria maritima Canard Rhizopulvinaria saxatilis Canard Rhodococcus spiraeae (Borchsenius) Rhodococcus turanicus (Archangelskaya) Saissetia coffeae (walker) Saissetia oleae (Olivier) Scythia craniumequinum Kiritshenko Scythia festuceti (Sulc) Sphaerolecanium prunastri (Fonscolombe)
I st 1st 1st 1 st 1st 1 st
1st 1st, 2ndg, 3rd9 1st 2nd 9, 2ndd' 1st 1st, 2ndg, 3rd9
Takahashia japonica Cockerell Toumeyella cerifera Ferris ToumeyeUa cubensis Heidel & Kohler ToumeyeUa liriodendri (Gmelin) Toumeyella mirabilis (Cockerell) Toumeyella nectandrae Hempel Toumeyella parvicornis (Cockerell) Toumeyella pini (King) ToumeyeUa quadrifasciata (Cockerell) Toumeyella sonorensis (Cockerell & Parrott) ToumeyeUa virginiana Williams & Kosztarab Vinsonia stellifera (Westwood) Waxiella africana (Green)
1st 1st 1st 1st 1st 1st 1st 1st 1st 1st 1st 1st, 2nd 9 nymphal instars
Canard, 1967, 1968 Canard, 1968 Canard, 1965, 1968 Canard, 1967, 1968 Canard, 1967, 1968 Borchsenius, 1957; l~eh~i~ek, 1960 Borchsenius, 1957 Brewer & Howell, 1981 15,eh~i~ek, 1960; Argyriou, 1967 Hodgson, 1994 Reh~i~ek, 1960 Silvestri, 1920; l~eh~i~ek, 1960; Ben-Dov, 1968 Kuwana, 1902 Sheffer & Williams, 1990 Sheffer & Williams, 1990 Sheffer & Williams, 1990 Sheffer & Williams, 1990 Sheffer & Williams, 1990 Sheffer & Williams, 1990 Sheffer & Williams, 1990 Sheffer & Williams, 1990 Sheffer & Williams, 1990 Sheffer & Williams, 1990 Green, 1909 Cilliers, 1967 [as C. mimosae Signoret]
REFERENCES Argyriou, L.C., 1967. The scales of olive trees occurring in Greece and their entomophagous insects. Annales de L'Institut Phytopathologique Benaki, (N.S.), 5: 353-377. 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., 1969. A generic diagnosis of Bodenheimera Bodenheimer (Homoptera: Coccidae) with redescriptions of B. rachelae (Bodenheimer). Proceedings of the Royal Entomological Society of London (B), 38: 70-74. Ben-Dov, Y., 1970. Laboratory rearing of wax scales. Journal of Economic Entomology, 63: 1998-1999. Ben-Dov, Y., 1973. The genus Euphilippia Berlese and Silvestri (l-lomoptera: Coccidae) with redescriptions of its type-species. Bolletino del Laboratorio di Entomologia Agraria "Filippo Silvestri", Portici, 30: 282-292. Ben-Dov, Y., 1975. On the identity of Filippia Targioni Tozzetti, 1868 and Lichtensia Signoret, 1873 (Homoptera: Coccidae). Journal of the Entomological Society of Southern Africa, 38: 109-121. Ben-Dov, Y., 1978. Taxonomy of the nigra scale, Parasaissetia nigra (Nietner) (Homoptera: Coccoidea: Coccidae), with observations on mass rearing and parasites ofan Israeli strain. Phytoparasitica, 6:115-127. Ben-Dov, Y., 1993. A Systematic Catalogue of the Soft Scale Insects of the World (Homoptera: Coccoidea: Coccidae), with Data on Geographical Distribution, Host Plants, Biology and Economic Importance. Flora and Fauna Handbook No. 9. Sandhill Crane Press, Inc. Gainesville, Florida, 536 pp. Ben-Dov, Y., Williams, M.L. and Ray, C.H., 1975. Taxonomy of the mango shield scale, Protopulvinaria mangiferae (Green) (l-lomoptera: Coccidae). Israel Journal of Entomology, 10: 1-17. Bielenin, I., 1958. La structure et l'apparition des filieres dorso-marginales chez le deuxieme stade larvaire du Lecanium corni Bouch6, Marchal (female nec male) Homoptera, Coccoidea, Lecaniidae. Polskie Pismo Entomologiczne, 27: 97-104. [In Polish, French summary]. Boratyfiski, K., 1970. On some species of "Lecanium" (Homoptera: Coccidae) in the collection of the Naturhistorisches Museum in Vienna; with description and illustration of the immature stages of Parthenolecanium persicae. Annalen des Naturhistorischen Museums, Wien, 74: 63-76. Boratyfiski, K., Pancer-Koteja, E. and Koteja, J., 1982. The life history of Lecanopsisformicarum Newstead (Homoptera: Coccinea). Annales Zoologici Warszawa, 36: 517-537. Borchsenius, N.S., 1957. Subtribe mealybugs and scales (Coccoidea). Soft scale insects Coccidae. Vol. IX. Fauna SSSR. Zoologicheskii Institut Akadamii Nauk SSSR, 66:1-493,447 figs. [In Russian]. Brewer, B. and Howell, J.O., 1981. Description of the immature stages and adult female of Saissetia coffeae (Walker). Annals of the Entomological Society of America, 74: 548-555. Camporese, P. and Pellizzari, G., 1994. Description of the immature stages of Ceroplastes japonicus Green (Homoptera: Coccoidea). Bolletino di Zoologia Agraria e di Bachicoltura, Series H, 26 (1): 49-58. Canard, M., 1965. Observations sur une Pulvinaire peu connue du midi de France: Eupulcinaria hydrangeae (Steinweden) (Coccoidea - Coccidae). Annales de la Socidtd Entomologique de France (N.S.), 1: 411-419. Canard, M., 1966. Une Pulvinarie de la vigne, nouvelle pour la France: Neopulvinaria imeretina (Coccoidea, Coccidae). Annales de la Socidtd Entomologique de France (N.S.), 2: 189-197. Canard, M., 1967. Les Rhizopulvinaires des oeillets Mediterraneens (Horn. Coccidae). Vie et Milieu. Bulletin du Laboratoire Arago, Universite de Paris. Serie C: Biologie terrestre, 18: 169-184.
The immature stages
47
Canard, M., 1968. Contribution a l'etude des Rhizopulvinaires Mediterraneens (Hom. Coccidae). Bulletin de la Socirt6 Entomologique de France, 73: 90-96. Canard, M., 1969. La lignee male de Eupulvinaria hydrangeae (Hom. Coccidae). Annales de la Socirt6 Entomologique de France ,(N.S.), 5: 457-460. Canard, M., 1994. Une cochenille floconneuse Pulvinaria horii Kuwana, 1902 (Homoptera: Coccidae) nouvelle pour la faune d'Europe continentale. Biologia gallo-hellenica, 21 (1): 35-40. Cilliers, C.J., 1967. A comparative biological study of three Ceroplastes species (Hemip. Coccidae) and their natural enemies. Entomology Memoirs. Department of Agricultural Technical Services, Republic of South Africa, Pretoria, 13: 1-59. Coleman, L.C. and Kannan, K., 1918. Some scale insect pests of coffee in South India. Bulletin of the Department of Agriculture, Mysore State, Bangalore. Entomological Series, 4: 1-66. Danzig, E.M., 1965. The wax scale - Ericerus pela Chav. (Homoptera: Coccoidea) in the USSR. Zoologicheskii Zhurnal, 44: 537-546. [In Russian, English summary]. Danzig, E.M., 1980. Scale Insects of the Far East SSSR (Homoptera, Coccinea) with Phylogenetic Analysis of Scale Insect Fauna of the World. Nauka, Leningrad. 366 pp. [In Russian]. Dziedzicka, A., 1968. Studies on the morphology and biology Lecanium fletcheri Cockerell (Homoptera: Coccidae) and related species. Zoologica Poloniae, 18: 125-165. Dziedzicka, A. and Sermak, W., 1967. The variability of the dorsal-marginal glands in larvae II and females of Lecanium comi Bouch6 on Taxus baccata L. Rocznik Naukowo-Dydaktyszny WSP w Krakowie, Prage z Zoologii, 29:25-31. Ezzat, Y.M. and Hussein, N.A., 1969. Redescription and classification of the family Coccidae in U.A.R. (Homoptera: Coccoidea). Bulletin de la Socirt6 Entomoiogique d'Egypte (1967), 51: 359-426. Ferris, G.F., 1950. Report upon the scale insects coUected in China (Homoptera: Coccoidea). Part II. (Contribution no. 68). Microentomology, 15: 69-124. Fonseca, J.P. da, 1953. Contribuicao para o estudo do Coccus hesperidum L. (Hemiptera: Coccoidea). lEstudo Sistem~itico e Morphol6gico Brotrria, Lisboa, 22: 5-53, 97-114. Fonseca, J.P. da, 1973. Contribuicao ao conhecimento dos coccideos do Brasil (Homoptera: Coccoidea). Arquivos do Instituto Biologicao, S~o Paulo, 42: 247-261. 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. Gill, R.J., 1979. A new species of Pulvinaria Targioni Tozzetti (Homoptera: Coccidae) attacking ice plant in California. Pan Pacific Entomologist, 55: 241-250. G6mez-Menor Ortega, J., 1937. C6ccidos de Espana. Universidad de Madrid, Madrid. 432 pp. G6mez-Menor Ortega, J., 1948. Adiciones a los "C6ccidos de Espana". 2a nota. EOS, 24: 73-121. G6mez-Menor Ortega, J., 1958. Cochenillas que atacen a los frutales (Homoptera, Coccoidea): II. Familias Lecanidae y Margarodidae). Boletin de Patalogia Vegetal y Entomologia Agricola, Madrid, 23: 43-173. G6mez-Menor Ortega, J., 1960. Adiciones a los "C6ccidos de Espana". V. Superfamilias Coccoidea. EOS, 36: 157-204. Gonz~ilez, R.H., 1989. Insectos y Acaros de lmportanicia Agricola y Cuarentenaria en Chile. Universidad de Chile, Santiago. 310 pp. Green, E.E., 1904. The Coccidae of Ceylon. Dulau and Co., London, 3: 171-249. Green, E.E., 1909. The Coccidae of Ceylon. Dulau and Co., London, 4: 250-344. Green, E.E., 1928. Observations on British Coccidae. XI. With descriptions of new species. Entomologist's Monthly Magazine, 64:20-31. Hamon, A.B. and Williams, M.L., 1984. The Soft Scale Insects of Florida. Arthropods of Florida and Neighboring land areas. Florida Department of Agriculture and Consumer Services, 11 : 194 pp. Hodgson, C.J., 1970. A new species of Coccus (Homoptera: Coccoidea) from Malawi. Entomologists' Monthly Magazine, 106: 35-53. Hodgson, C.J., 1971. The species assigned to the genus Ceroplastodes (Homoptera: Coccoidea) in the Ethiopian Region. Journal of Entomology (B), 40:49-61. Hodgson, C.J., 1991. A redescription of Pseudopulvinaria sikk~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 Press, Wallingford. 640 pp. Husseiny, M.M. and Madsen, H.F., 1962. The life history of Lecanium kunoensis Kuwana (Homoptera: Coccidae). Hilgardia, 33: 179-203. Kawai, S. and Tamaki, Y., 1967. Morphology of Ceroplastes pseudoceriferus Green with special reference to the wax secretion. Applied Entomology and Zoology, 2: 133-146. Kawecki, Z., 1958a. Studies on the Genus Lecanium Burm. IV. Materials to a monograph of the Brown Scale, Lecanium corni Bouchr, Marchal (Homoptera, Coccoidea, Lecaniidae). Annales Zoologici, 4: 125-230. Kawecki, Z., 1958b. Studies on the Genus Lecanium Burro. Part V. The Nut or Thorn Scale - Lecanium coryli (L.) sensu Marchal nee Sulc (Homoptera, Coccoidea, Lecaniidae). Polskie Pismo Entomologiczne, 27: 40-69. Koteja, J., 1966. Studies on morphology and biology of Luzulaspisfrontalis (Green) (Homoptera, Coccoidea). Polskie Pismo Entomologiczne, 34:177-184. Koteja, J., 1969. Psilococcus parvus Borchsenius (Homoptera: Coccoidea) - morphology, biology and taxonomy. Acta Zoologica Cracoviensia, 14: 21-41. Koteja, J. and Rosciszewska, M., 1970. Revision of the genus Parafairmairia Cockerell (Homoptera: Coccoidea). Polskie Pismo Entomologiczne, 40: 233-265. Kuwana, S.I., 1902. Coccidae from the Galapagos Islands. Journal of the Entomological Society of New York, 10: 28-33. Kuwana, S.I., 1923. The Chinese white-wax scale, Ericerus pela Chavarmes. Philippine Journal of Science, 22: 393-406.
48
Morphology Lambdin, P.L. and Kosztarab, M., 1973. Studies on the morphology and systematics of scale insects. No.5. Virginia Polytechnic Institute, Research Division Bulletin, 83" 1-110. Leonardi, G., 1920. Monografia delle Coccinigle Italiane. E. Della Ton-e, Portici (Naples), VII. 555 pp. Lepage, H.S. and Piza, M.T., 1941. Redescription of "Neolecanium silveirai (Hempel)" (Homoptera Coccidae), a serious pest of vine, and its control. Arquivos do Institute Biologico, Sao Paula, 12: 21-26. [In Portuguese, English abstract]. Manawadu, D., 1986. A new species ofEriopelris Signoret (Homoptera: Coccidae) from Britain. Systematic Entomology, 11 : 317-326. Man:hal, P., 1909. Contribution a l'6tude des coccides de 1' Afrique occidentale. Memoires de la Soci6t6 Zoologique de France, 22: 165-182. Miller, D.R., 1991. Superfamily Coccoidea. In: Stehr, F.W. (ed.): Immature Insects, Vol. 2, Kendall/Hunt Publishers, Iowa. pp. 90-106. Morrison, H. and Morrison, E.R., 1922. A redescription of the type species of the genera of Coccidae based on the species originally described by Maskell. Proceedings of the United States National Museum, Washington, 60: 1-20. Phillips, J.H.H., 1962. Description of the immature stages of Pulvinaria vitis (L.) and P. innumerabilis (Rathvon) (Homoptera: Coccoidea), with notes on the habits of these species in Ontario, Canada. Canadian Entomologist, 94: 497-502. Pollet, D.K., 1972. Morphology, biology and control of Ceroplastes ceriferus Fabricius and Ceroplastes sinensis Del Guereio in Virginia, including a redescription of Ceroplastes floridensis Comstock. Ph.D. dissertation, Virginia Polytechnic Institute and State University, Blacksburg, VA. 210 pp. Qin, T.K. and Gullan, P.J., 1989. Cryptostigma Ferris: a coccid genus with a strikingly disjunct distribution (l-lomoptera: Coccidae). Systematic Entomology, 14: 221-232. Quintana, F.J., 1956. Pulvinaria mesembryanthemi (Vallot) (Homoptera Stern.) nueva cochinilla para la fauna Argentina y sus Zooparasitos. Revista de la Facultad de Agronomia Argentina, La Plata, 32:75-110. Ray, C.H. Jr. and Williams, M.L., 1980. Descriptions of immature stages of Pseudophilippia quaintancii (Homoptera: Coccoidea: Coccidae). Annals of Entomological Society of America, 73: 437-447. Ray, C.H. Jr. and Williams, M.L., 1981. Redescription and lectotype designation of tesselated scale, Eucalymnatus tessellatus (Signoret) (Homoptera: Coccidae). Proceedings of the Entomological Society of Washington, 83: 230-244. Ray, C.H. Jr. and Williams, M.L., 1982. Description of the immature stages of Protopulvinaria pyriformis (Cockerell) (Homoptera: Coccidae). The Florida Entomologist, 65: 169-176. Ray, C.H. Jr. 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. l~eh~i~ek, J., 1960. Fauna puklic (Coccidae) Slovenska. Biologicke Prace 6, 12: 1-89. Richards, W.R., 1958. Identities of species of Lecanium Burmeister in Canada (Homoptera: Coccoidea). Canadian Entomologist, 90:304-313. Ringuelet, E.J., 1924. Contribuci6n al estudo de la "Pulvinariaflavescens": Br~thes. Anales de la Sociedad Cientifica Argentina, 97:61-80. Sankaran, T., 1962. The life history and biology of the wax-scale, Ceroplastes pseudoceriferus Green (Coccidae: Homoptera). Indian Journal of Entomology, 24: 1-18. Schmutterer, H., 1952. Die 0kologie der Cocciden (Homoptera, Coccoidea) Frankens. 2. Abschnitt. Zeitschritt fiir Angewandte Entomologie, 33: 544-584. Schmutterer, H., 1954. Zur Kenntnis einiger wirtschat~lich wichtiger mittleuropiiischer Eulecanium- Arten (Homoptera: Coccoidea: Lecaniidae). Zeitschift fiir Angewandte Entomologie, 36: 62-83. Schmutterer, H., 1956. Zur morphologie, systematik und bionomie der Physokermes - Arten an Fichte (Homoptera, Coccoidea). Zeitschrif~ fiir Angewandte Entomologie, 39: 445-466. Sheller, B.J. and Williams, M.L., 1990. Descriptions, distribution and host-plant records of eight first instars in the genus ToumeyeUa (Homoptera: Coccidae). Proceedings of the Eatomological Society of Washington, 92: 44-57. Shmelev, G.P., 1975. Morphology and metamorphosis of the willow scale - Pulvinaria salicicola Borchsenius (Homoptera: Coccoidea: Coccidae). In: U.L. Shchetkii and N.N. Muminov (eds.). Entomolgyia Tadzhikistana. Donish, Dushanbe, pp. 86-93. [In Russian]. Silvestri, F., 1919. Contribuzioni all conoscenza degli insetii dannosi e die loro simbionti. V. La cocciniglia del nocciuolo (Eulecanium coryli L.). Bolletino del Laboratorio di Zoologia Generale e Agraria della R. Scuola Superiore d'Agricultura in Portici, 9: 240-334. Silvestri, F., 1920. Appendice. In: Leonardi (ed.). Monografia delle Cocciniglie Italianae. Della Torre, Portici. pp 501-539. Smith, R.H., 1944. Bionomics and control of the nigra scale, Saissetia nigra. Hilgardia, 16: 225-288. Snowball, G.J., 1970. Ceroplastes sinensis Del Guercio (Homoptera: Coccidae), a wax scale new to Australia. Journal of the Australian Entomological Society, 9: 57-66. Targioni TozJ.etti, A., 1895. Sopra une specie di lacca del Madagascar e sopra gli insetti the vi si trivano. I. Lacca del Madagascar (Gascardia madagascariensis n.g.; n. sp.). Bolletino della Societ~ Entomologica Italiana (1894), 26: 457-464. Tereznikova, E.M., 1981. Scale insects. Eriococcidae, Kermesidae, and Coccidae. Fauna Ukraini. Akademiya Nauk Ukrainskoi RSR. Institut Zoologii, Kiev, 20: 1-215. [In Ukrainian]. Vilar, J.M.D.S., 1951. Subdfdio para o estudo dos Ceroplastes spp. 0nsecta - Coccidae) de Portugal. I. Brot6ria Lisboa, 20:111-136. Vilar, J.M.D.S., 1952. Subdfdio para o estudo dos Ceroplastes spp. (insecta - Coccidae) de Portugal. II. Brot6ria Lisboa, 21: 1-62. Williams, M.L. and Kosztarab, M., 1972. Insects of Virginia no. 5. Morphology and systematics of the Coccidae of Virginia, with notes on their biology (Homoptera: Coccoidea). Virginia Polytechnic Institute and State University Research Division Bulletin, 74:215 pp.
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.
1.1.2.4
49
The Male Test
GARY L. MILLER and MICHAEL L. WILLIAMS
INTRODUCTION The word test comes from the Latin t e s t a meaning shell or pot and, as applied to the structure produced by the second-instar male soft scale, the term is apt. The test is formed from waxes secreted by wax producing glands and remains intact throughout the subsequent development of the prepupal, pupal and adult stages, during which it serves as a protective covering against harsh environmental conditions and natural enemies. The systematics and taxonomy of soft scales have been based almost entirely on the adult female, while other stages, including the male test, have often been neglected. There are several disadvantages in relying solely on morphological characters of the adult females for systematics. Adult females have to be mounted on microscope slides and examined with a compound microscope for proper study and identification. Since older or more mature females are often too heavily sclerotised for study, the correct timing of collection is essential for obtaining suitable material. Conversely, the male test does not usually require special preparation for study and the timing of collection is not as critical as with the adult female. Tests can be studied throughout the later part of the life cycle of the developing male and even long after the adult male has emerged. Additionally, the test can be examined with a dissecting microscope or even a hand lens. Use of male test characters for identification and even classification represents an underutilized area in scale insect study and offers some promising results. Although some early workers on scale insects described and illustrated the male test in their studies (e.g., Signoret, 1873; Newstead, 1903), it was Sulc (1932) who provided the basis for describing male test morphology. He concentrated on soft scales from Czechoslovakia and recognized a generalized test morphology in which he identified plates, sutures and corresponding accessory structures. He also developed a key for the identification of genera and species and provided detailed illustrations and descriptions of the included tests. Since Sulc's work, several workers have used the male test as a means for species identification (Kawecki, 1954; Richards, 1958; l~eh~i~ek, 1960; Miller and Williams, 1990).
APPEARANCE OF THE MALE TEST
The tests in Figs 1.1.2.4.1,B-J and 1.1.2.4.2,A-J illustrate the variety of suture patterns and differences in dorsal habitus for 96 species in 44 genera of Coccidae worldwide. The suture patterns of each test was determined by studying field collected specimens as well as reviewing published illustrations and descriptions. The male test varies in colour, texture and shape depending upon the species examined. The test is actually composed of true waxes, fatty acids and alcohols (Tamaki 1970). The colour
Section 1.1.2.4 references, p. 54
50
Morphology
The male test
51
may range from opaque amber to white or grey. Appearance and fragility of the test is also variable between species and can range from a glassy, nearly transparent, cover to a granular appearing cover, or it can even be covered by flocculent wax. All tests are delicate structures, but some are comparatively hard or rigid while others are extremely fragile. Tests may also exhibit ornate sculpturing with numerous projections (Fig. 1.1.2.4.1,I), or they may be nearly featureless (Fig. 1.1.2.4.2,1), elongate (Fig. 1.1.2.4.2,H2), rosette-shaped (Fig. 1.1.2.4.2,J) or rounded (Fig. 1.1.2.4.1,H2). In addition to this variation of the surface features and general shape, the test also exhibits a series of plates, corresponding sutures and accessory structures. A generalized test consists of 9 major plates, 12 corresponding sutures, and accessory structures that may include anal plates, parastigmal projections, a peripheral fringe and an anal cleft (Fig. 1.1.2.4.1,A). The presence of these accessory structures is often variable. The anal plates of each test (Fig. 1.1.2.4.1,AI5) correspond to the position of the anal plates in the second instar and are extremely fragile and so are often broken or missing. Parastigmal processes (Figs 1.1.2.4.1,A16 and 1.1.2.4.2,A2) correspond to the position of the spiracles of the second-instar male. These processes appear as small flocculent spheres and are not present in all species. A peripheral fringe of wax (Figs 1.1.2.4.1,A17 and 1.1.2.4.1,12) may surround the test margin and is found in some species ofEulecanium Cockerell and Rhodococcus Borchsenius. The opening of the anal cleft (Fig. 1.1.2.4.1,A8) is quite variable and often depends on the degree of overlapping of the caudal plates (Fig. 1.1.2.4.1,AI2).
Fig. 1.1.2.4.1. Tests of male Coccidae with suture pattern and dorsal habitus variation. A, generalized test: 1. anterolateral suture; 2. anterior transverse suture; 3. mediolateral suture; 4. lateral longitudinal suture; 5. posterior transverse suture; 6. posterolateral suture; 7. preanal suture; 8. anal cleft; 9. anterior plate; 10. anterolateral plate; 11. posterolateral plate; 12. caudal plate; 13. median plate; 14. posterior plate; 15. anal plate; 16. parastigmal processes; 17. peripheral fringe (redrawn from Miller and Williams, 1990); B, suture configuration of Lecanochiton minor Maskell; C, 1. suture configuration and 2. dorsal habitus of Paralecanium zonatum Green (redrawn from Green, 1904); D, 1. suture configuration of Maacoccus bicruciatus (Green); Maacoccus piperis (Green); Paralecanium expansum (Green); Paralecanium geometricum (Green); Paralecanium marginatum (Green); Paralecanium maritimum (Green); Paralecanium paradeniyense Green; Paralecanium planum (Green); 2. dorsal habitus of Paralecanium peradeniyense Green (redrawn from Green, 1904); E, suture configuration of Ceronema koebeli Green; Ctenochiton eucalypti Maskell; F, suture configuration of Parafairmairia gracilis Green; G, suture configuration ofMarsipococcus marsupialis (Green); H, 1. suture configuration of Coccus aequale (Newstead); Coccus hesperidum Linnaeus; Coccus ophiorrhizae (Green); Coccus pseudohesperidum (Cockerell); Lichtensia viburni Signoret; Megapulvinaria maxima Green; Mesolecanium nigrofasciatum (Pergande); Milviscutulus mangiferae (Green); Neolecanium cornuparvum (Thro); Parasaissetia nigra (Nietner); Pulvinaria aurantii Cockerell; Chloropulvinaria floccifera (Westwood); Pulvinariella mesembryanthemi (Vallot); Pulvinaria tessellata Green; Rhizopulvinaria armeniaca Borchsenius; Rhizopulvinaria arenaria Canard; Saissetia coffeae (Walker); Saissetia oleae (Olivier); Toumeyella liriodendri (Gmelin); 2. dorsal habitus and lateral silhouette of leaf form of M. nigrofasciatum (redrawn from Miller and Williams, 1990); 3. dorsal habitus and lateral silhouette of twig form of M. nigrofasciatum (Pergande) (redrawn from Miller and Williams, 1990); I, 1. suture configuration of Ctenochiton flavus Maskell; Ctenochiton viridis Maskell; Eulecanium caryae (Fitch); Eulecanium ciliatum (Douglas); Eulecanium tiliae (Linnaeus); Luzulaspis luzulae (Dufour); Luzulaspis scotica Green; Neopulvinaria innumerabilis (Rathvon); Palaeolecanium bituberculatum (Signoret); Parthenolecanium corni (Bouchr); Parthenolecanium pomeranicum (Kawecki); Parthenolecanium quercifex (Fitch); Philephedra lutea (Cockerell); Physokermes piceae (Schrank); Pulvinaria acericola (Walsh and Riley); Pulvinaria vitis (Linnaeus); Rhizopulvinaria artemisiae (Signoret); Toumeyella pini (King); 2. dorsal habitus of Eulecanium caryae (Fitch) (from Miller and Williams, 1990); J, 1. suture configuration of Rhodococcus rosaeluteae Borchsenius; Rhodococcus spiraeae (Borchsenius); 2. dorsal habitus of Rhodococcus rosaeluteae Borchsenius (redrawn from Borchsenius, 1957).
Section 1.1.2.4 references, p. 54
52
Morphology
The male test
53 Test sutures can usually be distinguished from the surrounding wax and appear as either opaque or translucent seams between overlapping plates or they are elevated and of a different texture. However, the true suture pattern is sometimes obscured in species that exhibit highly ornate tests (e.g., Ceroplastodes acaciae Cockerell, Fig. 1.1.2.4.2,G2). For these species, it may be necessary to observe the suture pattern from the smooth underside of the test. Here, the pattern can also be distinguished but without interference from the exposed surface ornamentation. The position of sutures seems to correspond with the position of dorsal tubular ducts of the second instar. The suture patterns may differ greatly from the pattern illustrated in the generalized test (Fig. 1.1.2.4.1,A). For example, additional sutures may further subdivide the plates or the plates may lack this subdivision due to a reduction in the number sutures. Some suture patterns are encountered with greater frequency than others. The most common patterns are: a single posterior transverse suture (Fig. 1.1.2.4.2,H1), a pattern which mirrors the generalized test (Fig. 1.1.2.4.1,H1) and a pattern which resembles the generalized test but lacks mediolateral sutures (Fig. 1.1.2.4.1,11). While suture patterns are usually very consistent, there is often some degree of intraspecific variation of the tests. Slight differences in sculpturing, colour or texture may be due to weathering or genetic variation, while other differences are host induced. For example, the test of Mesolecanium nigrofasciatum (Pergande) (Fig. 1.1.2.4.1,I-12) is ovoid and procumbent on leaves, but obovoid and elevated medially on twigs (Fig. 1.1.2.4.1,H3). The suture pattern of the leaf and twig forms is, however, the same. There is generally great interspecific variation in the number of plates, sutures and overall appearance of the test. However, some genera do exhibit similarities in appearance. For example, species of Eriopeltis Signoret have only a single posterior transverse suture (Fig. 1.1.2.4.2,H1) and many species of Paralecanium Cockerell (Figs. 1.1.2.4.1,C and 1.1.2.4.1,D) have multiple lateral sutures.
Fig. 1.1.2.4.2. Suture pattern and dorsal habitus variation in tests of male Coccidae. A, 1. suture configuration of Toumeyella cerifera Ferris; Toumeyella virginiana Williams & Kosztarab; 2. dorsal habitus of Toumeyella cerifera Ferris (from Miller and Williams, 1990); B, suture configuration of Platylecanium asymmetricum Morrison; C, 1. suture configuration of Philephedra crescentiae (Cockerell); Philephedra tuberculosa Nakahara & Gill; 2. dorsal habitus of Philephedra tuberculosa Nakahara & Gill (from Miller and Williams, 1990); D, suture configuration of Phyllostroma myrtilli (Kaltenbach); E, suture configuration and dorsal habitus of ToumeyeUa pinicola Ferris; F, 1. suture configuration and 2. dorsal habitus of Pulvinaria hydrangeae Steinweden (redrawn from Canard, 1969); G, 1. suture configuration and dorsal habitus of Ceroplastodes acaciae Cockerell (from Miller and Williams, 1990); H, 1. suture configuration of Cryptes baccatus (Maskell); Ctenochiton depressus Maskell; Ctenochiwn serratus Green; Didesmococcua koreanus Borchsenius; Didesmococcus unifasciatus (Archangelskaya); Drepanococcus cajani (Maskell); Eriopeltis coloradensis Cockerell; Eriopeltis festucae (Fonscolombc); Eriopeltis lichtensteini Signoret; Eriopelris sachalinensis Borchsenius; Eriopeltis stammeri Schmutterer; Eriopeltis varleyi Manawadu; lnglisia ornata Maskell; Paralecanopsisformicarum (Newstead);Pseudophilippia quaintancii Cockerell; Pulvinaria bigeloviae Cockerell; Sphaerolecanium prunastri (Fonscolombe); Scythia festuceri (.Sulc)" Toumeyella mirabilis (Cockerell); Toumeyella parvicornis (Cockercll); Vitrococcus conchiformis (Newstead); 2. dorsal habitus of Eriopeltis coloradensis Cockerell (from Miller and Williams, 1990); I, 1. suture configuration of Ceroplastes irregularis Cockerell; Ctenochiton spinosus Maskell; Ericerus pela (Chavannes); Eulecanium franconicum (Lindinger); Inglisia malvacearum Cockcrell; Nemolecanium abietis Borchsenius; Pulvinaria ericicola McConnell; 2. dorsal habitus of Nemolecanium abietis Borchsenius (redrawn from Borchsenius, 1957); J, 1. suture configuration of Ceroplastes ceriferus (Frabricius); Ceroplastes destructor Newstead; Ceroplastes japonicus Green; Ceroplastes nakaharai Gimpel; Ceroplastesrusci (Linnaeus); Vinsonia stellifera (Westwood); 2. dorsal habitus of Ceroplastes ceriferus (l=rabricius) (from Miller and Williams, 1990).
Section 1.1.2.4 references, p. 54
54
Morphology
Currently, male tests are known for less than 10% of the described species of Coccidae. There are several reasons for this" (1) many species of soft scales are wholly parthenogenetic or are facultatively parthenogenetic and, therefore, males are either not present or rarely occur, so that the chances of finding a male test for these species would be impossible or exceptional; (2) when males are present in a population, they are often ignored by the collector because of the emphasis on adult females for identification purposes. However, as more workers come to appreciate the potential of the male test for taxonomic purposes, it should become more than a passing curiosity. The study and description of additional species will not only be useful as a taxonomic tool, but may also prove helpful in determining and clarifying phylogenetic relationships within the Coccidae.
REFERENCES 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. Canard, M., 1969. La lignre male de Eupulvinaria hydrangeae (Horn. Coccidae). Annales de la Socirt6 Entomologique de France (N.S.), 5: 457-460. Green, E.E., 1904. The Coccidae of Ceylon, Part Ill. Dulau & Co., London, pp. 171-249. Kawecki, Z., 1954. Studies on the genus Lecanium Burm. Part II. The yew scale, Lecanium pomeranicum sp. n. and some related species (Homoptera, Coccoidea, Lecaniidae). Annales Zoologici, 16: 9-23. Miller, G.L. and Williams, M.L., 1990. Tests of male soft scale insects (Homoptera: Coccidae) from America north of Mexico, including a key to the species. Systematic Entomology, 15: 339-358. Newstead, R., 1903. Monograph of the Coccidae of the British Isles. II. Ray Society, London, 270 pp. Richards, W.R., 1958. Identities of species ofLecanium Burmeister in Canada (Homoptera: Coccoidea). The Canadian Entomologist, 90:305-315. l~eh~i~ek, J., 1960. Fauna puklic (Coccidae) Slovenska. Biologick6 Pr~ice, 6" 1-89. Signoret, V., 1873. Essai sur les Cochenilles ou gallinsectes (Homoptbres-Coccides). Annales de la Socirtd Entomologique de France (ser. 5), 3: 395-558. Suit, K., 1932. (~eskoslovenskd druhy rodu puklice (Gn. Lecanium, Coccidae, Homoptera). Die tschechoslowakischen Lecanium-Arten. Prhce Moravskd P~ffiodov~deckd Spole~nosti (Acta Societatis Scientiarum Naturalium Moravicae), 7: 1-135. Tamaki, Y., 1970. Studies on waxy coverings of Ceroplastes scale insects. Bulletin of the National Institute of Agricultural Sciences (Japan), Series C, 24:I-111.
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.
55
1 . 1 . 2 . 5 Chemistry of the Test Cover YOSHIO TAMAKI
INTRODUCTION Many species of scale insects (Homoptera: Coccoidea) present problems of general interest to insect physiologists and biochemists. Many, but not all, secrete or excrete a large bulk of material onto their body surface. The material, usually referred to as a test, cover or waxy covering, is believed to protect scale insects from the deleterious effects of weather and from natural enemies. This cover is also effective against the action of insecticide sprays to control pest species on economically important crops. On the other hand, the cover of particular species has been utilized as a source of useful materials to man (see Chapter 1.3.3.1) for many centuries. Typical examples are shellac from Kerria lacca (Kerr) (Tachardiidae) and Ibota wax from Ericerus pela (Chavannes) (Coccidae). This Section deals with the chemistry and biochemistry of the test or cover of female scale insects, with special reference to soft scales, Coccidae. RELATIVE WEIGHT OF THE TEST OR COVER The weight of the cover differs between species, ages and sexes. The males of all scale insects are holometabolous and only secrete the cover during the 2nd-instar nymphal stage. The females are all hemimetabolous and continuously secrete the test or cover until the adult stage and consequently sometimes form a bulky cover. The data on 3 species of Ceroplastes Gray indicate that the cover of the adult female comprises between 58 and 98% of an individuals' weight. Ceroplastes spp. are rather unique because their cover contains relatively large amount of aqueous material other than waxy substances. For instance, the aqueous material of the cover of C. pseudoceriferus Green [ = C. ceriferus] amounts to 77.2 % of the cover, so that the crude wax soluble in chloroform amounts to only 22.8 %. For C. rubens Maskell, these values are 8.7% and 91.3% respectively (Tamaki, 1970). The aqueous materials of the cover of Ceroplastes spp. were called honeydew by Hackman & Trikojus (1952). However, detailed studies on Ceroplastes spp. in Japan have shown that the aqueous material in the cover has a different origin to that of the honeydew excreted from the anus of aphids and scale insects and therefore the name "interior honeydew" was suggested by Tarnaki and Kawai (1966) for this aqueous material in the cover of Ceroplastes spp. The large amount by weight of the cover in species of Ceroplastes suggests that the cover is important in the life of these insects. On the other hand, no species of Pseudococcidae or Diaspididae secrete such a thick cover. Indeed, the cover of Pseudococcus comstocki (Kuwana) (Pseudococcidae) constitutes only 4-8 % of the body weight (Tamaki, 1970), while that of Aonidiella aurantii (Maskell) (Diaspididae) comprises only 0.85% of the body weight (Dickson, 1951). The wax materials extractable with benzene or chloroform from the covers of other Coccoidea are as
Section 1.1.2.5 references, p. 69
56
Morphology follows: 9.0 % forAsterococcus muratae Kuwana (Cerococcidae) (Kohno, 1933c), 23.5 % in Pulvinaria horii (Kuwana) (Coccidae) (Kohno and Maruyama, 1934) and 36.5 % in Unaspis yanonensis (Kuwana) (Diaspididae) (Kohno and Maruyama, 1936).
COMPOSITION OF THE WAXY MATERIALS IN THE COVER (1) Waxes The cover of many scale insects is composed of large amounts of waxy materials. Xray diffraction techniques applied to the covers of many scale insects have indicated the presence of long-chain lipid compounds (Tamaki and Kawai, 1969). In some species, the waxy material is the only constituent. The waxy substances in the covers of three Ceroplastes spp. from Japan amount to 18-98 % by weight. Few analyses have been made on the wax of tests of other Coccoidea, although these secretions have been analyze~ for two commercially important families of the Coccoidea, the lac insects (Tachardiidae) and the cochineal insect (Dactylopiidae) (Chibnall et al., 1934a; Warth, 1956). Most of the data before the 1950's depended on classical analytical methods and the separation of waxy homologues was not sufficient to isolate individual substances from these mixtures. Since the 1960's, analytical methods for lipid materials have greatly improved and the general use of gas-liquid chromatography (GLC) has revealed that most of the earlier data needs to be reinvestigated. By using a detailed melting point analysis, Chibnall et al. (1934b) suggested that the ceryl cerotate isolated from the wax of Ceroplastes ceriferus (Fabricius) was composed of several esters; that is the ceryl alcohol part of the ester consisted of 40% C26-, 40% C28- and 20% C30-alcohols. Similarly, the cerotic acid part of the ester was a mixture of C26-, C28- and C30-acids. The same is true of melissyl alcohol, a C31-alcohol. This was considered to be a mixture of 20% C30-, 40% C32- and 40 % C34-alcohols. Higher fatty acids in the wax of C. destructor (Newstead) seemed to be a mixture of C26- and C28-acids (Hackman, 1951; Gilby, 1957). Recent developments in analytical methods has enabled reinvestigation of formerly isolated unique waxy substances. Psyllostearic acid (C33), isolated from the wax of Psylla alani by Chibnall et al. (1934b) and also from Ceroplastes pseudoceriferus and C. japonicus Green by Kohno (1933a,b), was not confirmed by gas-chromatographic analyses (Tamaki, 1966, 1970). Kohno (1932) isolated melissic acid (C31) with ceryl alcohols from Ceroplastes rubens Maskell, but these waxy fatty acids and fatty alcohols have not been confirmed in the cover of C. rubens by new analytical methods (Tamaki and Kawai, 1968; Tamaki, 1970). The crude waxes of the covers of C. pseudoceriferus, C. japonicus and C. rubens were analyzexl using GLC (Tamaki, 1966; Tamaki and Kawai, 1968). The saponifiable part of the ethanol insoluble and petroleum ether soluble fraction of the crude wax in the cover of C. pseudoceriferus made up 34.2 % of the crude wax and the unsaponifiable part of the same fraction made up 27.1% of the crude wax. Other fractions, such as the aqueous ethanol soluble fraction and the alkaline aqueous ethanol fraction, showed resinous material and consisted of 29.5 % of the crude wax. GLC analyses of the saponifiable fraction indicated that the major acids were C28 (2.6 % of crude wax), C30 (22.6% of crude wax) and C32 (6.1% of crude wax). However, the unsaponifiable matter was mostly composed of cyclic (and/or branched chain) compounds (24.4 % of crude wax) with a small amount of C26-alcohol (2.7 % of crude wax). Thus, the wax of C. pseudoceriferus is mostly composed of the esters of straight chain higher fatty acids and cyclic alcohols. True waxes, that is esters of higher fatty acids and higher fatty alcohols, seemed not to be the major component of the cover of this species (Tamaki, 1966, 1970). Hashimoto and Mukai (1965) reported ceryl alcohol (C26) and cerotic acid (C26) as major components of the saponified wax material of C. pseudoceriferus. The C26-acid moiety of this report is not consistent with other
Chemistry of the test cover
57
reports. Hashimoto et al. (1967b) also suggested that the true wax of C. pseudoceriferus amounted to about 16 % of total wax esters in the cover. The fatty acids C28, C30 and C32 have also been identified in the saponifiable fraction of the crude wax of Ceroplastes albolineatus Cockerell in Mexico (Rios and Colunga, 1965). Comparison of the composition of the cover of C. pseudoceriferus, C. japonicus and C. rubens has indicated an interesting relationship in their chemical composition. The major higher fatty acids were similar in the three species, but the ratio of the components differed. Ceroplastes rubens showed relatively larger amounts of fatty acid of large molecular weight as compared with C. pseudoceriferus, while those of C. japonicus were intermediate between the other two species (Tamaki and Kawai, 1968; Hashimoto et al., 197 lb). Ibotacerotic acid (C27) and ibotaceryl alcohol (C27) were isolated from the waxy substance of Ericerus pela (Koyama, 1934a,b); ibotaceryl alcohol was also reported as a component of the waxy secretion of Icerya purchasi Maskell by Kohno and Maruyama (1935) and Mukai et al. (1965). However, these odd carbon number compounds have not been confirmed from the wax of E. pela (Tamaki, 1970), although about equal amounts of C26 and C28 were detected. Reinvestigation of the ibota (Pela) wax from the male test of E. pela indicated that 81.7 % was extractable with chloroform, and that the saponifiable and unsaponifiable fractions were 43.6 and 52.3 % of the crude wax. GLC analyses of methyl esters of the saponifiable fraction indicated the presence of C26and C28-acids, amounting to 66.1% of the saponifiable fraction. In addition, C24- and C30-acids were also important components. These four acids comprised 92.8 % of the saponifiable fraction. The corresponding 4 alcohols were found to be major components of the unsaponifiable fraction of the crude wax. C26- and C28-alcohols comprised 44.1% of the unsaponifiable fraction (Tamaki, 1970; Hashimoto and Kitaoka, 1971b). Takahashi and Nomura (1982) confirmed that the wax esters of E. pela were composed of hexacosyl hexacosanoate (55.2 %), hexacosyl tetracosanoate (22.4 %) and hexacosyl octacosanoate (16.7 %). The comstock mealybug, Pseudococcus comstocki, secretes a relatively small amount of powdery wax on the body surface. The saponifiable fraction of this waxy material amounts to 81.1% of the total as methyl ester, while the unsaponifiable fraction constitutes only 10.4%. Major components of normal fatty acids in the saponifiable fraction for individuals reared on potato sprouts were C18 (16.5 %), C28 (36.1%) and C30 (8.6 %). The corresponding higher normal C28- and C30-alcohols were the major components in the unsaponifiable fraction. These two alcohols comprised 83.2 and 14.6 % ofthe fraction respectively (Tamaki, 1970). On the other hand, the bulky ovisacs produced by this mealybug consisted of waxy filaments and non-lipid strings. The saponifiable and unsaponifiable fractions of the waxy filaments were 43.2 and 44.4 % respectively, indicating the properties of true wax. Major fatty acids were C 18 (16.5 %), C28 (23.1%) and C30 (35.4%) while the major alcohols were C28 (7.9%), C30 (71.3%), C32 (16.6%) and C34 (2.9%), slightly different from that of the body wax (Tamaki, 1970). The margarodid, Drosicha corpulenta Kuwana, secretes waxy threads on the dorsal surface of the adult female. This wax was found to be composed of 82 % wax ester of chain length 52 formed by C26-alcohol and C26-acid (Hashimoto and Kitaoka, 1982). The remaining 12 % of the wax was a mixture of hydrocarbons. In the case of such Diaspididae as the peach white scale, Pseudaulacaspis pentagona (Targioni Tozzetti), the test cover is secreted as a hard scale. The chloroform extractable material from this cover was 35.0% and the remaining material was non-lipid insoluble matter (Tamaki, 1970). Similar non-waxy material amounting to about 50% has been recorded in the test of the Florida red-scale, Chrysomphalus aonidum (L.) (Ebstein and Gerson, 1971), and this was thought to be a polyphenol or melanin-like
Section 1.1.2.5 references, p. 69
58
Morphology
compound. These non-waxy materials have also been described as "proteineous N or "chitin-like" secretions (Dickson, 1951; Disselkamp, 1954). Saponification of the crude wax from the test ofP. pentagona yielded 49.5 % saponifiable and 49.2 % unsaponifiable fractions. The major fatty acids were C28 (25.9%) and C30 (60.3%) and the major alcohols C24 (15.4 %), C26 (37.7 %), C28 (28.4 %) and C30 (11.3 %) (Tamaki, 1970). Analytical data indicate that the wax esters from 10 species of Diaspididae were distributed between C40 and C68 (Hashimoto et al., 1971a). In their review on the biology and ecology of armored scales, Beardsley and Gonzalez (1975) summarized the compositions of several diaspidid scale coverings. (2) Hydrocarbons Hydrocarbons are not major components of the cover of scale insects. In the case of C. pseudoceriferus, C. japonicus and C. rubens, relatively small amounts of hydrocarbons with carbon numbers ranging from 27 to 33 were detected in the unsaponifiable fractions of ethanol insoluble crude wax; of these, C29- and C31-hydrocarbons were the major components (Tamaki and Kawai, 1968; Tamaki, 1970; Hashimoto et al., 1971b). In the case of Ericerus pela, hydrocarbons comprise only 0.77 % of the waxy secretion, of which C29, C31 and C33 amount to 77.8 % (Takahashi and Nomura, 1982). A few data from the analyses of the complete body (i.e. true body plus cover) have indicated the presence of C31-hydrocarbon in Tachardina theae Green (Tachardiidae) (Kohno and Maruyama, 1938b), C45- and C46-hydrocarbons in Asterococcus muratae Kuwana (Cerococcidae) (Kohno, 1933c), and C26-monounsaturated hydrocarbon in Pulvinaria horii Kuwana (Coccidae) (Kohno and Maruyama, 1934). White wax secreted by the adult female of the margarodid Drosicha corpulenta Kuwana is comprised of 18 % hydrocarbons, of which n-alkanes form 70.5 % and 2methylalkanes 27.6%. "rhe major components were C28- and C29-hydrocarbons (Hashimoto and Kitaoka, 1982). There have been many studies on cuticular waxes of insects (Wigglesworth, 1957; Beament, 1964) and one important function suggested for the cuticular wax is water regulation (Bergmann, 1938; Wigglesworth, 1945; Beament, 1945; Lees, 1947; Holdgate and Seal, 1956). Major components of general insect wax deposited on the epidermis are hydrocarbons (Gilby and Cox, 1963; Louloudes et al., 1962), except in a few cases, such as the powdery wax on the nymphal body surface of Samia cynthia ricini (Lepidoptera: Saturniidae) (Bowers and Thompson, 1965). In contrast to the cuticular wax of most insects, the test covers of soft scales consists principally of true waxes or esters of fatty acids and terpene alcohols. (3) Resinous materials or terpenoids In addition to higher aliphatic compounds, cyclic compounds are important components of the covers of various scale insects. The major components of the cover of Ceroplastes pseudoceriferus seemed to be esters of higher fatty acids and cyclic alcohols. GLC analyses of the crude wax indicated the presence of at least 12 compounds in the cyclic alcohol fraction, and 13 compounds in the cyclic acid fraction (Tamaki, 1966, 1970). Kohno and Maruyama (1937a, 1937b, 1938a) isolated several diterpene cyclic alcohols and acids from the cover of C. rubens, such as rubenol, rubabietic acid and rubenic acid. Recent advances in analytical techniques have enabled us to elucidate the detailed chemical structure of various cyclic compounds. From the waxy material of Ceroplastes albolineatus Cockerell from Mexico, a series of macrocyclic, bicyclic and tricyclic sesterterpenoids have been isolated. These are albocerol (Fig. 1.1.2.5.1.1), albolineol(2), ceralbol(3), ceroplastol-I(4), ceroplastol-II(5), ceroplasteric acid(6) and albolic acid (7)(Rios and Colunga, 1965; Rios and Quijano, 1969; Veloz et al., 1975; Rios et al., 1974; Calderon et al., 1978; Rios and Gomez, 1969). A number of related sesterterpenoids have also been found in the crude waxes of C. pseudoceriferus. These are ceriferol (Fig.l.l.2.5.2.8), ceriferic acid(9), a-cericerene(10), c~-cericerol-I(ll),
Chemistry of the test cover
59
ceriferol-I(12), cericerol-I(13), cerifedc acid-I(14), cericeroic acid(15), cericerene(16), 13-methoxy-eericerene(17), 13-ethoxy-cericerene(18), cericerol-II (Fig. 1.1.2.5.3.19), 15,23-dilaydroxy-cericerene(20), 18-dihydro-19-hydroxycericeroic acid(21) and two I
2
HO (I} albocelol 0
OH
OH
(2) albollneol
R (3) ceralbol (R=CH2OH)
R (4) ceroplastol-I (R=CH2OH) (7) albolic acld (R=COOH)
(5) ceroplastol-II (R=CH2OH) (6) ceroplasterlc acid (R=COOH)
Figure 1.1.2.5.1. Structureof some macrocyclic,bicyclic and tricyclic sesterterpenoidsfrom the wax test of Ceroplastes albolineatusCockerell. other sesterterpenoid acids (22, 23) (Miyamoto et al., 1979; Naya et al., 1980; Pawlak et al., 1983). In addition to these sesterterpenoids, tricyclic diterpenoid acids such as sandaracopimarie (Fig. 1.1.2.5.4.24), isopimaric(25), palustric(26), abietic(27), neoabietic(28), dehydroabietic(29), 7-hydroxy-dehydroabietic(30)and 7-oxodehydroabietic(31) acids, and a series ofbicyclic diterpenoid alcohols (32-35) were characterized in the crude waxes of C. pseudoceriferus (Miyamoto et al., 1980). Analyses of esters in the cover of this species indicated that the acetone insoluble true wax was composed of C16- to C34-fatty acids and C26-alcohol; in addition, two acetates of C26- and C28-alcohols were detected (Miyamoto et al., 1980). On the other hand, the cyclic wax in this species was found to consist of mono- and di-esters of bicyclic diterpenoid alcohols and C10- to C20-saturated acids. Sesterterpenoid esters consisted of C28- to C32-acids and cericerol-I, while C10- to C14-acids linked to cericerol-II were also detected in C. pseudoceriferus (Miyamoto et al., 1980). Tricyclic sesterterpenoids, such as floridenol (Fig. 1.1.2.5.5.36), 5-c~-hydroxyfloridenol(37), flocerol(39), floceric acid(40), floridenone(38) and flocerene(41) were identified from the cover of C. japonicus (Naya et al., 1981). Other tricyclic and tetracyclie sesterterpenoids, such as cerorubenic acid-I (Fig. 1.1.2.5.6.42), cerorubenic acid-II(44), cerorubenic acid-III(46), cerorubenol-I(43), cerorubenol-II(45) and
Section 1.1.2.5 references, p. 69
60
Morphology
cerorubenol-III(47) were also isolated and characterized from the cover of C. rubens. These compounds are the first representatives of a series having the tricyclo[8.4.1.0]pentadecane and tetracyclo[9.4.0.0.0]pentadecane skeletons (Tempesta et al., 1983). In addition to these higher terpenoids, 31 volatile sesquiterpenes have been detected in the secretions of C. pseudoceriferus and C. rubens. These volatile components comprise 0.59% of the cover of C. pseudoceriferus and 0.25 % of the cover of C. rubens (Naya et al., 1978).
/ R2
RI (8) cerlferol (9) cerlferic acid
CH2OH COOH
(I0)
(~-cericereneCH3
(11)
(~-cerlcerol-I
CH3 CH3
I
(12) (13) (14) (15) (16) (17) (18) Fig.
1.1.2.5.2.
cerfferol-I cericerol-I ceriferic acld-I cericeroic acid cericerene 13-methoxy-cericerene 13-ethoxy-cericerene Structure
of
some
CH3 CH3 CH2OH
2
RI CH2OH CH3 COOH CH3 CH3 CH3 CH3
sesterterpenoids
R2 CH3 CH2OH CH3 COOH CH3 CH3 CH3 from
the
crude
R3 H H H H H OCH3 OCH2CH3 waxes
of
Ceroplastes
pseudoceriferus Green.
It has been suggested that some terpenoid components play a role as kairomones for Anicetus beneficus Ishii & Yasumatsu (Hymenoptera, Encyrtidae), a parasitoid of Ceroplastes spp. This wasp appeared to utilize a mixture of sesterterpenoids and diterpenoids as a chemical stimulus when ovipositing in its host scale insects. Biological assays indicated that cerorubenol-I, cerorubenol-II, cerorubenol-III, ceriferol, and ceriferol-I individually stimulated the ovipositional behavior of the wasp. However, the activity of these individual compounds was not as strong as the crude extract
61
Chemistry of the test cover
additional components may be essential for eliciting the complete behavior of the wasp with regard to host finding and oviposition. In the case of diaspidid scale insects, wax esters of Unaspsis yanonensis seem to be utilized as kairomones in the host f'mding and oviposition behavior of Aphytis yanonensis DeBach & Rosen (Hymenoptera, Aphelinidae) (Takahashi et al., 1990). In addition, an ester of tyrosine and caffeic acid in the cover of the California red scale, Aonidiella aurantii (Maskell) (Diaspididae), was identified as a kairomone for the host f'mding and oviposition by Aphytis melinus (Daniel and Millar, 1992). 1
2
OH (19) cerlcerol-II {20) 15,23-dlhydroxycerlcerene
R1 CH3 CH2OH
R2 CH2OH CH3
COOH
H (21) 18-dlhydro- 19-hydroxycerlcerolc acid
HOOC.,.~ ..~ COOH
(22)
(23)
Fig. 1.1.2.5.3. Structure of further sesterterpenoids from the crude waxes of Ceroplastes pseudoceriferus Green. In addition to soft scales, the lac insects (Tachardiidae) are also well known as secreters of resinous materials. Lac production is an important industry in India and Thailand. The crude preparation of the secreted materials, the so-called seed lac, has been exported to developed countries. Various fractions of seed lac are still an important material for some high technology industries. Brown (1975) reviewed the
Section 1.1.2.5 references, p. 69
Morphology
62
chemical composition of lac resin and listed 12 compounds. He also stressed the necessity of further extensive studies to determine the chemical structure of each component.
"'COOH (24)
"COOH
(25)
(26)
L.
L. ~,,.COOH~/~
""COOH (27)
(28)
(29)
I
,OH
"COOH 9
OH
"'COOH
(30)
0
(31)
(32)
OH 2<,, v (33)
oH
~OH
Ho , (34)
(35)
Figure 1.1.2.5.4. Structure of some tricyclic diterpenoid acids and bicyclic diterpenoid alcohols from the wax test of Ceroplastespseudoceriferus Green.
(4) Pigments Various kinds of pigments are produced by scale insects and some were important commercial dyes before the advent of synthetics. For example, carmine is extracted from the cochineal scale, Dactylopius coccus Costa, which feeds on Opuntia cacti, while Venetian red comes from the kermesid, Kermes ilicis, on Quercus coccifera Linnaeus. According to Brown (1975), all known pigments of scales are polyketide anthraquinones, sometimes condensed further with amino-acid or carbohydrate moieties. Chemical structures such as erythrolaccin (Fig. 1.1.2.5.7.48), isoerythrolaccin(49), desoxyerythrolaccin(50), ceroalbolinic acid(51), laccaic acids A(62), B(63), C(64), D(52) and E(65), kermesic acid(53), carminic acid(54), emodin(55), 4-hydroxyemodin(56), 7-acetylemodin(57), W-hydorxyemodin(58), 7-acetyl-4-hydroxyemodin(59), 5,Wdihydroxy-emodin(60), endocrocin(61) and cochenillic acid (66) from the dactylopiids
Chemistry of the test cover
63
Dactylopius coccus and D. cacti, the kerriid Kerria lacca, eriococcid Eriococcus sp. and coccids Ceroplastes albolineatus, C. rubens and Cryptes baccatus (Maskell) have been proposed. A number of anthraquinones (Fig. 1.1.2.5.7.55-61) and a bianthrone glucoside (54) have also been identified as pigments from an Australian Eriococcus spp. and an asterolecaniid Callococcus acaciae (Maskell) (Brown, 1975; Banks et al., 1976a,b).
Ho HO
(36) florldenol
(37) 5-~-hydroxy-florldenol
R
(38) floridenone
-J
(39) flocerol (R=CH2OH) (40) floceric acid (R=COOH) (41) flocerene (R=CH3)
Figure 1.1.2.5.5. Structure of some tricyclic sesterterpenoids from the wax test of Ceroplastes japonicus Green.
(5) Other components Several unique lipid substances have frequently been detected as components of the waxy materials in the cover of scale insects. 13-oxodotriacontanoic acid (13-keto-C32acid) was reported in a wax obtained from a commercial source of the cochineal insect, D. coccus (Chibnall et al., 1934a). This has since been confirmed and the wax was found to be a ester of 13-keto-C32-acid and 15-keto-C34-alcohol (Meinwald et al., 1975). A wax ester of another cochineal insect species, D. confusus Cockerell, consisted of 11-keto-C30-acid and 15-keto-C34-alcohol (Meinwald et al., 1975). A unique dioic acid, tetradeca-l,14-dioic acid, was isolated and identified from the powdery wax secreted onto the body surface of the comstock mealybug, Pseudococcus comstocki (Tamaki, 1968). This dioic acid made up from 10.4 to 17.9% of the fatty acid fraction of the powdery wax, 2.5 % of the wax in the egg sac and 8.5 to 13.2 % of the fatty acid fraction of the body lipids (Tamaki, 1970).
COMPOSITION OF BODY LIPIDS Since some of the principal constituents of the wax material secreted by scale insects are esters of higher fatty acids, it is of interest to know the lipid composition of the
Section 1.1.2.5 references, p. 69
Morphology
64
H
-I
""H H
H
LR
""H H
R
(44) cerorubenlc acld-ll (R=COOH) (45) cerorubenol-ll (R=CH2OH)
(42) cerorubenlc acld-I (R=COOII) (43) cerorubenol-I (R=CH2OH)
H
9
"
R
H
(46) cerorubenlc acid-Ill (R=COOH) (47) cerorubcnol-lll (R=CH2OH) Figure 1.1.2.5.6.
Structure of some tricyclic and tetracyclic sesterterpenoids from the wax test of
Ceroplastes rubens Maskell.
insect body, which is considered to be a possible site of synthesis of these higher fatty acids. The chemical composition of body lipids of C. pseudoceriferus, C. japonicus and C. rubens were reported by Hashimoto and Mukai (1965), Tamaki and Kawai (1967) and Hashimoto et al. (1968a, 1969). The total body lipid content of adult female of C. pseudoceriferus, C. japonicus and C. rubens was 26.6, 12.8 and 10.4 % respectively, on a wet weight basis. Reported data on the body lipids ofhemipterous insects range from 5.2 to 20.0% on a wet weight basis (Fast, 1964) and, therefore, the value of C. pseudoceriferus is one of the highest in the Hemiptera. A large part of the total lipid, from 80 to 95 %, is neutral lipids, of which the major component is triglycerides. Fatty acids, particularly esterified acids, are the principal components of the total lipid; i.e. saponifiable matter contributes 83.2, 72.2 and 60.7 % of the total body lipid of C. pseudoceriferus, C. japonicus and C. rubens respectively. A small amount of free fatty acids (0.8-1.9%) was also detected in the body lipid. Unsaponifiable matter of the neutral lipid, around 2 % of the body lipid of these scale insects, consisted largely of hydrocarbons and alcohols (Tamaki and Kawai, 1967). The major triglycerides of C. pseudoceriferus were C30, C32 and C34; these were believed to be tricaprin, laurodicaprin and caprodilaurin (Hashimoto et al., 1968b). GLC analyses have indicated that the C18-series acids and the 14 fatty acids, ranging from C8 to C20 in the free fatty acid fractions, made up between about 66 to 79 % of these fractions. In the esterified fatty acid fractions, 10 acids ranging from C8 to C20 were detected in the three Ceroplastes species and patterns of these acids in the three species closely resembled each other, but were quite different quantitatively from those of the free acids. Of 10 acids, capric (C10) and lauric (C12) acids were dominant and the sum of the two accounted for over 75 % of the esterified fatty acid fractions of the three species. As 98-99% of the total fatty acids (free and esterified) consisted of esterified acids, the chemical nature of the esterified acids would strongly characterize the total fatty acids in the body lipids of the three species (Tamaki and Kawai, 1967). C10- and C12-acids were found to be the major fatty acids of body lipids of several other scale insects, such as the coccids Pulvinaria horii and Parthenolecanium corni (Bouchr), the ceroccid Asterococcus muratae and the pseudococcid Phenacoccus pergandei Cockerell (Hashimoto et al., 1967a, 1970). Trilaurin is the major component of egg lipids of P. horii and is 97 mole % of the total triglyceride of
65
Chemistry of the test cover
R
~2
O
I
~
HO T R6
OH
R3
TT-R, 0
Rs
R2
R3
R4
R5
(50) desoxyerythro-
R1 H H H
CH3 CH3 CH3
H OH H
OH OH OH
H H H
OH H H
laccin {51) ceroalbolinic acid (52) laccaic acid D {53) kermeslc acid (54) carminic acid (55) emodin (56) 4-hydroxyemodin {57) 7-acetylemodin
COOH COOH COOH COOH H H H
CH3 CH3 CH3 CH3 OH OH OH
OH H H C6Hl105 H H COCH3
OH OH OH OH CH3 CH3 CH3
H H OH OH H H H
H H H H H OH H
OH OH
H COCH3
CH2OH CH3
H H
H OH
OH
H
CH2OH
H
OH
OH
COOH
CH3
H
H
(48) erythrolaccin (49) isoerythrolaccin
{58) c0-hydroxyemodin H (59) 7-acetyl-4H hydroxyemodin (60) 5, c0-dihydroxyH emodin (61) endocrocin H
CH2R H
HOOC O O O C O
(62) (63) (64) {65)
laccalc laccalc laccaic laccaic
acid acid acid acid
OH
~ OH R CH2NHCOCH3 CH2OH CH(NH2)COOH CH2NH2
A B C E
COOH H O ~ c o 0
H
COOH {66} cochentlllc acid
Fig. 1.1.2.5.7. Structure of some compounds isolated from the pigments present in some Coccoidea.
Section 1.1.2.5 references, p. 69
66
Morphology the egg lipid (Hashimoto et al., 1968c). On the other hand, the major fatty acids of body lipids in several scale insects, such as the diaspidids Pseudaulacaspis pentagona and Unaspis euonymi, the coccids Eulecanium cerasorum Cockerell and Ericerus pela, the lecanodiaspid Lecanodiaspis quercus Cockerell and the margarodid Icerya purchasi, were reported to belong to the C16- and C18-series (Hashimoto and Kitaoka, 1971a). Analytical data on the body lipids of 30 insect species have indicated that the dominant fatty acids were generally of the C16- and C18-series, with the exception of those of aphids, in which the main fatty acid was myristic acid (C14) (Fast, 1964). Thus, the fatty acid composition of the body lipid of Ceroplastes spp. and other scale insects seemed to be similar to that of aphids, another important group of Homoptera; both scale insects and aphids show a high content of fatty acids from C10 to C14 compared with the C16- and C18-acids in other insects. An homologous series higher than C20-acid could not be detected in the body lipids of Ceroplastes spp. Since the principal fatty acid in the wax of their waxy cover is a 30-carbon fatty acid (Tamaki, 1966; 1970), it is reasonable to assume that synthesis of the 30-carbon acid and subsequent synthesis of wax in the cover takes place in a tissue, probably a wax gland or related tissue of epidermal origin, closely connected with the exterior, so that the synthesized wax would then be secreted onto the dorsal surface of the scale insects (see Section 1.1.2.7).
COMPOSITION OF THE AQUEOUS MATERIALS IN THE TEST COVERS
(1) The two kinds of "honeydew" in scale insects Hackman and Trikojus (1952) referred to the aqueous component in the cover of three Ceroplastes spp., namely C. destructor, C. ceriferus and C. rubens, as "honeydew". Gilby and Alexander (1957) also used the word "honeydew" for the aqueous constituent in the cover of C. destructor. However, detailed observations on the Japanese species of Ceroplastes have shown that the aqueous constituents in their tests are different from those in the "real" honeydew excreted from their anus (Tamaki, 1963). As the use of the term "honeydew" to describe both the aqueous components in the cover and those dropped from the anus is confusing, Tamaki (1970) coined the terms "interior honeydew" for that from the test cover and "dropped honeydew" for that eliminated from the anus. (2) Amino acid composition The amino acids in the "interior honeydew" of the test of C. pseudoceriferus feeding on tea plants were alanine, arginine, aspartic acid, cysteine, glutamic acid, glycine, leucine (and/or isoleucine), lysine, phenylalanine, serine, threonine, tyrosine, theanine and valine. Eight amino acids were detected from the anal "dropped honeydew" of the same species off the tea: alanine, aspartic acid, glutamine, glutamic acid, glycine, leucine (and/or isoleucine), theanine and valine. The amino acid composition of these "honeydews" differed with the host plants on which the scale insects fed. When the scale insect was reared on a pumpkin, several additional amino acids were detected in both the "interior'' and the "dropped honeydew" (Tamaki, 1964a; Tamaki and Kawai, 1966; Tamaki, 1970). (3) Carbohydrate composition The carbohydrates in the "interior honeydew" of C. pseudoceriferus also differed in their composition between host plants (Tamaki, 1964b; Tamaki and Kawai, 1966; Tamaki, 1970). The carbohydrate composition of the "interior honeydew" from the test of individuals infesting different races of the tea plant also differed. Glucose, maltose, raffinose and stachyose were often detected in the "interior honeydew" of individuals on tea plants, but the carbohydrates in those feeding on pumpkin were fructose, glucose,
Chemistry of the test cover
67
sucrose, maltose, raff'mose and an unidentified sugar. It is noteworthy that the unique sugar alcohols, ribitol and mannitol, were always detected in the "interior honeydew" of insects feeAing on both tea and pumpkin. Ribitol was also reported in the "interior honeydews" of three species of Australian Ceroplastes scales (Hackman and Trikojus, 1952), and these authors suggested that the sugar alcohol was directly derived from the host plant. However, the sugar alcohols ribitol and mannitol from C. pseudoceriferus, were only detected in the "interior honeydews" from the test and not in the anal "dropped honeydew" and were only detected in trace amounts in the host plant juice, suggesting that the sugar alcohols could be metabolic products of these scale insects. (4) Possible function of "interior honeydew" Normal honeydew, i.e. the "dropped honeydew" eliminated through the anus, has been studied mostly from aphids, which feed on the phloem sap of their host plants and excrete aqueous droplets from the anus. The honeydew of aphids contains various amino acids and carbohydrates (Auclair, 1958, 1963; Gray, 1952; Lamb, 1959; Baron and Guthrie, 1960; Maltais and Auclair, 1952; Mittler, 1953). Based on the data from stylectomy of the aphid Tuberolachnus saligunus (Gmelin), Kennedy and Mittler (1953) found that the flow rate of phloem sap exudation from the cut end of the stylet was similar to the rate of honeydew exudation from the aphid anus. Kennedy and Mittler (1953) suggested that the phloem sap flows into the digestive tract of aphids under pressure from the phloem. Thus, the aphid passively feaxls on the phloem sap, selectively absorbing particular nutrients and then excreting the excess sap from the anus as honeydew. It is not known whether the same speculation could be applied to scale insects. The "interior honeydew" in the test cover of Ceroplastes species is quite different from the normal or "dropped honeydew", because the former is secreted from dermal glands on the dorsal surface and not from the anus. However, the composition of "interior honeydew" shows some similarity with "dropped honeydew". Comparison of the three species of Ceroplastes from Japan has shown that C. pseudoceriferus, which contains the largest amount of "interior honeydew", excreted the least volume of "dropped" honeydew, suggesting that some relationship might exist between the excretion of "interior" and "dropped" honeydews. Perhaps the "interior honeydew" has a similar function to that of "dropped honeydew". However, the aqueous "interior honeydew" is apparently one of the major components of the cover, because two-thirds of the test of C. pseudoceriferus is aqueous "interior honeydew" and about 95 % of this honeydew is water. Thus, the cover of C. pseudoceriferus is a wax-water mixture, which appears to form an effective barrier for the protection of the actual insect's body.
MODE OF SECRETION
(1) Changes in the composition of the cover during the growth The cover of C. pseudoceriferus changes qualitatively and quantitatively during growth and development (Tamaki, 1970). The weight of the cover and its two major components, the wax and aqueous materials ("interior honeydew"), increase with increasing weight of the actual insect's body but the relative production of the cover is greatest during the 3rd and early 4th (adult) instars. A striking change in the composition of the waxy covering occurs during nymphal development. In the 1st and 2nd instars, only wax material ("dry wax") is produced whereas the cover of the 3rdinstar nymphs and adult scales consists of both wax material and aqueous material ("wet wax ").
Section 1.1.2.5 references, p. 69
68
Morphology Little or no difference was found in amino acid and carbohydrate composition of the "interior honeydew" during the growth of C. pseudoceriferus. However, qualitative differences were revealed in the wax material in the cover during the growth of C. pseudoceriferus and C. japonicus (Tamaki, 1970). The relative amount of esters with straight chain fatty acids and straight chain alcohols decreased with growth, while esters with straight chain fatty acids and cyclic alcohols increased. Hashimoto and Mukai (1967) also detected cyclic wax only in the 3rd-instar nymphs and in adults of C. pseudoceriferus. The fatty acid composition of the cover of this species also changed during their growth. The concentration of low molecular weight fatty acids (less than C20), which were predominant in the 1st and 2nd instars, declined and those of higher molecular weight (C30-C32) became predominant in the adult, indicating changes in fatty acid biosynthesis during growth (Tamaki, 1970). (2) Secretion and construction of the cover Observations on the process of cover construction in C. pseudoceriferus have indicated that lst- and 2nd-instar nymphs secrete white fragile wax ('dry wax') from both the medial and submarginal areas of the dorsum. After the second moult, the whole surface of the dorsum became covered with a new type of wax ('wet wax'). On the median dorsal area, the "dry wax" secreted by the 1st and 2nd instars was then pushed up by the newly secreted "wet wax" and the cover developed into a conical or hem-like structure. During the 4th (adult) stage, a large amount of "wet wax" was secreted onto the dorsum, forming a dome on top of which a very small amount of the old "dry wax" remained. The "wet wax" consisted of both wax and aqueous materials, giving a bubble-like structure composed of fine droplets of the aqueous material coated with wax. On the other hand, the "dry wax" consists of waxy material alone, and is fibrous in structure. On the ventral body surface, at least two different waxy secretions were observed. One was a white line of powdery wax along each stigmatic furrow, present in all instars; the other was a powdery wax secreted around the vulva of the mature females (Kawai and Tamaki, 1967; Tamaki, 1970). Detailed observations on the body surface of C. pseudoceriferus using light and scanning electron microscopy have shown the presence of six types of dermal gland pores (Kawai and Tamaki, 1967; Tamaki et al., 1969). These are simple pores, cruciform pores, quinquelocular disc-pores, multilocular disc-pores, tubular ducts and filamentous ducts. Based on the distribution of wax and the timing of its appearance on the body surface, it is suggested that the simple pores are, at least partly, responsible for the secretion of "wet wax', the quinquelocular disc-pores for the wax along the stigmatic furrow and the multilocular disc-pores for the wax around the vulva. The simple pore gland consists of one principal cell and one to four accessory cells and is referred to as the Ceroplastes-pore by Foldi (Section 1.1.2.7) and Hodgson (Section 1.1.3.1). Histochemical studies have revealed that the principal cell is responsible for the secretion of the aqueous material, which is described in Section 1.1.2.7. It is noteworthy that the cuticular area of the dorsum covered with the "dry wax" has no glandular structures. Hence, it is the pore canals and related structures that are likely to have been concerned with the "dry wax" secretion on the dorsum, as is the case of normal cuticular wax in other insect species (Locke, 1960, 1961). The morphology of the dermal glands on the body surface of C. japonicus and C. rubens are similar to those of C. peudoceriferus (Tamaki, 1970). The shape and fine structure of waxy secretions of scale insects appears to be a species characteristic and to depend on the dermal gland pores, when observed by scanning electron microscopy (Tamaki et al., 1969; Hashimoto and Kitaoka, 1971b).
Chemistry of the test cover
69
CONCLUSION The chemical composition of the test or cover of scale insects differs between species. In the case of soft scales, waxy materials are an important component of the cover. However, in the case of Ceroplastes spp., particular aqueous components of the test referred to as "interior honeydew" are also important constituents, in addition to the waxy materials. Although true wax, esters of higher aliphatic fatty acids and higher aliphatic alcohols, are the major components of the waxy fraction, cyclic waxes are unique components in the test of Ceroplastes spp. Except for sugars and amino acids in the "interior honeydew", almost all the components seem to be biogenic products of the scale insects themselves. Production and secretion of the bulky cover by soft scales are in contrast to the thin, hard cover of armored scale insects. Although there is little information on the chemical properties of non-lipid materials in the test covers of armored scales, the covers of both soft scales and armored scales apparently play an important role in the protection of the insect's body from deleterious environmental factors and natural enemies. It is interesting to note that these bulky or hard covers seem to be utilized only by non-moving species and by particular stages during their development. Although mixtures of components or purified fractions of the covers of particular scale insects have been utilized as important materials for industrial purposes, detailed information on the chemical composition of these covers is still not adequate. Further studies, using more modem analytical techniques, are essential for an expansion in the use of these interesting biological and natural materials or compounds.
ACKNOWLEDGEMENTS The author thanks to Drs. Akira Hashimoto, Shozo Kawai and Shozo Takahashi for their helpful suggestions on the manuscript.
REFERENCES Auclair, J.L., 1958. Honeydew excretion in the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae). Journal of Insect Physiology, 2: 330-337. Auclair, J.L., 1963. Aphid feeding and nutrition. Annual Review of Entomology, 8: 439-490. Banks, H.J., Cameron, D.W., Edmonds, J.S. and Raverty, W.D., 1976a. Chemistry of the Coccoidea. [U. Isolation of a bianthrone glucoside from Callococcus acaciae and of ceroalbolinic acid from Cryptes baccatum (Hemiptera: Insecta). Australian Journal of Chemistry, 29: 2225-2230. Banks, H.J., Cameron, D.W. and Crossley, M. J., 1976b. Chemistry of the Coccoidea. IV. Polyhydroxyanthraquinones and their glucosides fromEriococcus coriaceus (Hemiptera: Insecta). Australian Journal of Chemistry, 29: 2231-2245. Baron, R.L. and Guthrie, F.E., 1960. A quantitative and qualitative study of sugars found in tobacco as affected by the green peach aphid, Myzus persicae and its honeydew. Annals of Entomological Society of America, 53: 220-228. Beament, J.W.L., 1945. The cuticular lipoids of insects. Journal of Experimental Biology, 21:115-131. Beament, J.W.L., 1964. The active transport and passive movement of water in insects. Advances in Insect Physiology, 2" 67-129. Beardsley, W.J. and Gonzalez, R.H., 1975. The biology and ecology of armored scales. Annual Review of Entomology, 20: 47-73. Bergman, W., 1938. The composition of ether extractives from exuviae of the silkworm, Bombyx mori. Annals of Entomological Society of America, 31 : 315-321. Bowers, W.S. and Thompson, M.J., 1965. Identification of the major constituents of the crystalline powder covering the larval cuticle of Samia cynthia ricini (Jones). Journal of Insect Physiology, 11:1003-1011. Brown, K.S., 1975. The chemistry of aphids and scale insects. Chemical Society Reviews, London, 4: 263-288. Calderon, J.S., Quijano, L. and Rios, T., 1978. Ceralbol, a new sesterterpenic alcohol isolated from insect wax. Experientia, 34" 421-422. Chibnall, A.C., Latner, A.L., Williams, E.F. and Ayre, C.A., 1934a. The constitution of coccerin. Biochemical Journal, 28:313-325.
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Morphology Chibnall, A.C., Piper, S.H., Pollard, A., Williams, E.F. and Sahai, P.N., 1934b. The constitution of the primary alcohols, fatty acids and paraffins present in plant and insect waxes. Biochemical Journal, 28: 2189-2208. Daniel, H.J. and Millar, J.O., 1992. Isolation and identification of an oviposition stimulant for Aphytis melinus from its host, California red scale. Proceedings of the 9th Chemical Ecology Meeting, Kyoto, p. 78. Dickson, R.C., 1951. Construction of the scale covering of Aonidiella aurantii (Mask.). Annals of Entomological Society of America, 44: 596-602. Disselkamp, C., 1954. The scale formation of the San Jose scale (Quadraspidiotus perniciosus Comst.). H6fchen-Briefe, Bayer Pflanzenschutz-Nachrichten, 7:105-151. Ebstein, R.P. and Gerson, U., 1971. The non-waxy component of the armored-scale insect shield. Biochimica et Biophysica Acta, 237: 550-555. Fast, P.G., 1964. Insect lipids: review. Memoirs of the Entomological Society of Canada, No. 37., 50 pp. Gilby, A.R., 1957. Studies of cuticular lipids of arthropods. II. The chemical composition of the wax from Ceroplastes destructor. Archives of Biochemistry and Biophysics, 67: 307-319. Gilby, A.R. and Alexander, A.E., 1957. Studies of cuticular lipids of arthropods. I. The influence of biological factors on the composition of the wax from Ceroplastes destrucwr. Archives of Biochemistry and Biophysics, 67" 302-306. Gilby, A.R. and Cox, M.E., 1963. The cuticular lipids of the cockroach, Periplaneta americana (L.). Journal of Insect Physiology, 9: 671-681. Gray, R.A., 1952. Composition of honeydew excreted by pineapple mealybugs. Science, New York, 115: 129-133. Hackman, R.H., 1951. The chemical composition of the wax of the white wax scale, Ceroplastes destructor (Newstead). Archives of Biochemistry and Biophysics, 33: 150-154. Hackman, R.H. and Trikojus, V.M., 1952. The composition of the honeydew excreted by Australian coccids of the genus Ceroplastes. Biochemical Journal, 51: 653-656. Hashimoto, A. and Kitaoka, S., 1971a. Studies on the lipids of scale insects. Part XVI. The particular distribution of fatty acids in the triglycerides of several scale insect fats. Agricultural and Biological Chemistry, 35: 275-277. Hashimoto, A. and Kitaoka, S., 1971b. Scanning electron microscopic observation of the waxy substances secreted by some scale insects. Japanease Journal of Applied Entomology and Zoology, 15: 76-86. Hashimoto, A. and Kitaoka, S., 1982. Composition of wax secreted by a scale insect, Drosicha corpulenta Kuwana (Homoptera: Margarodidae). Applied Entomology and Zoology, 17: 453-459. Hashimoto, A. and Mukai, K., 1965. Studies on the lipids of coccids. Part H. Glycerides and true waxes in the lipids of Ceroplastes pseudoceriferus (Green). Nippon Nogeikagaku Kaishi, 39: 489-494. Hashimoto, A. and Mukai, K., 1967. Studies on the lipids of coccids. Part VI. Formation of the wax-shell and change in the composition of lipid class in the seasonal life cycle of Ceroplastes pseudoceriferus (Green). Nippon Nogeikagaku Kaishi, 41 : 282-289. Hashimoto, A., Yamada, K. and Mukai, K., 1967a. Studies on the lipids of coccids. Part v m . Chromatographic separation of the lipids from Lecanium horii (Kuwana). Nippon Nogeikagaku Kaishi, 41 : 393-398. Hashimoto, A., Yoshida, H. and Mukai, K., 1967b. Studies on the lipids of coccids. Part IX. Separation and characterization of saturated and unsaturated wax esters from the wax-shell lipids of Ceroplastes pseudoceriferus (Green). Agricultural and Biological Chemitry, 41: 498-505. Hashimoto, A., Yamada, K. and Mukai, K., 1968a. Studies on the lipids of coccids. Part XI. Lipid composition of the insect body of Ceroplastes rubens (Maskell) and Ceroplastesjaponicus (Green). Nippon Nogeikagaku Kaishi, 42- 158-164. Hashimoto, A., Yamada, K. and Mukai, K., 1968b. Studies on the lipids of coccids. Part XII. The triglyceride composition of Ceroplastespseudoceriferus Green. Nippon Nogeikagaku Kaishi, 42:197-206. Hashimoto, A., Yamada, K. and Mukai, K., 1968c. Studies on the lipids of coccids. Part XIII. Most particular triglyceride composition of the egg lipids of Lecanium horii (Kuwana). Nippon Nogeikagaku Kaishi, 42:509-512. Hashimoto, A., Yamada, K. and Mukai, K., 1969. The triglyceride composition of fats of Ceroplastes rubens and Ceroplastes japonicus. Nippon Nogeikagaku Kaishi, 43: 269-272. Hashimoto, A., Hirotani, A., Mukai, K. and Kitaoka, S., 1970. Studies on the lipids of coccids. Part XIV. Composition of the triglycerides of four scale insect fats. Agricultural and Biological Chemistry, 34: 1839-1842. Hashimoto, A., Hirotani, A., Mukai, K. and Kitaoka, S., 1971a. Studies on the lipids of scale insects. Part XVII. Wax ester composition of 10 species of scale insects. Nippon Nogeikagaku Kaishi, 45: 100-109. Hashimoto, A., Yoshida, H., Mukai, K. and Kitaoka, S., 1971b. Studies on the lipids of scale insects. Part XV. Composition of hydrocarbons, wax esters and free fatty acids in the wax-shell lipids of Ceroplastes rubens, Ceroplastes japonicus and Ceroplastes pseudoceriferus. Agricultural and Biological Chemistry, 45: 96-99. Holdgate, M.W. and Seal, M., 1956. The epicuticular wax layers of the pupa of Tenebrio molitor L. Journal of Experimental Biology, 33: 82-106.
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Kawai, S. and Tamaki, Y., 1967. Morphology of Ceroplastes pseudoceriferus Green with special reference to the wax secretion. Applied Entomology and Zoology, 2: 133-146. Kennedy, J.S. and Mittler, T.E., 1953. A method of obtaining phloem sap via the mouth-parts of aphids. Nature, London, 171 : 528. Kohno, M., 1932. Chemical studies on scale insects in Japan (Part 1). Waxy materials of Ceroplastes rubens Mask. Nippon Nogeikagaku Kaishi, 8:1150-1160. Kohno, M., 1933a. Chemical studies on scale insects in Japan (Part 2). Waxy materials of Ceroplastes ceriferus And. Nippon Nogeikagaku Kaishi, 9: 458-466. Kohno, M., 1933b. Chemical studies on scale insects in Japan (Part 3). Waxy materials of Ceroplastes floridensis Comst. Nippon Nogeikagaku Kaishi, 9: 467-474. Kohno, M., 1933c. Chemical studies on scale insects in Japan (Part 5). Nitrogenous compounds and waxy material of Cerococcus muratae Kuw. Nippon Nogeikagaku Kaishi, 9: 1276-1283. Kohno, M. and Maruyama, T., 1934. Chemical studies on scale insects in Japan (Part 7). Carbohydrates and waxy material of Pulvinaria horii. Nippon Nogeikagaku Kaishi, 10: 1228-1235. Kohno, M. and Maruyama, T., 1935. Chemical studies on scale insects in Japan (Part 9). Carbohydrates and waxy material of lcerya purchasi Mask. Nippon Nogeikagaku Kaishi, 11: 647-658. Kohno, M. and Maruyama, T., 1936. Chemical studies on scale insects in Japan (Part 12). Carbohydrates and waxy material of Prontaspis yanonensis Kuw. Nippon Nogeikagaku Kaishi, 12: 523-530. Kohno, M. and Maruyama, T., 1937a. Chemical studies on scale insects (part 13). Resinous material of Ceroplastes rubens Mask. (No. 2). On a new resin acid, rubenic acid. Nippon Nogeikagaku Kaishi, 13: 177-184. Kohno, M. and Maruyama, T., 1937b. Chemical studies on scale insects (part 14). Resinous materials of Ceroplastes rubens Mask. (No. 3). On a new resinol, rubenol. Nippon Nogeikagaku Kaishi, 13: 191-199. Kohno, M. and Maruyama, T., 1938a. Chemical studies on scale insects in Japan (part 17). Resinous materials of Ceroplastes rubens Mask. (No. 4). On rubabietic acid. Nippon Nogeikagaku Kaishi, 14: 318-326. Kohno, M. and Maruyama, T., 1938b. Chemical studies on scale insects in Japan (part 20). Carbohydrates and waxy materials of Tachardina theae Green et Mann. Nippon Nogeikagaku Kaishi, 14: 1364-1370. Koyama, R., 1934a. Studies on lbota wax (Part 2). On the fatty acid components (No. 2). Nihon Kagaku Kaisi, 55: 348-352. Koyama, R., 1934b. Studies on lbota wax (Part 3). On the unsaponifiable matters (No. 3). Nihon Kagaku Kaisi, 55: 802-808. Lamb, K.P., 1959. Composition of the honeydew of the aphid, Brevicorne brassicae (L.), feeding on swedes (Brassica napobrassica De.). Journal of Insect Physiology, 3: 1-13. Lees, A.D., 1947. Transpiration and the structure of the epicuticle in ticks. Journal of Experimental Biology, 23: 397-410. Locke, M., 1960. The cuticle and wax secretion in Calpodes ethlius (Lepidoptera: Hesperidae). Quarterly Journal of Microscopical Science, 101:333-338. Locke, M., 1961. Pore canals and related structures in insect cuticle. Journal of Biophysical and Biochemical Cytology, 10:589-618. Louloudes, S.J., Chambers, D.L., Moyer, D.B. and Starkey III, J.H., 1962. The hydrocarbons of adult houseflies. Annals of Entomological Society of America, 55: 442-448. Maltais, J.B. and Auclair, J.L., 1952. Occurrence of amino acids in the honeydew of the crescent-marked lily aphid, Myzus circumflexus (Buck.). Canadian Journal of Zoology, 30: 191-193. Meinwald, J., Smolanoff, J., Chibnall, A.C. and Eisner, T., 1975. Characterization and synthesis of waxes from homopterous insects. Journal of Chemical Ecology, 1: 269-274. Mittler, T.E., 1953. Amino-acids in phloem sap and their excretion by aphids. Nature, London, 172: 207. Miyamoto, F., Naoki, H., Takemoto, T. and Naya, Y., 1979. New macrocyclic sesterterpenoids from a scale insect (Ceroplastes ceriferus). Tetrahedron, 35: 1913-1917. Miyamoto, F., Naoki, H., Naya, Y. and Nakanishi, K., 1980. Study of the secretion from a scale insect (Ceroplastes ceriferus) diterpenoids and sesterterpenoids. Tetrahedron, 36: 3481-3487. Mukai, K., Hashimoto, H. and Tsujimoto, K., 1965. Studies on the lipids of coccids. Part I. Higher alcohols of lcerya purchasi Mask. Nippon Nogeikagaku Kaishi, 39: 77-81. Naya, Y., Miyamoto, F. and Takemoto, T., 1978. Formation ofenantiomeric sesquiterpenes in the secretions of scale insects. Experientia, 34: 984-986. Naya, Y., Miyamoto, F., Kishida, K., Kusumi, T., Kakisawa, H. and Nakanishi, K., 1980. Revised structure of ceriferic acid. Chemistry Letters, 883-886. Naya, Y., Yoshihara, K., Iwashita, T., Komura, H. and Nakanishi, K., 1981. Unusual sesterterpenoids from the secretion of Ceroplastes floridensis (Coccidae), an orchard pest, application of the allylic benzoate method for determination of absolute configuration. Journal of American Chemical Society, 103: 7009-7011. Pawlak, J.K., Tempesta, M.E, lwashita, T., Nakanishi, K. and Naya, Y., 1983. Structures of sesterterpenoids from scale insect Ceroplastes celfferus. Revision of the 14-membered ceriferene skeleton from 2-t/6-c/10-t to 2-c/6-t/10-t. Chemistry Letters, 1069-1072. Rios, T. and Colunga, F., 1965. Three new alcohols from insect wax, ceroplastol I, II and albolineol. Chemistry & Industry, June 26, 1184-1185.
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Morphology Rios, T. and Gomez, G.F., 1969. Albolic acid, a new sesterterpenic acid isolated from insect wax. Tetrahedron Letters, 34: 2929-2930. Rios, T. and Quijano, L., 1969. The structure of ceroplastol II, a sesterterpenic alcohol isolated from insects wax. Tetrahedron Letters, 17:1317-1318. Rios, T., Quijano, L. and Calderon, J., 1974. Albolineol, a sesterterpene with a novel bicyclic skeleton. Journal of the Chemical Society, Chemical Communications, 728-729. Takabayashi, J. and Takahashi, S., 1985. Host selection behavior of Anicetus beneficus Ishii et Yasumatsu (Hymenoptera: Encyrtidae). HI. Presence of ovipositional stimulants in the scale wax of the genus Ceroplastes. Applied Entomology and Zoology, 20: 173-178. Takahashi, S. and Nomura, Y., 1982. Wax composition of the soft scale Ericeruspela (Hemiptera: Coccidae). Entomologia Generalis, 7:313-316. Takahashi, S. and Takabayashi, S., 1984. Host selection behavior ofAnicetus beneficus lshii et Yasumatsu (Hymenoptera: Encyrtidae). II. Bioassay of oviposition stimulants in Ceroplastes rubens Maskell (Hemiptera: Coccidae). Applied Entomology and Zoology, 19:117-119. Takahashi, S., Hajika, M., Takabayashi, J. and Fukui, M., 1990. Oviposition stimulants in the coccoid cuticular waxes of Aphytis yanonensis De Bach & Rosen. Journal of Chemical Ecology, 16: 1657-1665. Tamaki, Y., 1963. Preliminary studies on wax material and honeydew excretion of Ceroplastes pseudoceriferus (Green). Japanese Journal of Applied Entomology and Zoology, 7: 355-357. Tamaki, Y., 1964a. Amino acids in the honeydew excreted by Ceroplastespseudoceriferus (Green). Japanese Journal of Applied Entomology and Zoology, 8: 159-164. Tamaki, Y., 1964b. Carbohydrates in the honeydew excreted by Ceroplastes pseudoceriferus (Green). Japanese Journal of Applied Entomology and Zoology, 8: 227-234. Tamaki, Y., 1966. Chemical composition of the wax secreted by a scale insect (Ceroplastes pseudoceriferus Green). Lipids, 1" 29%300. Tamaki, Y., 1968. Isolation of tetradecan-l,14-dioic acid from the comstock mealybug, Pseudococcus comstocki Kuwana (Homoptera: Pseudococcidae). Lipids, 3: 186-187. Tamaki, Y., 1970. Studies on waxy coverings of Ceroplastes scale insects. Bulletin of National Institute of Agricultural Sciences (Japan), C, 24:1-111. Tamaki, Y. and Kawai, S., 1966. Seasonal change of the waxy covering and its components era scale insect, Ceroplastes pseudoceriferus Green. Botyu-Kagaku, 31: 148-153. Tamaki, Y. and Kawai, S., 1967. Fatty acids, alcohols and hydrocarbons in the body lipid of Ceroplastes pseudoceriferus Green, Ceroplastes japonicus Green and Ceroplastes rubens Maskell (Homoptera: Coccidae). Botyu-Kagaku, 32: 63-69. Tamaki, Y. and Kawai, S., 1968. Fatty acids, alcohols and hydrocarbons in the waxy coveting of Ceroplastes pseudoceriferus Green, Ceroplastes japonicus Green and Ceroplastes rubens Maskell (Homoptera: Coccidae). Japanese Journal of Applied Entomology and Zoology, 12: 23-28. Tamaki, Y. and Kawai, S., 1969. X-ray diffraction studies on waxy covering of scale insects (Homoptera: Coccoidea). Applied Entomology and Zoology, 4: 79-86. Tamaki, Y., Yushima, T. and Kawai, S., 1969. Wax secretion in a scale insect, Ceroplastespseudoceriferus Green (Homoptera: Coccidae). Applied Entomology and Zoology, 4: 126-134. Tempesta, M.S., lwashita, T., Miyamoto, F., Yoshihara, K. and Naya, Y., 1983. A new class of sesterterpenoids from the secretion of Ceroplastes rubens (Coccidae). Journal of the Chemical Society, Chemical Communications, 1182-1183. Veloz, R., Quijano, L., Galderon, J.S. and Rios, T., 1975. Albocerol, a new macrocyclic sesterterpene. Journal of the Chemical Society, Chemical Communications, 191-192. Warth, A.H., 1956. The Chemistry and Technology of Waxes, Chap. 3, p. 78-341. Reinhold Publish. Corp., New York, 940 pp. Wigglesworth, V.B., 1945. Transpiration through the cuticle of insects. Journal of Experimental Biology, 21: 97-114. Wigglesworth, V.B., 1957. The physiology of insect cuticle. Annual Review of Entomology, 2: 37-54.
Soft Scale Insects - Their Biology, Natural Enemies and Control
Y. Ben-Dov and C.J. Hodgson (Editors) 1997 Elsevier Science B.V.
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1.1.2.6 Internal Anatomy of the Adult Female IMRI~ FOLDI
INTRODUCTION Although the internal anatomy of soft scales has many unusual features, its' study has been greatly neglected. This is despite the fact that many questions remain unresolved with regard to the structure and function of soft scales which could help in the basic understanding of their biology and thus in their more efficient control. In addition, it is likely that studies of their comparative anatomy will reveal varying degrees of affinity between taxa within the Coccoidea and, therefore, form the basis for further hypotheses regarding their relationships. There are two basic early studies on the anatomy of soft scales insects, namely those of Berlese (1894), who was amongst the earliest workers to made fine, detailed anatomical observations, and Pesson who wrote a large monograph (1944) on his exhaustive and very detailed comparative study on the head, mouthparts and nervous and digestive systems of female scale insects. The only significant studies done since then are those of Bielenin, who initially described the anatomy and histology of both the male and female reproductive system of the soft scale, P a r t h e n o l e c a n i u m p o m e r a n i c u m (Kawecki) (1962a, 1962b) and then the nervous system and the alimentary canal (1963a, 1963b). A compilation of the anatomical data available in the first third of the Twentieth Century was made by Balachowsky (1937). This Section summarizes our knowledge on the internal anatomy of soft scale insects, supplemented with original scanning and transmission electron microscopy observations by the author. A diagrammatic view of the layout of the internal anatomy of a female soft scale is presented in Fig. 1.1.2.6.1,A.
DIGESTIVE SYSTEM AND ASSOCIATED STRUCTURES Berlese (1894), Pesson (1944) and Bielenin (1963a, 1963b) made major studies on the soft scale digestive system. All three showed that the most anterior part of the alimentary tract is the food canal, located in the maxillary stylets. This leads into the pharyngeal duct. The pharynx, a short narrow tube, leaves the tentorial box anteriorly and then turns upwards and posteriorly, where it becomes the oesophagus. The oesophageal tube, a broader tube than the pharynx, runs posteriorly beneath the salivary glands and above the nervous system to open into the midgut. This is a still broader tube (Fig. 1.1.2.6.4), which forms a big loop in the haemocoel, finally passing back to and connecting with the anterior part, forming the filter chamber. The filter chamber opens into the small ileum, followed by a very broad rectum (Figs 1.1.2.6.1,A and 1.1.2.6.4).
Section 1.1.2.6 references, p. 89
74
Morphology HEAD CAPSULE In soft scale insects, sclerotised structures are much reduced and the limits of the different plates constituting the head capsule are no longer recognisable. However, as with all Hemiptera, there has been considerable modification of the buccal structures to produce the two pairs of long interlocking stylets. There have been two proposals as to how these originated and these are known as the appendicular and the parietal theories.
salivary glands
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B Xmandibularstylets
Fig. 1.1.2.6.1. A - Longitudinal section through an adult female soR scale showing the typical layout of its internal anatomy; oes - oesophagus; ph - pharynx; fch - filter chamber; sg - suboesophageal ganglion. B - Cross section of the stylets of a soR scale; n - neurons. C - Dorsal view of the salivary pump of Chloropulvinariafloceifera (Westwood).
The appendicular theory suggests that the stylets, the levers and the mandibular and maxillary plates evolved from the complete ancestral mandibular and maxillary elements. A scenario for their evolution was proposed by Hamilton (1981). The parietal theory also suggests a cranial origin for such structures as the mandibular and maxillary plates but this theory suggests that the origin of the levers was probable composite, i.e. both appendicular and parietal (Denis and Bitsch, 1973; Bourgoin, 1986a). The parietal theory was first proposed by Pesson (1944) after a study of a range of scale insect species. Later, Parsons (1964, 1974) suggested a series of steps for the evolution of the Hemiptera head capsule and she and Bourgoin (1986b) have provided some morphological evidence to support it. However, although the parietal theory has the merit of providing a relatively simple explanation of the observed morphological structures, details of both it and the appendicular theory still need to be confirmed by further careful embryological studies.
MOUTHPARTS AND FEEDING STRATEGIES
The mandibles and maxillae of all Hemiptera have become highly modified into four long, fine stylets which interlock and which are ideally adapted for piercing and sucking
Internal anatomy of the adultfemale
75
nutritious fluids, particularly from plants but which may also be used for sucking body contents and/or blood, such as by the predatory bugs. Ancestral Hemiptera are considered to have been phytophagous. From these, the Heteroptera evolved as predators, some later reverting to a phytophagous habit, while the Homoptera remained basically phytophagous. The structure of the mouthparts of female Coccidae, as with all scale insects, is related to their specialised feeding behaviour, involving the acquisition of sap from plant vascular tissues, although, at present, it is not clear whether coccids feed only on phloem sap or whether some may also tap xylem, parenchyma or other tissues or combinations of tissues. A detailed study of mouthparts of some Coccoidea is provided by Pesson (1944). More recently, the comparative morphology of the labium, clypeolabral shield and salivary pump was studied by Koteja (1974, 1976a, 1976b). The basic structure throughout the scale insects, and thus including the soft scales, consists internally of the tentorium, stylets, pairs of mandibular and maxillary levers, the hypopharynx and also the external labium.
STYLETS The four long, fine stylets, which correspond to the modified mandibles and maxillae, have become interlocked to form a tight bundle, which has the appearance of a single structure (Fig. 1.1.2.6.1,B). The stylets become interlocked immediately below the salivary pump and the stylet bundle is about 3-5 #m in diameter and subcircular in crosssection. The maxillary stylets, which lie internally, are closely interlocked by crests and grooves running along the entire inner surface, while the mandibular stylets cover them externally without such grooves and ridges. Within the maxillary stylets are located the food and salivary canals. The former is placed dorsally and is connected with the pharyngeal duct, while the latter is ventral and joins with the salivary pump. Each stylet also includes a microcanal which appears to be always empty. On the inner base of each stylet, there is a lever for muscle attachment. The extremity of each stylet is sharply pointed for penetrating the plant tissue. The outer mandibular stylets are innervated so that stylet direction and movement can be controlled in response to sensory perception. The neurons of these nerves lie in a central cavity which runs along the entire length of each stylet. The stylets of Coccoidea are usually long and sometimes longer than the body, when not embedded in the plant, are enclosed in the crumena. The crumena is a posterior extension of the hypopharynx and is an elongate, ventral, cuticular sac which extends into the abdomen, enclosing part of the stylets. The piercing and feeding mechanisms were studied by Pesson (1944), who found that only the outer mandibulary stylets were involved in the initial penetration of host plant tissue, each stylet being moved independently and successively by a series of short thrusts and each stylet penetrating for an equal distance into the tissue. The maxillary stylets then follow but their movement is in unison, penetrating together rather than independently. During the penetration of the stylets into the host plant, saliva is injected along the stylet path and forms a coat or sheath around the stylets; this salivary sheath is easily detected in histological preparations. The path taken by the stylets through the plant tissue is initially rather straight but, if an obstacle is encountered or some other difficulty occurs, then the stylets are withdrawn a short distance and then pushed forward again in another direction (Baranyovits, 1953).
Section 1.1.2.6 references, p. 89
Morphology
76 TENTORIUM AND STYLET LEVERS
A detailed study on the tentorium of soft scales is provided by Pesson (1944), while a valuable introduction to the general interpretation and terminology of the tentorium in Hemiptera is given by Bourgoin (1986a) The tentorium forms the internal skeleton of the head capsule to which are attached numerous muscles, especially the powerful mandibular and maxillary muscles. The tentorium is composed of two anterior tentorial arms or pretentoria, which together form the pretentorium, and two posterior tentorial arms or metatentoria, which together form the metatentorium. These four arms are formed from four invaginations or apodemes of the integument, called pretentorina and metatentorina. A transverse bar or corpotentorium links these four apodemes together. Two dorsal arms or supratentoria may arise from the pretentoria as in other Hemiptera (Fig. 1.1.2.6.2). These are expansions of the anterior apodemes and are characterised by the absence of exocuticle. The mandibular and maxillary levers are considered to be sclerites of morphologically composite origin and are, therefore, not thought to be just extensions of the stylet elements (Denis and Bitsch, 1973, Bourgoin, 1986a).
A
B
supratentoria
aa
.-.
:~!..
.
o 9 0
pretcntorina
et
metatentorina
_ pa
Li
C Fig. 1 . 1 . 2 . 6 . 2 . A - Generalized d i a g r a m o f an h e m i p t e r a n tentorium. B - F a c e - v i e w and C - Profile o f a soft scale t e n t o r i u m (alter Pesson, 1944). a a - anterior arm; d - clypeus; c t - corpotentorium; e p - e p i p h a r y n x ; h - h y p o p h a r y n x ; L 1 - m a n d i b u l a r lever; I.,2 - maxillary lever; m a s - m a n d i b u l a r stylet; m s - maxillary stylet; l m - posterior arm;
Ida - p h a r y n x .
A SEM micrograph of the tentorium of Parthenolecanium rufulum (Cockerell), is shown in Fig. 1.1.2.6.3 and appears to be different in structure from the diagram of a soft scale given by Pesson (1944) (Fig. 1.1.2.6.2,A). There are only two tentorial arms and these are considered to be the pretentoria; the metatentoria appear to be absent. Ventrally, each pretentoria is prolonged by a strong internal ridge of the lateral sulcus of the clypeus. These ridges join ventrally to form the hypopharyngial plate. Dorsally, this plate bears two long hypopharyngial wings which extend anteriorly, with each wing linked to the distal part of a pretentoria and to the corpotentorium. The whole structure,
Internal anatomy of the adult female
77
the tentorial elements, hypopharyngial structures and the internal clypeal ridges, form what is known as the "tentorial box ".
Fig. 1.1.2.6.3. Dorsal view of the tentorium of Parthenolecanium rufulum (Cockerell), SEM micrograph, xl,000, aa - Anterior arm; ct - Corpotentorium; h - hypopharynx; hp - hypopharyngial plate; hw - Hypopharyngial wing; ies - Lateral clypeal sulcus; mdl- Mandibular lever; taxi - Maxillary lever.
Similar significant variations have been observed in other Coccoidea and a comparative study of the ultrastructure of the tentorium is being undertaken by the author for use in a phylogenetic analysis of higher categories.
SALIVARY PUMP The withdrawal of the saliva from the salivary duct and its injection into the salivary canal within the maxillary stylets is made by a small cuticular device, the salivary pump (Fig. 1.1.2.6.1,C). This has been described by Pesson (1944) and also by Koteja (1976), who undertook an extensive comparative study. The salivary pump is located at the base of the pharynx and consists of two parts: the piston and the pump chamber. The ventral part of salivary pump communicates with the salivary canal in the maxillary stylets, while the pump chamber receives the posterior end of the common duct from the salivary glands. The walls of the pump chamber are all strongly sclerotized, except that dorsally which is membranous and is used as part of the piston. This membranous wall bears an apodeme to which numerous muscles are attached, so that the wall can move in two directions, thus sucking the saliva into the pump chamber and then expelling it into the salivary canal. Unpublished SEM observations by the present author have indicated that the piston, pump chamber and common salivary duct can all vary in both
Section 1.1.2.6 references, p. 89
78
Morphology
shape and size, both within the Coccidae and more widely in the Coccoidea. In addition, the surface of the pump chamber can be either smooth or rough with finely differentiated microstructures.
FILTER CHAMBER The digestive system of female soft scales is characterized by the presence of a device known as the filter chamber which, by osmoregulation, directs excess water and also, perhaps, some of the sugar in the plant sap from the anterior part of the midgut across the modified epithelium into the posterior part of the midgut. The filter chamber is thus formed by the close juxtaposition of the two extremities of the midgut which, along with part of oesophagus and the ileum, are enclosed in an invaginated cavity developed from the enlarged anterior part of rectum. This envelope encloses most of the gut, isolating the filter chamber from the haemocoel (Fig. 1.1.2.6.4).
oesophagus
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.
.
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filter chamber
rectum Malpighian tubules
) invaginated anus anal ring ~tae
Fig. 1.1.2.6.4. Alimentarytract of Coccus hesperidum L. showingthe structure of the filter chamber.
79
Internal anatomy of the adultfemale
Fig. 1.1.2.6.5 illustrates a cross section through the filter chamber and shows the close contact of the two extremities of the midgut, their modified epithelia and also the surrounding membrane formed from the rectum. The structure of the filter chamber differs significantly between the Stemorrhyncha (in which the Malpighian tubules are not included in the filter chamber, as in the scale insects) and that of the Auchenorrhyncha (where the Malpighian tubules are included in the filter chamber). Good, clear illustrations of the filter chamber ofPulvinarieUa (Pulvinaria) mesembryanthemi (Vallot) and Coccus hesperidum L. are provided by Pesson (1935, 1944). Plant sap, upon which all scale insects feed, contains large quantities of water and sugars, particularly that derived from the phloem. It is believed that the filter chamber is important in the elimination of this excess water and sugar by "short circuiting" most of the gut. This idea was entirely hypothetical until recently when ultrastructural studies of the guts oflcerya purchasi MaskeU (Foldi, 1972), Planococcus citri (Foldi, 1973) and Coccus hesperidum (unpublished observations) have revealed specific peculiarities of that part of the midgut that forms the filter chamber (Fig. 1.1.2.6.6). Foldi (1972, 1973) showed that the filter chamber appeared to be structurally well adapted for the transport of surplus water and solutes by passive osmosis from the dilute sap in the anterior end of the midgut directly into the posterior end of the midgut. In the soft scales, therefore, the filter chamber acts as an osmoregulatory device that develops a local osmotic gradient, directing the water across the modified epithelia into the proctodeum. Modem concepts explaining the movement of water and solutes across epithelial membranes suggest that this is a consequence of the local secretion of ions into a space or channel within the epithelial cells, resulting in the development of a local osmotic gradient. modified rectum .
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Fig. 1.1.2.6.5. Cross section of filter chamber of Coccushesperidum L.
Section 1.1.2.6 references, p. 89
80
Morphology
Fig. 1.1.2.6.6. Modified epithelium of the midgut in the filter chamber of Coccus hesperidum L. SEM micrographs (A, xT,000, B, xS,000); impb - invagination of plasmic basal membrane. It has also been found that there are distinct differences in the ultrastructure of the epithelia in the filter complex and that of conventional epithelial cells. Thus, in Coccus hesperidum, the epithelial cells of the filter chamber complex were greatly reduced in size, varying from between 2-7#m high, and their cellular surface was increased by the presence of microvilli and by folding of the basal plasma membranes (Fig. 1.1.2.6.5). The high permeability of these cells is probably linked to the existence of intra-membranous particles in the microvilli and in the invaginated plasma membrane which are visible by cryofracture studies. The small amount of cytoplasm contains only ribosomes and a few mitochondria.
RESPIRATORY SYSTEM Oxygen and carbon dioxide diffusion within the body of the scale insect is performexl within a well-developed tracheal system, assuring gaseous exchange between cells and the outside air. This tracheal network is connected to the exterior through two pairs of spiracles situated latero-ventrally on the meso- and metathorax. Recently, Hodgson (1994) gave a detailed review of the spiracles in the family Coccidae and noted some differences at the subfamily level (Fig. 1.1.2.6.7). The basic structure of each spiracle consists an outer sclerotised cavity, referred to as the peritreme, which can vary slightly in size and even in structure between species. At
81
Internal anatomy of the adultfemale
its inner end, the peritreme has two valves, a dorsal and a ventral valve, which regulate air circulation. The dorsal valve is sclerotised and is probably not movable but the ventral valve is membranous and it is considered to be movable. From the ventral margin of the peritreme arises a large sclerotised cuticular structure, the muscle plate, which serves for attachment of the muscles which regulate the movement of the ventral valve and from which the ventral valve arises. Beneath the valves, there is a further cavity, the atrium and, from here, the broad outer tracheae arise, extending inwards on either side of the body and then dividing into several finer branches (Fig. 1.1.2.6.8,A,B). A secondary sclerotisation can be also observed, which arises on either side of muscle plate and which is often particularly pronounced in old specimens. Another typical feature of the spiracles of most soft scale species is the presence of spiracular or stigmatic grooves. These are shallow grooves which extend from the peritreme of each spiracle to the lateral margin of the insect and within which lie a band of disc-pores, generally quinquelocular in structure. At the margin end of this groove, o n e or more stigmatic spines are often present and there may also be a stigmatic cleft.
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vv Ventral view and longitudinal section through the spiracle o f a hypothetical soR scale insect. a- spiracular atrium; dp - disc-pores; dv - dorsal valve; mp - muscle plate; p - peritreme; pc - peritreme cavity; sg - spiracular groove; ss - stigmatic spines; ssr - stigmatic sclerotisation; t - tracheae; vv -ventral valve and 2s- secondary sclerotisation. (After Hodgson, 1995).
Fig. 1 . 1 . 2 . 6 . 7 .
The principal tracheae, which appear as silvery-white tubes in live specimens, arise from the basal part of the atrium and radiate from each spiracle; they are about 5 #m in diameter. These principal tracheae are connected longitudinally (Fig. 1.1.2.6.8,A), while distally they gradually divide into more and more slender branches which ramify throughout the whole body (Fig. 1.1.2.6.8,A). The structure of the tracheae is constant (Fig. 1.1.2.6.8,C) and consists of a cuticular intima forming an inner layer, surrounded by an epithelium and with a connective sheath externally. The intima is composed of
Section 1.1.2.6 references, p. 89
82
Morphology
Fig. 1.1.2.6.8. Pulvinaria regalis Canard, adult female, tracheae, SEM micrographs. A - Tracheae arising from the atria of the anterior and posterior spiracle, x200. B - Trachea arising from a spiracular atrium, x800. C - Cuticular part of a trachea after treating with KOH, xl,900; ci = cuticular intima; tc = tracheal cell. D,E - Fine structure of a trachea showing the helicoidal pattern of the taenidial threads, xS,000; x30,000; tth = taenidial threads.
83
Internal anotomy of the adult female
the epicuticle and taenidium. The taenidial threads are arranged in a helical pattern, each helix being in close contact with the adjacent one, with only a very small intertaenidial space (Figs 1.1.2.6.8,D,E). This structure gives great flexibility to the trachea. The epithelium surrounding the intima is formed by the tracheal cells, which are fiat and elongated along the axis of the trachea and which are joined by gap junctions at their apex. Their cytoplasm contains mitochondria, ribosomes and numerous microtubules. A relatively thick connective sheath surrounds the tracheal epithelium.
EXCRETORY SYSTEM The function of the excretory system, which stores the waste products of metabolism and ensures their elimination, thus regulating the salt and water balance, is performed by the Malpighian tubules. The adult females possesses two Malpighian tubules. These lie dorsally within the haemocoel and become united before they open into the posterior part of midgut (Fig. 1.1.2.6.4). They are brownish-yellow in colour and their outline appears sinusoidal (Fig. 1.1.2.6.1,A). In live insects, a peristaltic movement along the tubules can be seen. The walls of the Malpighian tubules are formed from a single layer of cells. Studies of their ultrastructure have shown that, as in the Diaspididae, two types of cells can be distinguished, one with well-developed extracellular channels in their basal region, associated with numerous mitochondria (and therefore characteristic of transporting epithelia), while the cytoplasm of the other cells contains numerous spherites and various other inclusions which are involved in the accumulation of substances from general metabolism (Foldi, 1990).
NERVOUS SYSTEM The nervous system of soft scales, as in other groups of scale insects, is quite condensed. Precise, detailed descriptions of the nervous system of the females of several scale insect groups, including that of the soft scale Pulvinariella mesembryanthemi, have been given by Pesson (1944). He showed that the nervous system consisted of the brain, suboesophageal ganglion and the thoracic and abdominal ganglia (Fig. 1.1.2.6.9). The
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brain suboesophageal ganglion Fig. 1.1.2.6.9. Nervous system of Pulvinariella mesembryanthemi (Vallot) (After Pesson, 1944). an - abdominalnerve; antn - antennal nerve; d - deutocerebron; hn - hypopharyngialnerve; in - labial nerve; mdn.mxn - mandibular and maxillary nerves; nl - nerves of legs; Olin - optical nerve; p - protocerebron; t - tritocerebron.
Section 1.1.2.6 references, p. 89
Morphology
84
brain and suboesophageal ganglion are connected by long oesophageal nerve commissures (Fig. 1.1.2.6.9). The brain is composed of three centres corresponding to the three pairs of ganglia, the protocerebron, deutocerebron and tritocerebron. The tritocerebron appears to be rather isolated from the deutocerebron. Later, Bielenin (1963) described the nervous system of Parthenolecanium pomeranicum in which the brain is piriform in shape, small and flattened, 0.1 mm long and 0.11 mm broad, and in which the ganglia of the suboesophageal chain are unified into a single mass orientated along the axis of the body. The nerve cells are concentrated in the periphery of the brain and the neurosecretory cells are found in the dorsal part of the protocerebrum. The corpora allata is a large paired body, 0.0743.2 mm by 0.243.05mm depending on age, and is located dorsal to the brain. The cells of the corpora allata are slightly elongated and their cytoplasm contains numerous secretory vesicles. The corpora cardiaca is located anterior to corpora allata as two strings of cells.
FEMALE REPRODUCTIVE SYSTEM The external genitalia have been completely lost in the female of the Coccidae. A drawing of the internal female reproductive system of Chloropulvinaria (Pulvinaria) floccifera (Westwood) is presented in Fig. 1.1.2.6.10 and parts of the ovary as seen by SEM are shown in Fig. 1.1.2.6.12.
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//conlmon oviduct vagina vaginal (accessory)glands vulva
Fig. 1.1.2.6.10. General organization of the female reproductive system of Chloropulvinariafloccifera (Westwood).
Internal anatomy of the adultfemale
85
The basic organisation consists of two ovaries, each with a simple lateral oviduct of endodermal origin, joined to a very short common oviduct of ectodermal origin. This oviduct is attached to the vagina (which is longer than the oviduct), into the dorsal part of which a single spermatheca opens at the point where the lateral oviducts unit. More posteriorly, there are usually four vaginal (accessory) glands present, arising posteriorly around the vagina (Figs 1.1.2.6.10, 1.1.2.6.12).
trophic chamber
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B vestibular cell Fig. 1.1.2.6.11. Chloropulvinariafloccifera (Westwood). A - Diagrammatic illustration of the cell structure of the ovarioles before vitellogenesis. B - Diagrammatic illustration of the cell structure of the ovarioles after vitellogenesis.
Fig. 1.1.2.6.12. C~goropulvinariafloccifera (Westwood). SEM micrographs (A,B) of a portion of an ovary showing the ovadoles, the spermatheca and the vaginal (accessory) glands, x160; x l l 0 . vg - vaginal, (accessory) glands.
Section 1.1.2.6 references, p. 89
86
Morphology
The female gonads of soft scales are of the teletrophic type, which is common in all other scale insects. This type is characterised by each ovariole producing only one oocyte, by the nurse cells (trophocytes) being located in the germarium and by the nutrients for the developing eggs being produced by a nutritive cord (Figs 1.1.2.6.11,A,B). Each ovary bears numerous ovarioles which are directly attached to the lateral oviducts by a pedicel (Figs 1.1.2.6.11,A,B). The ovarioles vary in size and shape according to their developmental stage but, contrary to the situation found in the Diaspididae (where the more developed ovarioles are located at the apex of the ovary), the age of the ovarioles is mixed along the length of the ovary in soft scale insects. Basically, each ovariole is composed of three elements: (1) atrophic chamber, composed of three nurse cells located at the apex of each ovariole; (2) the egg chamber or vitellarium, which contains a single oocyte connected by a nutritive cord to the nurse cells, and (3) follicular cells, which surround the oocyte and which form the pedicel connecting the ovariole to the oviduct (Fig. 1.1.2.6.11,B) (Foldi, 1990). Another unusual type of cell, the vestibular cell, can be observed at the base of the pedicel of each ovariole. These cells are also called Krassilshschik's cells and were also observed by Bielenin (1962) in Parthenolecanium pomeranicum. These cells are thought to either play the trophic role of nourishing the spermatozoa (Tremblay, 1960; Bonafonte, 1979) or they may assist in the transport of the sperm from the oviduct to the ovariole (Pesson, 1948; Bielenin, 1962) (Fig. 1.1.2.6.11,B). Whichever is the case, fertilization is in situ, requiring the spermatozoa to reach the oocyte. It is here considered likely that the vestibular cells probably play both roles, because mating usually takes place when the oocytes are immature and, at this time, each vestibular cell could receive 10-15 spermatozoa and then migrate to the base of an ovariole, where it could take on its trophic role while the oocytes mature. The nurse cells, the oocyte and the prefollicular cells originate in an initial bud composed of five cells. One of these cells is of mesodermic origin and gives rise to the prefollicular cells, which later give rise to the follicular cells. The other four cells are sister cells which originate from two successive mitotic divisions of the initial oogonia, one cell of which differentiates into an oocyte and the other three cells into nurse cells. The nurse cells contain numerous ribosomes, a little rough endoplasmic reticulum and mitochondria. Whilst the oocyte is growing, it is connected to the nurse cells via the nutritive cord, thus assuring the necessary nutrition for egg development. The nutritive cord is mainly composed of many microtubules oriented along the longitudinal axis and interspersed with numerous ribosomes. A few mitochondria and, more rarely, some cistemae of rough endoplasmic reticulum have also been observed, identical to those observed in the Diaspididae (Fig. 1.1.2.6.11,B). Apparently, the lipids and protein yolk are formed by an identical mechanism to that observed in diaspidids. The interface between the follicular cells and oocyte is characterized by the presence of large microvilli and by intense pinocytotic activity on the oocyte surface. During viteUogenesis, numerous lipid droplets and proteid yolk spheres are formed in the oocyte cytoplasm. At the moment of mating, the ovarioles are so numerous that they can occupy almost the whole body. The follicular cells at the end ofviteUogenesis secrete the chorion around the egg. Bielenin (1962) found that a female of P. pomeranicum laid between about two and three thousand eggs. The lateral oviducts have a single layer of epithelial cells without a cuticular intima. At their junction, a very short common oviduct is formed and the epithelial cells are covered by a thick cuticular intima. At this point, the spermatheca (seminal receptacle) is connected by a short canal to the ventral side of the oviduct. Each spermatheca is spherical in shape and 200-250 #m in diameter. Its wall is formed by a single layer of tall cylindrical cells covered by a thick cuticular intima. The duct of the spermatheca is surrounded by a thick, circular muscular layer. After mating, the sperm bundles are received and stored in the spermatheca. According to Tremblay (1960) and Bonafonte (1979), the spermatheca also has the function of breaking down the sperm bundles into their constituant spermatozoa. The vagina is about 300 #m long and 200 /xm in
Internal anatomy of the adultfemale
87
diameter, its epithelial cells have a cuticular intima and the lumen is irregular in shape. The circular muscles around the vagina are very well developed. Two semicircular lobes within the lumen of the vagina of P. pomeranicum were observed by Bielenin (1962). The four vaginal (accessory) glands at the base of the vagina are located symmetrically and orientated around the long axis of the vagina (Fig. 1.1.2.6.10). Each gland is composed of 8-12 glandular cells, whose cytoplasm contains rough endoplasmic reticulum, mitochondria, Golgi apparatus and numerous vacuoles. The cells also have well-developed invaginations in the plasmic basal membrane and have microvilli at their apex, identical to those found in the oviductal gland of Porphyrophora crithmi Goux (Foldi, 1986). The receptor ductule opens distally into a narrow ductule which passes through the thick layer of circular muscles and penetrates between the vaginal cells, opening into the lumen of the vagina. Recently, a short study was made of the structure of the spermatheca and vaginal glands by De Marzo et al. (1990) to determine whether there are evolutionary trends in the structure of the reproductive system of the Coccoidea, using 28 species from 11 families. Among the various types of reproductive system found, the Y-shaped system was considered to be ancestral (i.e. with a spermatheca in the proximal position and with 2 or 4 vaginal glands, as found in Pseudococcus longispinus (Targioni Tozzetti) (Pseudococcidae) and similar to that describexl above for the Coccidae.
MALE REPRODUCTIVE SYSTEM The internal reproductive system of the adult male consists a pair of small, slender, elongated testes, a seminal duct and an ejaculatory duct. The epithelial cells forming the sheath of the testes are characterized by a well-developed rough endoplasmic reticulum, with mitochondria and microvilli at their apex. A transverse section of the testis shows that the lumen contains numerous sperm bundles in a liquid, each sperm bundle containing 8-12 spermatozoa. The external parts or copulative structures of the reproductive system consists of an aedeagus and a genital style. A transverse section of aedeagus shows that it is a simple structure, consisting of an outer thick cuticular wall enclosing the ductus seminis, which is formed from two membranes. The aedeagus is located ventrally in a strongly sclerotize~ genital style. In cross section, each lateral part of the genital style has a cavity containing the neurons which probably control the mechano-sensory functions, as in the Diaspididae (Foldi, 1990).
ANAL APPARATUS In the soft scales, the elimination of the products of metabolism, i.e. the honeydew, which have been stored in the rectum, is performed by an anal apparatus. This device propels drops of a viscose, sugary liquid (called honeydew) away from the body to a distance of up to 10 to 15 mm or more, thus avoiding self-contamination. The accumulation of honeydew can be harmful to other conspecific individuals and to the host plant. Thus, young scales can become trapped and/or asphyxiated in the honeydew, while it can also serve as a substrate for the development of sooty molds, which can severely reduce the rate of photosynthesis. Nonetheless, this disposal mechanism is inefficient in dense colonies, because the eliminated honeydew contaminates neighbouring individuals. Under these circumstances, it is clear that the action of ants
Section 1.1.2.6 references, p. 89
Morphology
88
Fig. 1.1.2.6.13.
SEM micrographs of successive steps in the ejection of a honeydew droplet by by the anal apparatus. A - anal plates starting to open and anal robe starting to evert, x700. B - detail of the wall of the anal tube, x3,000. C - anal plates completely opened, x600. D - everted anus, showing six anal ring setae with wax strands and a droplet of excreted honeydew, xS00. E - lateral view of everted anus, showing wax covered anal ring setae and honeydew droplet, x450. F - everted anus without droplet, showing the wax covered anal ring setae, xS00. G - anal ring setae with wax strands, x1600. H - highly magnified view of wax strands on an anal ring seta, x6000. I - internal view of the stout anal ring, showing the numerous wax-secreting pores, xl,300.
Chloropulvinariafloccifera (Westwood)
Internal anatomy of the adult female
89
in removing this material and/or the selection of the under-surface of leaves on which to settle, so that the droplet falls away, is highly advantageous. The anal apparatus lies at the inner end of an internal anal tube and consists of an anus surrounded by a sclerotized anal ring with a variable number of wax coated anal ring setae and covered, when not evened, by a pair ofanal plates (Fig. 1.1.2.6.13,A). This anal ring is an enlarged, stout, cuticular ring bearing numerous wax gland pores (Fig. 1.1.2.6.13,I) through which wax glands secrete long, white waxy filaments which coat the entire length of each anal ring seta (Figs 1.1.2.6.13,G,H). This wax on the anal setae protects them from contamination with the honeydew during the process of elimination. At the moment of elimination , the anal plates open dorso-laterally (Fig. 1.1.2.6.13,C), allowing the complete eversion of the anal tube, so that the tube is totally external with the now evaginated anus at its extremity and with the wax-coated setae splayed (Figs 1.1.2.6.13,D,E,F,G). A spherical droplet of honeydew appears from the anus and its ejection is by the rapid withdrawal of the anal tube into the body, forcing the splayed anal ring setae to close, thus catapulting the liquid droplet away from the body (Williams and Williams, 1980). However, occasionally the present author has also observed propulsion of the honeydew droplet away during the eversion of the anal tube (rather than during its withdrawal), the very rapid eversion being accompanied by a powerful opening of the anal ring setae, the two processes catapulting the droplet away from the insect.
REFERENCES Balachowsky, A., 1937. Les Cochenilles de France, d'Europe, du Nord de l'Afrique et du Bassin Mediterran6en. Vol.2. Caract~res g6n6raux des Cochenilles. Morphologie interne. Actualit6s Scientifiques et Industrielles, no. 564: 1-129. Baranyovits, F., 1953. Some aspects of the biology of armored scale insects. Endeavour, 12: 202-209. Berlese, A., 1894. Le cocciniglie Italiane viventi sugli agrumi, Parte II. I Lecanium. Rivista di Patologia Vegetale, 3: 49-100. Bielenin, I., 1962a. Anatomical and histological investigations on the genus Lecanium Burro. Part I. Female reproductive organs ofLecanium pomeranicum Kaw. (l-lomoptera, Coccoidea). Acta Biologica Cracoviensia, 5: 9-25. Bielenin, I., 1962b. Anatomical and histological investigations on the genus Lecanium Burm. Part II. The male reproductive organs of Lecanium pomeranicum Kaw. (Homoptera, Coccoidea). Acta Biologica Cracoviensia, 5: 125-140. Bielenin, I., 1963a. Anatomical and histological investigations on the genus Lecanium Burro. Part IIl. The nervous system of Lecanium pomeranicum Kaw. (Homoptera, Coccoidea). Zoologica Poloniae, 13: 185-219. Bielenin, I., 1963b. Anatomical and histological investigations of the genus Lecanium Burro. Part IV. The alimentary canal of Lecanium pomeranicum Kaw. (Homoptera, Coccoidea). Zoologica Poloniae, 13: 221-253. Bonafonte, P., 1979. Structure du sperme et migration des spermatozoides duns les voies g6nitales femelles de Chrysomphalusficus (Homopt., Diaspididae). Annales de la Soci&6 Entomologique de France, 15: 505512. Bourgoin, T., 1986a. Morphologie imaginale du tentorium des Hemiptera Fulgoramorpha. International Journal of Insect Morphology and Embryology, 15: 237-252. Bourgoin, T., 1986b. Valeur morphologique de la lame maxillaire chez les Hemiptera; Remarques phylogenetiques. Annales de la Soci6t6 Entomologique de France, 22: 413-422. De Marzo, L., Romano, V. and Tranfaglia, A., 1990. Types of the female reproductive system in some scale insects (Homoptera: Coccoidea). Proceedings of the Sixth International Symposium of Scale Insects Studies, Cracow, August 6-12, 1990, Part II: 41-46. Denis, J. and Bitsch, J., 1973. Morphologie de la tSte des Insectes. In: P.P. Grass6 (Editor), Trait6 de Zoologic, VIII (1). Masson et Cie, Paris, pp. 1-593. Foldi, I., 1972. Donn6es ultrastructurales et histochimiques sur le tube digestifet en particulier sur la chambre filtrante de deux Cochenilles, Icerya purchasi Mask. et Planococcus cirri Risso (lnsecta, Homoptera). Th~se de Doeteur-Ing6nieur h l'Universit~ de Paris VI. 1-82 + 24 plates. Foldi, I., 1973. Etude de la chambre filtrante de Planococcus citri (lnsecta, Homoptera) Histochimie et ultrastructure. Zeitschrift fiir Zellforschung und Microscopische, 143: 549-568.
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Morphology Foldi, I., 1986. Ultrastructure et histochimie des glandes oviductales de la cochenille Porphyrophora r (Homoptera, Margarodidae). Annales de la Soci~t~ Entomologique de France (N.S.), 22: 145-151. Foldi, I., 1990. Internal anatomy. In: D. Rosen (Editor), Armoured Scale Insects, their Biology, Natural Enemies and Control. Vol. A. Elsevier Science Publishers, Netherlands, pp. 65-80. Hamilton, F.G.A., 1981., Morphology and evolution ofthe rhynchotan head (Insecta: Hemiptera, Homoptera). Canadian Entomologist 113: 953-974. Hodgson, C.J., 1995. Observations on the structure of the spiracles of adult female Coccidae. Israel Journal of Entomology, 24: 47-55. Parsons, M.C., 1964. The origin and development of the Hemipteran cranium. Canadian Journal of Zoology, 24: 409-432. Parsons, M.C., 1974. The morphology and possible origin of the Hemiptera loral lobes. Canadian Journal of Zoology, 52: 189-202. Pesson, P., 1935. Contribution ~ l'~tude du tube digestif des Coccides. Bulletin Biologique, 69: 138-152. Pesson, P., 1944. Contribution ~ l'I~ude Morphologique et Functionnelle de la TSte, de l'Appareil Buccal et du Tube Digestif des Femelles de Coccides. Monographie. Centre National de Recherches Agronomiques, Service de Documentation, Versailles, 266 pp. Pesson, P., 1950. Sur un ph~nom~ne de phot~sie des spermatozoides par des cellules d'origine oviductaire, chez Aspidiotus ostreaeformis Curt. (Coccoidea, Diaspidinae). Proceedings of the VIIlth International Congress of Entomology, Stockholm, 1948, pp. 566-570. Pflugfelder, O., 1939. Coccina. In: Bronns H.G. (Editor), Klassen und Ordnungen des Tierreichs, V. Arthropoda, 3. Insecta. Leipzig. pp. 1-121. Tremblay, E., 1960. Ciclo cromosomico e simbiosi endocellulare nella Diaspis (= Pseudaulacaspis) pentagona Targ. Bolletino del Laboratorio di Entomologia Agraria "Filippo Silvestri" Portici, 18:151-225. 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) 1997 Elsevier Science B.V.
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1.1.2.7 Ultrastructure of Integumentary Glands IMPU~ FOLDI
INTRODUCTION Although the important role played by wax glands in the life of scale insects was appreciated by the earliest coccidologists, e.g. Berlese (1894), Ferris (1928), Steinweden (1929), ~ulc (1932), Balachowsky (1937), Pesson (1951) and Benassy (1961), a better understanding of their structure has become possible with the availability of transmission and scanning electron microscopy. Amongst the Coccoidea, it is members of the family Coccidae which have the most diverse range of wax gland systems. Five basic structures have been identified within the superfamily Coccoidea (Foldi, 1991). All five are known in some species but generally they occur in various combinations, while their frequency per individual can vary from less than a hundred to several thousand, distributed either throughout the dorsum and venter or restricted to specific areas, such as near the vulva, anus, spiracles or margin. Many are so small that no pore opening can be seen under the light microscope and their presence is only indicated by the wax they secrete. The great diversity and abundance of the pores and ducts through which these gland systems secrete their wax makes them important taxonomic features, particularly as they are the main cuticular characters which remain once a specimen has been treated with KOH. Their distribution and f'me structure are important taxonomic characters not only at the specific level but provide important characters which can be used to demonstrate wider relationships within the Coccoidea. With the ever increasing power of the computer, it should become possible to store data on the structure of these pores and ducts in great detail and to use it for taxonomic and classificatory purposes. These glands in the Coccidae secrete a diverse range of waxes which vary in quantity, shape, size and chemical constitution, but the function of the waxes is thought to be mainly protection, either of particular structures, such as the eggs, vulva, spiracles, anal complex or respiratory pathways, or the entire body, as with the thick body wax of the Ceroplastinae. In the latter case, the wax can be so abundant that it can engulf the entire colony, the only link between the insects and the outer environment being the wax tunnels produced by the spiracular glands (Figs 1.1.2.7.1,A,B,C), as in Gascardia madagascariensis Targioni Tozzetti and all Ceroplastes species, and in the nonceroplastine Ericerus pela (Chavannes). Indeed, the wax produced by the 2nd-instar males of E. pela is so abundant that it is collected commercially for a number of valuable industrial uses because of its light melting point (80-85~ (see Section 1.2.3.2).
Section 1.1.2.7 references, p. 109
92
Morphology
Fig. 1.1.2.7.1. A - Colony of Gascardia madagascariensis, x20, and B - a colony of 2nd-instar male Ericerus pela (Chavannes), xS, embedded in masses of amorphous wax. C - Ceroplastes sp., xl0, adult females. D, E and F - Coccus hesperidum L., adult female: amorphous secretion on the dorsum forming numerous superimposed layers, xl0, x200 and x300. G - Saissetia coffeae (Walker), adult female: spiracular disc-pores (5-1ocular) extruding C-shaped filaments of wax, x14,000. H - Saissetia coffeae (Walker), adult female: SEM micrograph of ventral view of spiracular seta showing secretion from spiracular seta (an'owed) and from spiracular disc-pores, x6,000.
Ultrastructure of integumentary glands
93
The structure of the integumentary glands in relation to their secretory function has been extensively studied in Coccidae by Foldi (1978, 1983, 1991), Waku and Foldi (1984), Foldi and Cassier (1985) and by Foldi and Pearce (1985). The present Section is based on these observations and on some previously unpublished information and illustrations.
THE IMPORTANCE OF WAX GLAND STRUCTURE IN THE CLASSIFICATION OF THE COCCIDAE
Importance of the cuticular structures Wax glands play a major role in soft scale taxonomy due to their great diversity, distribution, frequency and constancy of form. Usually their cuticular structure is well preserved in slide-mounted specimens and is important taxonomically both at the species and genetic level where it is considered that taxa sharing particular combinations are probably more closely related than those not sharing them. However, quantitative data on the frequency of these structures is one of the most neglected parameters in many taxonomic descriptions. I have tested the frequency of certain gland systems in several species and they appear to be relatively constant. Individual variation is slight, usually less than 10%, and it is strongly recommended here that the frequency of each gland system should be indicated in species descriptions.
Description and terminology There are three basic cuticular structures involved in the transport and extrusion of wax secretions - (i) pores, (ii) ducts and (iii) ductules. The current terminology describing these in the Coccidae is based on the structure of the cuticular parts as seen under the light microscope but, whilst often simple, these terms or names do not always express the true structural characteristics. For example, the terms dorsal microductule (Fig. 1.1.2.7.2,C - common to all Coccidae) and 8-shaped pore (common in the pit scales, Asterolecaniidae) appear to designate two entirely different gland systems. However, in reality, their general organisation is very similar and each has the same basic structure (Foldi and Lambdin, 1995). Thus, it is important that the terms chosen to describe particular structures are suitable for use both between and within families and also in evolutionary and phylogenetic studies. a. Pores (Figs 1.1.2.7.2, 1.1.2.7.3, 1.1.2.7.5,F). Pores are specialised cuticular structures through which particular secretions (usually waxes) are extruded. The term pore can be confusing because it implies either an obvious opening, such as found with ducts and ductules which have a true orifice, or the openings of simple or multilocular disc-pore glands which have closed pores (see below). In reality, there are three types of pores: (1) open pores: true pores, with a single distinct opening or orifice, typically associated with ducts and ductules (Figs 1.1.2.7.2, B, C, D, E, F); (2) locular pores: pores with several distinct micro-orifices or loculi which are clearly visible under the light-microscope but in which the inner base of each loculus is closed by a narrow layer of modified, porous cuticle through which the wax is secreted (Fig. 1.1.2.7.2,A), and (3) closed pores: pores which are completely covered by cuticle and appear to lack any obvious orifice under the light microscope. However, this cuticular cover is porous and is modified to permit the passage of various secretions. Closed pores always lack ductules and are generally sessile, with either a smooth or granular surface. They are usually flat and circular, but may be of various shapes and sizes, some being either convex or concave. Simple pores (Fig. 1.1.2.7.5,F) are closed pores but generally have numerous micro-orifices on their surface when viewed by SEM.
Section 1.1.2.7 references, p. 109
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Morphology
Fig. 1.1.2.7.2. General organization and histology of six basic types of wax glands in the Coccidae.
Ultrastructure of integumentary glands
95
Fig. 1.1.2.7.3. A - Choloropulvinariafloccifera (Westwood), adult female: multilocular disc-pore, external view, x12,000. B - Ditto: internal view, xl 1,000. C - Pulvinaria regalis Canard, adult female: multilocular disc-pore with a slit central loculus, x13,000. D - Saissetia oleae (Olivier), adult female: wax secretion extruded from multilocular disc-pore, x7,000. E - Ceroplastes s/nens/s Del Guercio, adult female: trilocular spiracular disc-pore, x12,000. F - Ditto" quadrilocular spiracular disc-pore, x 2 0 , 0 ~ . G - Ditto: quinquelocular spiracular disc-pore, x9,000. H - Etiennea petasus Hodgson, adult female: internal view of a ventral microduct, xl 1,000.
96
Morphology
Ultrastructure of integumentary glands
97
The use of the terms open and closed to describe these types of pores facilitates the description of complex pore systems, particularly where more than one type of pore is present. Thus, the pores of dorsal microductules (Fig. 1.1.2.7.2,C) and ventral microducts, which are minute, 8-shaped pores, are composed of a central simple open pore, through which an inner ductule opens, and two lateral closed pores which have no obvious orifices on their surface. b. Ducts (Figs 1.1.2.7.2,B, 1.1.2.7.3,H, 1.1.2.7.4, 1.1.2.7.7,B). The term duct is used to describe an invaginated cuticular tube. These can be of various shapes and sizes, but always consist of two distinct parts, an outer and an inner ductule. The outer ductule opens to the exterior through the cuticle by an open pore and is generally stouter and longer than the inner ductule. The inner ductule is generally narrower and arises from the side of the outer ductule and terminates with a more or less well-developed knob. The shape, size, length and width of the inner and outer ductules and their distribution are all of taxonomic significance. In addition, the inner end of the outer ductule is invaginated and this invagination, which is cup-shaped, also varies in shape, depth, width and thickness between species. De Lotto (1969, p. 413) proposed the term clistostomatic for the tubular ducts of the Coccidae but this term is confusing and should be avoided. When there is no inner ductule, the structure is termed a tubular pore. In some modified ducts, such as the ventral microduct, the inner ductule arises from the centre of the inner end of the microduct. c. Ductules (Figs 1.1.2.7.2,C, 1.1.2.7.4,D, 1.1.2.7.6, 1.1.2.7.9) This term is used to describe small, cuticular tubes which are not divided into an outer and an inner part. Ductules are usually parts of larger structures, as in the dorsal microductule glands or the Ceroplastes-type glands, or are openings into a cuticular tube as in some dorsal tubercles. However, they can also be separate structures, such as the filamentous ductules in some Ceroplastes species. The term filamentous duct was proposed by Kawai and Tamaki (1967) to def'me slender branched tubules which occur on the submargin of Ceroplastes ceriferus (Fabricius) and C. sinensis Del Guercio (Figs 1.1.2.7.4,D, 1.1.2.7.9,A,B). The ductule in soft scale insects varies considerably in shape and size and their structure and presence or absence are important taxonomic characters.
CUTICULAR STRUCTURES ASSOCIATED WITH THE WAX GLANDS The integument of soft scales may have at least seven types of wax pores and a few have even more. These are separable based on their cuticular structure as seen under the light microscope, as follows: i. Simple pores (Fig. 1.1.2.7.5,F): these are always without ducts and ductules and are usually round, minute, closed pores when observed under the light microscope.
Fig. 1.1.2.7.4. A - Etiennea petasus Hodgson, adult female: tubular duct showing terminal knob, x5,000 and x12,000. B - Messinea conica De Lotto, adult female: invaginated inner end of outer ductule of tubular duct showing a centrally located cuticular projection, apparently similar in structure to those of pit scale, x I 1,000. C - Chloropulvinaria psidii 0Vlaskell), adult female: tubular duct with a thin inner ductule, x7,000. D Ceroplastes ceriferus (Fabricius), adult female: filamentous ductule of the type distributed around the margin of the body, x2,000. E - Saissetia oleae (Olivier), adult female: tubular duct with an broad inner ductule, x8,000. F - Eulecanium cerasorum (Cockerell), adult female: ventral tubular duct with a large terminal knob, xS,000. G - Chloropulvinaria floccifera (Westwood), adult female: ventral tubular duct with long inner ductule, x5,000.
Section 1.1.2.7 references, p. 109
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Morphology
Fig. 1.1.2.7.5. A - Dorsal tubercle of Etiennea petasus Hodgson, x2,500. B - Dorsal tubercle of Parthenolecanium persicae (F.), x4,000. C - Dorsal tubercle ofAnopulvinaria cephalocarinata da Fonseca, x3,000. D - Dorsal tubercle of Etiennea villiersi Matile-Ferrero, x2,500. E - Ceroplastes sinensis Del Guercio, adult female: preopercular closed pores anterior to anal plates, x7,000. F - Coccus hesperidum Linnaeus, adult female" dorsal simple closed pore x15,000.
However, viewed by SEM, it is clear that the surface of these pores has numerous micro-orifices, as in Coccus hesperidum L. Simple pores are generally fiat, their surface level with the derm, and are randomly distributed over the dorsum.
ii. Dorsal microductules (Figs I. 1.2.7.2,C, 1.1.2.7.6): these are randomly distributed over the dorsum, frequently in the middle of an areolation. The pore of each microductule opens at the base of a shallow cavity in the cuticle. In C. hesperidum, each consists of a central open pore with a closed pore on either side, often giving a bilocular or 8-shaped appearance not unlike the minute 8-shaped pores of pit scales.
Ultra.structure of integumentaryglands
99
iii. Spiracular disc-pores (Figs 1.1.2.7.1,H, 1.1.2.7.3,E-G): these are circular pores, generally with 5-1oculi and are frequently called quinquelocular pores, but they may occasionally have from two to ten or more loculi. Spiracular disc-pores occur either as a band between the spiracular peritreme and the margin or are associated with the spiracles. iv. Multilocular disc-pores (Figs 1.1.2.7.2,A, 1.1.2.7.3,A-D): these are basically similar to spiracular disc-pores but usually have from seven to ten or more loculi and are generally most abundant around the vulva opening (thus the term pregenital disc-pores of Hodgson (1994)), although they may be found throughout the venter. v. Ventral microducts (Figs 1.1.2.7.2,D, 1.1.2.7.3,H): these are minute open pores located at the base of a 3-4/~m deep outer ductule and which have a short, usually broad, inner ductule. They are most frequent in a sparse submarginal band and near the mouthparts, but can be found apparently randomly throughout the venter in many species.
vi. Preopercular pores (Fig. 1.1.2.7.5,E)" these are closed pores and are generally found on the dorsum in a group anterior to the anal plates but can be more widespread over the dorsum. They are variable in size and shape between species and can be identical to simple pores, as in some Pulvinaria and Coccus species. vii. Tubular ducts (Fig. 1.1.2.7.4,A-G): these consist of, relatively long (5-15#m) outer and inner ductule, the latter possessing a terminal knob and arising from the margin of the cup-shaped invagination of the latter. They may be found almost anywhere on the dorsum or venter but are most frequent in a ventral submarginal band. In addition to these seven types, several other types of pore may be present, such as dorsal tubercles and cribriform plates but these tend to be limited to a few genera. viii. Dorsal tubercles (Figs 1.1.2.7.2,E, 1.1.2.7.5,A-D): these are large, usually strongly convex structures, generally distributed on the submargin. They are considered to represent the most complex glands observed in soft scale insects (cf. the satellite wax glands of Foldi, 1991). ix. Cribriform plates" these are large, sclerotized plates with numerous orifices on their external surface, which are usually round but may be shaped otherwise, as in Eutaxia in which the orifices are elongated and curved (Hodgson, 1994). The following paragraphs describe the structure of each type of gland and then discusses their function in the life of the insect.
WAX GLANDS ASSOCIATED WITH THE SPIRACLES AND SPIRACULAR FURROWS The main type of pore associated with the spiracles is a wax gland with a 5-1ocular disc-pore which usually occurs in a band between the spiracles and the margin. The number of these pores in each band varies but Coccus hesperidum L. has between 20-30 and ToumeyeUa pini (King) has over 300. However, whilst these glands generally have five loculi, it can vary between species. In most species, the loculi are approximately round, but Ceroplastes sinensis may have only three or four loculi per pore, each loculus
Section 1.1.2.7 references, p. 109
Morphology
100
rather irregular in shape, whilst Pseudophilippia quaintancii Cockerell has pores with two to six irregularly shaped loculi. Some species have even more loculi, such as in Toumeyella cerifera Ferris which has 10 loculi per spiracular disc-pore. 1. T h e s p i r a c u l a r s e t a e (Fig. 1.1.2.7.1,H). At the point where the band of 5-1ocular disc-pores meets the margin, there are frequently groups of setae which are differentiated from marginal setae. These are termed spiracular spines or setae and the most frequent number in each group is three. These setae secrete wax strands along their length, the secretion being extruded through minute pores located in lines on either side of each seta (Foldi and Pearce, 1985). Each strand curls downwards and inwards, giving the appearance of a feather. These strands are secreted in regular bursts and then appear to become joined laterally at a point along their length.
2. The 5-1ocular wax glands i. Cuticular structures (Figs 1.1.2.7.3, 1.1.2.7.7,A). Each of these pores consists of a round, cuticular, sessile pore, whose diameter varies between 4-8 #m, and which has five circular loculi or micro-orifices, each with a diameter of about 0.2 #m, arranged in a circle. These pores are served by a gland system consisting of a common reservoir and eight glandular cells. Under high magnification, each loculus can be seen to consist of a small, elongated, cuticular structure with an elongate opening. These openings act as moulding devices which determine the shape and structure of the secreted wax. However, during secretion, the wax first passes from the common reservoir of the gland system through the modified cuticle found at the base of each loculus. This modified cuticle is made of endocuticle and epicuticle. The endocuticle consists of a network of fine tubular structures, 2030 nm in diameter, which is covered by an epicuticle perforated by numerous epicuticular pores about 10 nm in diameter. Numerous short filaments cover the inner side of the endocuticle and these are in contact with the secretion; these are constantly present and resist extraction with pronase. This modified cuticle represents a generalized structure for the transport of wax secretions through the cuticle from the wax gland (Foldi, 1981, 1991).
ii. General structure and cytological characters (Fig. 1.1.2.7.7,A). Each gland of a 5-1ocular pore consists of eight identical glandular cells, arranged in a single circular layer, which is attached to the sclerotised pore both at its periphery and centrally. Each of these glandular cells opens into a large common reservoir which lies beneath the actual pore. The cytoplasm of each cell is characterized by well-developed ribosomes, rough and smooth endoplasmic reticulum, large mitochondria and Golgi bodies. Apically, there are no microvilli. These cells are also characterized by a remarkably well-developed collector network, formed by the invagination of the apical plasma membrane. The outermost part of each invagination is large and circular but becomes slender, with smaller lateral branches ramifying in all directions and into all parts of the cell. The secretion is collected and stored in the large common reservoir, from which it then crosses the modified cuticle located at the base of each loculi. Histochemical studies revealed the presence of lipids and glyco-lipidic substances, particularly in the reservoir. iii. Micromorphology and function of the secretion (Fig. 1.1.2.7.1,G). The wax secreted through the 5-1ocular wax glands is C-shaped in cross-section and forms long curls. These curled filaments form a loose network of material around the spiracles and along the spiracular furrow. The wax is hydrophobic and thus prevents water penetration and facilitates air circulation.
Ultrastructure of integumentary glands
I01
Fig. 1.1.2.7.6. Longitudinal section through a dorsal microductule of Coccushesperidum L., x20,000. Inset: pore of the microductule gland, x16,000, where cu = cuticle, d = ductule, my -- microvilli and p - pore.
102
Morphology
Fig. 1.1.2.7.7. Pulvinaria regalis Canard, adult female. A - Section through a quinquelocular disc-pore gland showing pore (p), common reservoir (cr) and collector network (on) formed by invaginations of apical plasma membrane (ipm), x7,000. B - Section through inner end of outer ductule (od), inner ductule (id) and common reservoir (cr) of tubular duct, xl 1,000.
Ultrastructure of integumentary glands
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VENTRAL WAX GLANDS ASSOCIATED WITH SITES OF REPRODUCTION Two types of wax gland are found ventrally associated with the area around the vulva, namely the tubular duct wax glands and the multilocular disc-pore wax glands. Both are involved in the production of the ovisac and are particularly abundant in species of the tribe Pulvinariini. The ovisac protrudes from the end of abdomen and is composed of a harder external part, which is made with the long filaments produced by the tubular ducts glands, and a looser inner part made from the short curved filaments extruded through the multilocular disc-pore glands. In other taxa, which do not produce an ovisac, the wax produced by these glands is deposited on the ventral abdominal surface and on the eggs.
1. The tubular duct wax glands i. Cuticular structures (Fig. 1.1.2.7.4, 1.1.2.7.7,B). The duet is an invaginated cuticular tube composed of an outer and an inner ductule. The size of the ductules varies. Adult female Chloropulvinariafloccifera (Westwood) have three types of ventral tubular duct, of which one has an outer ductule 12 #m long and 4/~m wide and an inner ducmle 17 #m long and 2/tin wide; the shape of the inner end of the latter is 'flowery-tipped'. The inner end of the outer ductule is invaginated and in most cases strongly sclerotised. The actual shape of the wax secreted depends on the shape of the outer ductule. The invaginated inner end in Messinea conica De Lotto possess a small cuticular projection apparently similar in structure to those of some pit scales (Foldi and Lambdin, 1995). The form of the inner ductule varies between species. For instance, in C. floccifera (Fig. 1.1.2.7.4,G), one of the three ventral tubular duct types has the inner ductule longer than the outer ducmle; in other species, such as Saissetia coffeae (Walker) (Fig. 1.1.2.7.4,E), the inner and outer ductules may both be broad. In addition, the shape of the " flowery tipped "apex of the inner ductule can also vary in size and shape. The external pore is usually a simple circular opening but is hexagonal, with a raised rim, in Pulvinaria regalis Canard.
ii. General organisation and cytological characteristics (Figs 1.1.2.7.2,B). The gland of each tubular duct consists of a central glandular cell at the end of an inner ductule, surrounded by four to six lateral glands which are attached to the inner end of the outer ductule. Each central cell has a reservoir apically, delimited by numerous microvilli and a ductule receptor. The cytoplasm of each central cell is composed ofweU-developed rough, endoplasmic reticulum, ribosomes, mitochondria and Golgi bodies. The lateral cells all open into a common reservoir situated at the inner end of the outer ductule. Each gland is characterised by the presence of rough and smooth endoplasmic reticulum, ribosomes and mitochondria. The apical plasma membrane of these cells is invaginated and forms a collector network identical to that for the 5-1ocular wax glands. Wax secretion from the tubular duct wax glands involves the secretion of wax from the lateral wax glands, which is collected in the common reservoir, from which it then passes through the duct cuticle into the lumen of the outer ductule. This cuticle is located in the cup-shaped invagination at the inner end of the outer ductule and has the same structural characteristics as the modified cuticle describeA for the 5-1ocular wax gland. The secretion from the central cell passes through the ductule receptor into the inner ductule, from where it is transported to the base of the ductule and there becomes mixed with the secretions from the lateral wax glands.
Section 1.1.2.7 references, p. 109
Morphology
104
iii. Micromorphology and function The function of the tubular wax glands in taxa such as the Pulvinariini is to secrete the cottony ovisac which protrudes from the posterior end of the body of the adult female. This ovisac provides the necessary microenvironment for the eggs and newly hatched nymphs, which quickly become desiccated if the ovisac is removed experimentally. It is composed of long strands of wax which are hexagonal in cross section in species of Pulvinaria. Each strand appears to be hollow and thickened at each comer of the hexagon, apparently to give it strength. The filaments can reach up to 10 mm or even longer in length, occasionally up to 25-30 mm if the ovipositing female withdraws its stylets and moves forwards (Foldi and Pearce, 1985). In the former case, where the mouthparts remain in situ, the production of the ovisac can cause the posterior end of the body to rise, reaching an angle of 68 ~ from the substrate in some cases. These wax filaments form the outer layer of the ovisac and provide a solid cover which can even be sticky when touched. Within the ovisac, there is a powdery secretion which covers the surface of the eggs. This latter wax is C-shaped in cross section and is broken into short, curved pieces. It is secreted by the multilocular disc-pores around the vulva. 2 . M u l t i l o c u l a r d i s c - p o r e g l a n d s (Figs 1.1.2.7.2,A, 1.1.2.7.3,A-D). The general organisation and cytological characteristics of the multilocular wax glands are identical to that of the 5-1ocular wax glands described above. The cuticular structure of each disc-pore consists of a circular, sclerotised, cuticular pore, diameter 5-8 #m, with usually 7 to 12 micro-orifices arranged in a circle around a central slit. Each loculus possesses a trifurcate internal secondary structure which causes the wax strands to be C-shaped. The wax is hydrophobic and, when deposited around the eggs, keeps them from sticking to each other and protects them from immersion and desiccation.
WAX GLANDS ASSOCIATED WITH HONEYDEW EXCRETION Soft scale insects are honeydew-producing Homoptera and possess an anal apparatus for the propulsion of this liquid away from the body. This ejection of honeydew droplets is associated with the sudden withdrawal of the wax covered anal setae into the anal tube (see Foldi and Pearce, 1985). This wax on the anal ring setae is produced by glands located on the anal ring, which is located around the anus at the base of an eversible anal tube. In Pulvinaria regalis, the anal ring bears 6 setae and the wax glands are located in a crescent in each half of the anal ring. The wax glands have a special structure, each consisting of a small thimble-like eminence, 4/zm in diameter and 4 #m high, with numerous microstructures on the upper surface. Each pore is encircled by a cuticular wall. The wax secreted by the pores is very narrow, about 0.15 /~m in diameter, and is produced continuously, forming a thick network around each seta.
W A X GLANDS ASSOCIATED WITH DEFENCE The sedentary life of soft scale insects exposes them to various external stresses, such as climate and pollution, as well as injury from predators and parasites. Probably in response to these factors, soft scale insects have evolved a series of external protective covers. The material needed for these is secreted by a variety of dorsal wax glands, the most obvious examples being that secreted by the dorsal glands of Ericerus pela and Gascardia madagascariensis and other Ceroplastinae, which completely cover the insects. In some cases, they are filamentous, woolly secretions which completely cover the scale insect but the majority of soft scales secrete only a thin, amorphous wax in a series of layers or plates, thus increasing the thickness of the dorsum and reinforcing its resistance. These cuticular dorsal pores fall into four main types.
Ultrastructure of integumentary glands
105
Dorsal microductule glands Microductules are usually abundant and uniformly distributed throughout the dorsum, without any regional or specific spatial pattern. i. Cuticular structures (Fig. 1.1.2.7.6). The cuticular pore associated with this glandular system is complex and consists of an ellipsoidal central open pore corresponding to the pore of the ductule and two closed pores placed laterally, associated with the reservoirs of the lateral cells. When observed under the light microscope, the arrangement of these three pores has an 8-shaped image. In Coccus hesperidum, the inner ductule is 7-8 #m long and 0.5 #m in diameter and opens through an oval pore into a small external cavity (Fig. 1.1.2.7.6). The cuticle of the closed lateral pores is modified to allow the passage of wax in a similar manner to that described for the 5-1ocular wax pores above.
ii. General organisation and cytological characteristics (Figs 1.1.2.7.2,C, 1.1.2.7.6). The general organisation of a dorsal microductule is shown in Fig. 1.1.2.7.2,C and is quite different from that of a ventral microduct. Each glandular unit consists of four cells: a central cell, an intermediate cell and two lateral cells. The central cell is narrow, 20-21 #m high and 2 #m wide and is swollen. The basal part is composed of cytoplasm, with a rough endoplasmic reticulum, ribosomes, mitochondria, Golgi bodies and numerous secretory vesicles. Histochemical tests have revealed micropolysaccharide substances in the secretory vesicles. The apical part of the cytoplasm has numerous microvilli extending into an upper reservoir. The small intermediate cell surrounds the filamentous ductule. The basic structure is similar to the central cell, except that numerous dense filaments are present which pass through the wall of the ductule. The cytoplasmic basal part includes some rare organelles, mitochondria, ribosomes and, in particular, microtubules. The two lateral cells surrounding the central cell consist mainly of a basal cytoplasmic region with a collector network which opens into an apical reservoir. The cytoplasm is characterised by the presence of ribosomes, mitochondria, smooth endoplasmic reticulum and less developed rough endoplasmic reticulum. The microtubules are numerous. The apical plasma membrane lacks microvilli, but is deeply invaginated into the cytoplasm, forming an extensive collector network which opens into a small reservoir. Each cell is attached to the cuticle around the cuticular pore.
iii. Micromorphology and function of the secretion (Figs 1.1.2.7.1,D,E,F) The secreted material of the dorsal microductule gland is amorphous. It flows out through the pores and solidifies into small, thin plates. In Coccus hesperidum, the secretion is continuous and results in a number of overlapping, superimposed plates (Figs 1.1.2.7.4, 5 & 6). In Saissetia coffeae (Walker), we have observed 25 overlapping plates. The secretion is transparent and has a smooth surface in young females. In some species, the secreted material is glassy in appearance, as in Inglisia vitrea Cockerell, or may form platelets, as in Pulvinaria ericicola McConnell. The solidified secretion reinforces the dorsal integument, which becomes highly sclerotised in mated females.
Section 1.1.2.7 references, p. 109
106
Morphology
Fig. 1.1.2.7.8. Ceroplastes sinensis Del Guercio, adult female: micrograph of the Ceroplastes-type gland. A - Showing the interpenetration of Gland cells A and B (a, b) and the dense granules of secretion (gr), x19,000. B - Detail of the basal region of Gland cell B, showing the well-developed smooth endoplasmic reticulum (set), x20,000.
Ultrastructureof integumentaryglands
107
Ventral microduct wax glands (Figs 1.1.2.7.2,D, 1.1.2.7.3,H). These are minute glands which are present in almost all Coccidae species. They are very common on the venter and tend to be most abundant in the submarginal areaThe general structure of the ventral microduct is shown in Fig. 1.1.2.7.2,D and is different to that of the dorsal microductule. There is a central glandular cell surrounded by 6-8 lateral glandular cells, and their structure appears to be identical to that of the tubular duct gland (Fig. 1.1.2.7.2,B). The cuticular structures vary slightly between species. Each outer ductule is 2-4/xm deep, with an inner end which is thickened and sclerotized. The pore is usually oval but, in slide mounted specimens, can appear cruciform or more square-shaped, with or without a rimmed orifice. The inner ductule is narrow near the pore opening but broadens sharply and its surface carries numerous finger-like cuticular microstructures (Fig. 1.1.2.7.3,H). The secretion is amorphous.
Ceroplastes-type glands (Fig. 1.1.2.7.2,F, 1.1.2.7.8). These glands appear to be restricted to species of Ceroplastes and related genera. They are very unusual in their general organisation. Each consists of a very large central glandular cell, here referred to as Gland A, which is completely surrounded by another glandular cell, Gland B. These two glands are themselves surrounded by several lateral wax glands. Gland A contains large, dense granules of secretion (Fig. 1.1.2.7.8,A) and has numerous, long, cytoplasmic expansions which are deeply invaginated into Gland B, each expansion containing microtubules and finishing in small cavities at their extremities within Cell B (Fig. 1.1.2.7.8,A). These expansions form a well-developed network which transfers the secretion of Gland B into Gland A. Gland cell A possesses a reservoir which contains an irregularly-shaped receptor ductule. The cytoplasm of Gland A contains a well-developed rough endoplasmic reticulum, ribosomes, Golgi bodies and microtubules and, in particular, a large number of mitochondria. Gland cell B has a very well-developed smooth endoplasmic reticulum (Fig. 1.1.2.7.8,B). The ductule is filamentous with branched, slender tubules (Fig. 1.1.2.7.9). The lateral wax glands exhibits the same characteristics as the central cells of others wax glands and have microvilli, a receptor ductule and a small ductule (Fig. 1.1.2.7.2,F).
Dorsal tubercles (Figs 1.1.2.7.2,E, 1.1.2.7.5,A-D). Dorsal tubercles are the most complex glands found in the Coccoidea and usually occur in a submarginal ring. Each tubercle is composed of several types of gland, all in one structure. Each dorsal tubercle has a central tube located within a cavity, which is surrounded by a circular rim which can have further pores in its surface. These are similar in general organisation to that described as satellite wax glands in Anopulvinaria cephalocarinata da Fonseca (Foldi, 1991). These tubercles generally occur in a ring around the dorsal submargin, spaced at regular intervals. They are present in many species of the genera Coccus, Eucalymnatus, Kilifia, Parthenolecanium, Pulvinaria and Saissetia. The ultrastructural features of the glands are similar to that described above for the central and lateral cells of tubular and 5-1ocular glands. The wax secreted by them is amorphous, forming a flaky mass around each tubercle.
Section 1.1.2.7 references, p. 109
Morphology
108
INTEGUMENTARY GLANDS OF UNKNOWN FUNCTION P r e o p e r c u l a r g l a n d s (Fig. 1.1.2.7.5,E). These are usually situated in a group on the dorsum just anterior to the anal plates, but may occur in a double or single line or without specific pattern. They are always closed pores but are rather variable between ~ i e s and genera. Each pore may be flat and
Fig. 1.1.2.7.9. Ceroplastess/nens/s Del Guercio, adult female. A - Longitudinal section of filamentous duetule, x16,000. B - Transverse section of the filamentous ductule, x26,000.
circular shape, as in most Coccus and Pulvinaria spp., when they are similar to simple pores; or they may be tubercle-like in shape, as in Ceroplastes spp. (Fig. 1.1.2.7.5,E). When observed under the light microscope, each preopercular pore on Ceroplastes sinensis consists of a closed pore, 1.5-2 #m in diameter but, when viewed by s e i n i n g electron microscope at high magnification, the cuticle is seen to have numerous, very small openings. The cuticle is composed of two distinct parts, the epicuticle, which is perforated by numerous minute pores, 7-10 nm in diameter, and the endocuticle which has a dense tubular network, 20-30 nm in diameter. The gland system associated with these pores consists of four identical cells and the ultrastructural characteristics of these cells appear to be similar to that describexl above for the 5-1ocular glands. I have been unable to detect a wax secretion associated with these glands and suggest that it produces a volatile product, probably a pheromone.
Dorsal simple pore glands (Fig. 1.1.2.7.5,F). These are very small (2-3 #m in diameter) closed pores and are often numerous and scattered over the dorsum, without any particular pattern. The pores are of various types, usually fiat and circular, lying at the same level as the surface, but some are slightly convex or concave. They have either a smooth or granular surface and may
Ultrastructure of integumentary glands
109
have a weakly sclerotised rim. In Coccus hesperidum, viewed by SEM, it can be seen that they are closed pores with numerous small openings (Fig. 1.1.2.7.5,F) which allows the passage of the waxy secretions. The glandular cells and general organisation of simple pores appears to be identical to those of other ductless glands. The cells are very small, 5-6 mm deep and 3-4 mm wide, and their cytoplasm is characterised by the presence of smooth endoplasmic reticulum, ribosomes and mitochondria.
REFERENCES Balachowsky, A., 1937. Les Cochenilles de France, d'Europe, du nord de l'Afrique, et du bassin M6diterran6enne. II. Caract~res g6n6raux des Cochenilles. Morphologie interne. Actualit6s Scientifiques et Industrielles, 414: 1-68. Benassy, C., 1961. Les s~cr&ions t6gumentaires chez les Coccid6s. Ann6e Biologique, 37: 321-341. Berlese, A., 1894. Le Cocciniglie italiane viventi sugli agrumi. Parte II. I. Lecanium. Rivista di Patologia Vegetale, Anno In, 1-8: 107-201. De Lotto, G., 1969.On a few old and new soft scales and mealybugs (Homoptera: Coccoidea). Journal of the Entomological Society of Southern Africa, 32: 413-422. Ferris, G.F., 1928. Wax secreting organs of the Coccidae. Pan Pacific Entomologist, 5: 67-70. Foldi, I., 1978. Ultrastructure des glandes t6gumentaires dorsales, s6cr&rices de la "laque" chez la femelle Coccus hesperidum L. (Homoptera: Coccidae). International Journal of Insect Morphology & Embryology, 7: 55-163. Foldi, I., 1981. Ultrastructure of the wax gland system in subterranean scale insects (Homoptera, Coccoidea, Margarodidae). Journal of Morphology, 168: 159-170. Foldi, I., 1983. Les glandes t6gumentaires des Cochenilles. Ultrastructure compar6e et signification 6volutive. Th~se d'Etat, Universit6 Paris VI, 224 pp. Foldi, I., 1991. The wax glands in scale insects: comparative ultrastructure, secretion, function and evolution (Homoptera: Coccoidea). Annals de la Soci6t6 Entomologique de France (N.S.), 27: 163-188. Foldi, I. and Cassier P., 1985. Ultrastructure compar~e des glandes t6gumentaires de treize families de Cochenilles (Homoptera: Coccoidea). International Journal of Insect Morphology & Embryology, 14: 33-50. 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). International Journal of Insect Morphology & Embryology, 14: 259-271. Foldi, I. and Lambdin, P., 1995. Ultrastructural and phylogenetic assessment of wax glands in pit scales (Homoptera: Coccoidea). International Journal of Insect Morphology & Embryology, 24: 35-49. Hodgson, C.J., 1994. The Scale Insect Family Coccidae: An Identification Manual to Genera. CAB International, Wallingford, 639 pp. Kawai, S. and Tamaki, Y., 1967. Morphology of Ceroplastes pseudoceriferus Green with special reference to the wax secretion. Applied Entomology and Zoology, 2:133-146 Pesson, P., 1951. Ordre des Homopt6res. In: P.P. Grass6 (Exlitor), Trait6 de Zoologic, Vol. 10, Masson et Cie, Paris, pp. 1390-1647. Steinweden, J.B., 1929. Bases for the generic classifications of the coccoid family Coccidae. Annals of the Entomological Society of America, 22: 197-245. Sulc, K., 1932. Ceskoslovensk6 druhy rodu puklice (gn. Lecanium, Coccidae, Homoptera). Die tschecoslowakischen Lecanium-Arten. Prate Moravsk6 Prirodovedeck6 Spolecnosti, 7: 1-134. Waku, Y. and Foldi, I., 1984. The fine structure of insect glands secreting waxy substances. In: R.C. King (Editor), Insect Ultrastructure, Vol. 2. Plenum Publishing Co., pp. 303-322.
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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.
1.1.3
111
Systematics
1 . 1 . 3 . 1 Taxonomic Characters Adult Female CHRIS J. HODGSON
INTRODUCTION Almost invariably, it is the adult female which is used for specific identification of soft scales. Rather few of them can be identified to species with complete confidence based solely on their live appearance, because the latter is considerably affected by environmental factors such as geographic distribution, host plant, part of plant attacked, time of year, etc (e.g., Parthenolecanium corni (Bouchr) (see Ebeling (1938) and Section 1.1.3.5). Nonetheless, some initial indications can be obtained from these data at the genetic level. The shape of the insect and the presence or absence of a test and its composition can be particularly important. Thus, the recording of as much collection data as possible could be very helpful in clarifying the subsequent identification. However, in most instances it will require slide-mounted material to confirm the specific identification and for this it is generally only the youngest adult females that make satisfactory preparations (see Section 1.4.1). In the following discussion, the family and other group names used follow the system used in Section 1.1.3.4. and in Hodgson, 1994a. It should also be noted that the genetic names used below refer primarily to the type species.
EXTERNAL APPEARANCE OF UNMOUNTED INSECTS Test and ovisac Probably all Coccidae secrete some wax, mainly through the dorsal microductules and ventral microducts from internal glands (see Foldi, 1991 and Section 1.1.2.7). This wax forms a thin coveting whose function is probably to reduce water loss. In addition, the derm of most Coccidae has numerous other wax-secreting ducts and pores and these secrete wax which can have a very specific appearance, reflecting both the distribution and the types of ducts and pores beneath. These waxy coverings, referred to as tests, may have a range of different functions. The composition and structure of the tests is an important taxonomic character at the subfamily level. Thus, in some of the more primitive subfamilies, such as the Filippiinae and Eriopeltinae (Fig. 1.1.3.1.1" K,L,M,N), the test is composed of long, f'me, hollow wax filaments, rather similar to those found in the Pseudococcidae (see Cox and Pearce, 1983). These wax filaments are secreted by tubular ducts which are present on both the dorsum and venter. The Filippiinae and Eriopeltinae have woolly or felted tests which usually completely cover the dorsum. These tests may extend posteriorly to form an ovisac for storage and protection of the eggs or l st-instar crawlers and this
Section 1.1.3.1 references, p. 136
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Systematics
Fig. 1.1.3.1.1. Appearance of unmounted adult females of some subfamilies in the Coccidae. Cardiococcinae: A - Mitrococcus celsus Borchscnius, B - Dicyphococcus bigibbus Borchsenius. Ceroplastinae: C - Ceroplastes sinensis Del Guercio. Cissococcinae: D - Cissococcusfulleri Cockerell, where (a) complete galls and (b) section through gall showing adult female within. Coccinae (Coccini): E - Coccus hesperidum Linnaeus. Coccinae (Pulvinariini)" F - Rhizopulvinaria armeniaca Borchscnius, G-Chloropulvinaria floccifera (Westwood). Coccinae (SaissOiini): Saissetia coffeae (Walker). Cyphococcinae: I - Messinea loisa Hodgson (where (a) = dorsal view, (b) = plan view, and t = glassy test, c = area of dorsum covered by glassy test and u = area of dorsum not covered by test). Eulecaniinae: J - Eulecanium tiliae (Linnaeus). Eriopeltinae: K - Eriopeltis rasinae Borchscnius, L - Scythia festucae (Sulc), M - Luzulaspis grandis Borchsenius. F'dipp'finae: N - Lichtensia viburni (Signoret). Myzoleeanllnae: 0 - Toumeyella pinicola Ferris, P - Toumeyella cerifera Fen'is. (A, B from Borchsenius, 1959; D after Brain, 1918; I after Hodgson, 1969; O after Gill, 1988; P after Hamon and Williams, 1984; remainder from Borchscnius, 1957).
Taxonomic characters - adultfemale
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structure is probably secreted by the tubular ducts on the venter. It is likely that the main function of these tests is protection of the insects from predators and parasitoids, while the ovisacs may also reduce desiccation of the eggs and crawlers. In the tribe Pulvinariini (subfamily Coccinae) (Fig. 1.1.3.1.1: F,G), the number of tubular ducts on the dorsum (and therefore the woolly tests secreted by them) have been much reduced or lost, although a few species have retained a small number of tubular ducts which secrete a light woolly covering. However, in this tribe, the ovisac (which is secreted by a range of tubular ducts on the venter) has become much enlarged and can extend to many times the length of the adult female, e.g., in Pulvinarisca serpentina (Balachowsky), where the ovisac may be more the 30 mm long! In order to secrete such a long ovisac, the mature female has to stop feeding, withdraw her mouthparts and then slowly move forwards as the ovisac is secreted. This secretion pushes the posterior end of the scale upwards so that the insect lies almost vertically with its head down, supported by the ovisac. The tests of the Filippiinae, Eriopeltinae and Pulvinariini are white to off-white, although this may be modified by the colour of the underlying insect. The wax coverings in the former two subfamilies tend to be rather loose, but the ovisacs of the Pulvinariini are often dense and somewhat sticky, possibly ensuring that they stick to the substrate below and increasing the protection from egg parasitoids or predators. In almost all Pulvinariini, there are at least three different types of tubular duct on the venter, possibly accounting for the rather complex structure of their ovisacs. Because the ovisacs stick to the host, it is not uncommon to f'md just the ovisacs, the adult females having fallen off, e.g., those of Chloropulvinaria psidii (Maskell). Woolly tests are also found in a few other groups. The Pseudopulvinariinae secrete a very dense and sticky, white, felted covering which can be quite difficult to remove; this is not secreted by tubular ducts but by abundant sclerotised quinquelocular pores found throughout the dorsum. In addition, species of the Brazilian genera Eutaxia and Stictolecanium (Coccinae: Coccini) have a thin woolly covering which is apparently secreted by small cribriform plates (see below). The tests on species of Ceroplastinae are composed of thick and rather watery wax which is probably secreted by the Ceroplastes-type pores present on most of the dorsum. The tests can be quite complex in structure (Fig. 1.1.3.1.1,C ; see Gimpel et al. 1974) and, although usually white, can be quite brightly coloured, particularly with reds and browns, as in Ceroplastes sinensis Del Guercio and Waxiella zonata (Newstead). In Gascardia madagascariensis Targioni Tozzetti, the wax covering is so thick and the insects are often so densely packed that the branch can look like a candle. A thick, waxy test is also produced by Ericerus pela (Chavannes) (Eulecaniinae) but this is secreted by the 2nd-instar males (see Section 1.2.3.2). A glassy wax coveting occurs on members of the Cardiococcinae and Cyphococcinae (Fig. 1.1.3.1.1: A,B,I). In the former subfamily, the glassy test can take the form of two plates which meet along the mid-dorsal line, resembling the two halves of a bivalve shell, as in Cardiococcus umbonatus Cockerell, or like the plates of a tortoise, as in some Ctenochiton spp. The suture lines between these plates appear to be associated with pores around the margin and either along the mid-dorsal line, as in C. umbonatus, or forming a distinct reticulate pattern, as in C. perforatus Maskell. The function of the test appears to be mainly to protect the eggs and lst-instar crawlers for, as oviposition proceeds, the adult female shrivels up at the anterior end, leaving the resultant space for the eggs and crawlers. In the Cyphococcinae (which contains only the African genera Cyphococcus and Messinea), the test appears to cover only the
Section 1.1.3.1 references, p. 136
114
Systematics
median area of the dorsum and looks rather like an Indian tepee. This test appears to be secreted by a range of microtubular ducts bearing a close resemblance to those found in the Eriococcidae and otherwise unknown in the Coccidae. The more lateral areas are presumably covered in the usual thin wax layer. In these two subfamilies, the glassy wax is transparent and the body colours of the insect show through. The only dermal wax cover in the subfamilies Coccinae, Eulecaniinae, Myzolecaniinae and perhaps the gall-forming Cissococcinae (Fig. 1.1.3.1.1: D,E,H,J,O,P) is a thin, transparent coating which covers all the derm, probably secreted by the microductules. Beneath this wax cover, the derm can quickly become so dense after the last moult that no characters can be discerned on a slide-mounted specimen. This sclerotisation occurs rather quickly and one of its main functions may be to protect the eggs and crawlers which are found in a ventral, concave brood chamber. Size, shape and colour Adult female soft scales are generally small insects (3-6 mm long), although a few, such as Paracardiococcus actinodaphnis Takahashi, may be only about 1.5 mm long, whilst the largest species may reach 15-18 mm long, e.g., Megalecanium testudinis Hempel. Most teneral adult females are oval and fiat, although those found on grasses and other monocotyledonous plants tend to be long and narrow. A few species remain almost fiat as they become mature (e.g., Coccus hesperidum Linnaeus) but most swell to some extent and many become highly convex (e.g., Physokerrnes and Eulecanium spp.) and may even become wider than long. Some specimens may be forced to grow asymmetrically due to the structure of the plant surface on which they have settled, but other species, such as Platinglisia noacki Cockerell and Podoparalecanium machili (Takahashi), appear to be naturally asymmetrical. Occasionally the dorsum may be adorned with distinct cavities, as in species of Couturierina and Umwinsia, or with knobs or ridges as in species of Palaeolecanium and Parafairmairia. The stigmatic clefts (Fig. 1.1.3.1.2) may be represented by shallow indentations in the margin where each band of spiracular disc-pores reaches the margin. In some genera, these clefts are entirely absent, as in Hemilecanium and Pseudopulvinaria. In other groups, such as the Paralecaniini and the Myzolecaniinae, the clefts are quite distinct and, in the latter, can extend medially as far as the spiracles. The anal cleft (Fig. 1.1.3.1.2) may be short and unobtrusive in the females of some groups (e.g., the Filippiinae and Eriopeltinae) - indeed may appear to be almost absent in some genera, such as Cryptes and Allopulvinaria (here included in the Eulecaniinae). In other genera, such as Protopulvinaria and Milviscutulus, the cleft is almost half the length of the body. In a few genera and species, the sides of the cleft are probably fused at maturity, as in Megalocryptes and Perilecanium. In the subfamily Ceroplastinae, where the body is covered in a dense waxy test, the anal plates are carried high on the dorsum on a characteristic cone-shaped sclerotisation called the caudal or anal process. This cone-shaped process raises the anal plates above this thick test so that the insects can eliminate their honeydew. The colour of most post-teneral adult female soft scales is various shades of brown, the heavier the degree of sclerotisation, the darker the dorsum. However, young females of some species are quite highly coloured, such as Poaspis jahandiezi (Balachowsky), which is a rich pomegranate red and Vittacoccus longicornis (Green), which is yellow with two broad longitudinal bands of red on the dorsum. For these and other examples of the colourful appearance of young female soft scales, see the colour photographs in Gill, (1988), Hamon and Williams (1984), Kosztarab (1966) and Kosztarab and K o ~ r (1988).
Taxonomic characters - adultfemale
115
THE MOUNTED INSECT: STRUCTURES ON THE DORSUM Derln The derm of teneral females is generally thin and relatively unsclerotised and it is at this stage that they can be most easily mounted and identified. In the Eriopeltinae and Filippiinae, the derm remains relatively thin and becomes only slightly sclerotised, perhaps because it is partially protected by the woolly test. In many other groups, such as the Eulecaniinae and Ceroplastinae, the test quickly becomes sclerotised after the last moult. In a few species which have dense areolations, the derm may be quite thick even just after the final moult but, even so, becomes still thicker with age, so that the dorsal derm may be up to 10 times thicker than the ventral derm, although it may be quite thin at each areolation. For a description of derm development, see Koteja and Lubowiedzka (1976). The size and distribution of the areolations is a useful taxonomic character at the species level. The derm may also have some characteristic markings and sclerotisations. It may be divided into distinct polygonal areas, each of which may be quite large, as in Eucalymnatus, or rather small and densely packed, as in Parasaissetia, where each polygon contains a small areolation with a dorsal microductule. In Mesolecanium, there are radial lines extending medially from the margin which may be less heavily sclerotised. Other areas may also have distinctive sclerotisations. The most frequent is the anal sclerotisation (Qin and Gullan, 1989) which forms a band or crescent around the anterior margin of the anal plates (Fig. 1.1.3.1.2). This is present in the adult females of most subfamilies, but has become greatly enlarged to form the caudal or anal process in the Ceroplastinae. Whilst this crescent is usually uniformly sclerotised (although frequently with areolations), the crescent has a cellular structure in the genera closest to Eulecanium, each cell being elongate and radiating out from the anal plates. In the gall-forming genus Cissococcus, this sclerotised crescent is much enlarged and unique in shape. Another area which sometimes becomes differentially sclerotised is the inner margin of the stigmatic cleft. This is particularly conspicuous in the Paralecaniini and is sometimes referred to as the spiracular sclerotisation (e.g., Qin and Gullan, 1989) (Fig. 1.1.3.1.2) although stigmatic sclerotisation might be a clearer term (see under stigmatic clefts below). In the Cardiococcinae, which mainly secrete a glassy test, the derm frequently becomes sclerotised along the mid-dorsal line and around the margins where the test-secreting pores occur. In the Myzolecaniinae, discrete areas may become sclerotised, such as the quadrate sclerotisations in Houardia and the areas around the cribriform plates in Myzolecanium. The dorsum may also be thrown into lobes, as in the Ceroplastinae and Acantholecanium, or may have shallow cavities as in Umwinsia. In a few genera, such as Cyclolecanium and Lecanochiton, the area of the true dorsum is rather small, the bulk of the dorsal surface being formed from a greatly expanded venter which has become several times the width of the dorsum. This is reasonably clear in these two genera because the band of spiracular disc-pores extends over onto the dorsal surface and then medially to the true margin. This expansion of the venter may have occurred also in Physokermes at the anterior end. However, the most extreme example is Cissococcus, in which the dorsum is restricted to a small area around the anal plates and anal sclerotisation, while the rest of the dorsal surface consists of the expanded venter (Hodgson, 1994a).
Section 1.1.3.1 references, p. 136
Systematics
116
Segmentation This is rarely visible on the dorsum of female Coccidae, but is perhaps most obvious in the two related genera Psilococcus and Paralecanopsis, where the segmentation is clear, at least on the abdomen. It is likely that this is a primitive character.
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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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R2 "~:'"~I;'X
DERMAL SPINULES
Fig. 1.1.3.1.5. Taxonomic characters of adult female soft scales : tubular ducts: side views showing a variety of shapes: T1 = with a deep cup-shaped invagination, thin inner ductule and large terminal gland; T2 = with a shallow cup-shaped invagination and filamentous inner ductule and no terminal gland; T3 = deep cup-shaped invagination, broad inner ductule and large terminal gland; T4 = with broad inner ductule but no terminal gland; T5 = without a cup-shaped invagination and T6 = with a cone-shaped dermal opening; where cdp = cone-shaped dermal pore; ci = cup-shaped invagination; dp = dermal pore; id = inner ductule" od = outer ductule and tg = terminal gland. Microtubular ducts: restricted to the Cyphococcinae; side views showing variation in shapes; where rid = filamentous inner ductule and od = outer ductule. Disc-pores: ventral views: D1 = 5-1ocular disc-pore, typical of spiracular disc-pores and pregeniizl disc-pores in families such as Cardiococcinae; D2-D4 = multilocular disc-pores typical of pregeniizl disc-pores in most families, showing variations in structure as seen under the light microscope; where cp = central pore and 1o = loculi. Preantennal pore: P = side and ventral view. Anal plates: Dorsal views: A1 = anal plates with anterior margin almost at right-angles to body axis and with apical and subapical seize (as in many Ceroplastesspp.); A2 = plates with anterior and posterior margins subequal in length, with inner margin, distal, apical and subapical seize; A3 = pyriform plates with apical and subapical seize; A4 = plates with highly divergent inner margins (as in many Cardiococcinae) and with spinose seize along inner margin, posterior margin and on apex; and A5 = plates with outer margins rounded and numerous seize on dorsal surface (as in many Myzolecaniinae); where ac = anal cleft; am = anterior margin; as = apical seiz; (Is = discal seta; im = inner margin; pm = posterior margin and sas = subapical seize. Ano-genital fold: G1 = dorsal view and G2 = ventral view of typical ano-geniizl fold; where ar = anal ring; am = anterior margin; ares = anterior margin seize; at = anal tube; hs = hypopygial seize; l m = lateral margin; Ires = lateral margin seize and sb = supporting bar. Anal ring: R1 = typical anal ring; R2 = reduced ring as in Physokermes hemicryphus; where ars = anal ring seize and wp = wax-pores. Dermal spinules" surface view.
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Tubular ducts (Figs 1.1.3.1.5) The structure, frequency and distribution of these ducts are of major taxonomic significance at all levels in the taxonomy of the Coccidae. Each duct consists of four parts: (a) an outer ductule, which is thin-walled, barely sclerotised, round in crosssection and generally at least 10#m long; this opens through the dorsum by a small pore which is usually inconspicuous but occasionally can be mildly or even strongly sclerotised (as in Etiennea and Hemilecanium, in which they are cone-shaped). At the inner end of the outer ductule is (b) a characteristic structure, here referred to as the 'cup-shaped invagination' because the outer ductule terminates in a thicker walled structure which is bowl- or cup-shaped. These are generally slightly asymmetrical because from one side of the cup arises (c) the inner ductule, which is usually shorter and narrower than the outer ductule. The inner ductule terminates in (d) a 'flowerbead'-like structure, here called the terminal gland. Tubular ducts vary in the relative lengths and widths of the inner and outer ductules, in the form (particularly the depth) of the of the cup-shaped invagination and in the size of the terminal gland (a range of different ducts is illustrated in Steinweden, 1929). A given species may have a total of 4 or 5 types of tubular duct altogether (i.e. in the dorsum plus venter) and their structure and distribution is remarkably constant within species and is therefore a good diagnostic character. Most species have only one type on the dorsum, but occasionally 2 or 3 may be present, as in Ceronema, Idiosaissetia and Philephedra. Dorsal tubular ducts are most frequent in the Eriopeltinae and Filippiinae and secrete the woolly test. Although generally present throughout the dorsum, they may have a more restricted distribution, as in Conofilippia, Membranaria and Waricoccus, in which they are mainly marginal. In Hadzibejliaspis stipae (Hadzibejli), the inner surface of the outer ductules is characteristically ridged. Dorsal tubercles (Figs 1.1.3.1.4) These structures have usually been referred to as sub-marginal tubercles by earlier authors but, as they can occur throughout the dorsum (as in Lagosinia, Philephedra and Pseudophilippia), Hodgson (1994a) considered the term dorsal tubercle more appropriate. Dorsal tubercles are variable in structure but appear to be divisible into two main groups: (a) normal convex tubercles and (b) inverted tubercles. Most dorsal tubercles of the normal, non-inverted type are strongly convex, rather sclerotised and have a central inner duct. This inner duct resembles a tubular duct, but it lacks the cupshaped invagination, which has been replaced by a small swelling on one side at its inner end from which a short filament or inner ductule arises; no structure similar to the terminal gland of a tubular duct is present but very occasionally there may be a minute swelling. In Ceronema banksiae Maskell, there are a number of submarginal structures apparently intermediate between dorsal tubercles and tubular ducts; these may be similar to the submarginal chambered ducts described by Qin and Gullan (1992) in Pulvinaria dodonaeae Maskell. Dorsal tubercles may be roundly convex, as in Coccus and Saissetia, or they may have a central concavity with the inner duct originating from its base and extending above the outer tubercle. These tubercles can become highly complex, with satellite tubular ducts arising from the walls of the tubercle or from the base of the central duct. Inverted tubercles are concave, many of them looking rather like convex tubercles which have been turned 'inside-out', as in Alichtensia and Lagosinia. In the most extreme examples, such as in Perilecanium, the inner duct appears to open at the base of the cavity. Dorsal tubercles vary greatly in size, those in Coccus being small, about 5#m in diameter, but they can be up to at least 25#m in diameter, as in Alichtensia; in addition,
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Systematics
they are usually wider than they are tall but, in Alecanochiton, they are at least three times taller than wide.
Pocket-like sclerotisations (Figs 1.1.3.1.4) These have been observed so far only in some genera in the Saissetiini and Filippiinae and in Perilecanium, but they may be more widespread. As their name suggests, these are sclerotisations which have a pocket-like invagination. They are usually quite heavily sclerotised, 5-20#m wide, and take up stain well except in the youngest adults in which no dermal sclerotisation has yet occurred. When present, they are almost invariably found associated with the submarginal band of dorsal tubercles, either appearing to replace them or lying between them within the band; occasionally they occur between a tubercle and the margin or close to a tubercle. Only very rarely have pocket-like sclerotisations been noted in the absence of dorsal tubercles, e.g, in the highly variable Parthenolecanium corni (Bouch6). Pocket-like sclerotisations tend to be most frequent at the anterior and posterior ends. Their function is unknown, but Boratyfiski (1970) considered that these sclerotisations represented the scar-like rudiments of the dorsal tubercles (bicylindrical pores of Boratyfiski, 1970) of the previous instar. This is highly probable but needs to be checked. Anal plates (Figs 1.1.3.1.5) These are two approximately triangular plates which lie at the anterior end of the anal cleft, coveting the anal ring. Earlier authors have sometimes referred to them as anal opercula. Anal plates are a major characteristic of the Coccidae, only being absent in adult Physokermes; they are otherwise known only in the Eriochitonini (Eriococcidae) (Hodgson, 1994b). Prior to the ejection of honeydew, the plates open anterolaterally, apparently being hinged along their anterior margins. In most Coccidae, these two plates lie with their inner margins more or less parallel, so that together they are approximately quadrate. In some genera, however, the inner margins diverge posteriorly and then they invariably have a least one (and sometimes several) spinose seta along the inner margin (e.g., in typical Cardiococcinae and Filippia). The shape of the plates is a helpful diagnostic character. The anterior and posterior margins (sometimes referred to as the anterolateral or cephalolateral and posterolateral or caudolateral margins by other authors) can be of very unequal length; thus in Kilifia, Milviscutulus and Udinia, the posterior margin is much shorter than the anterior margin and the plates are then referred to as pyriform (pear-shaped). In the Ceroplastinae, the anterior margin is almost at right-angles to the long axis of the body and much shorter than the convex posterior margin. In Pseudopulvinaria, the two anal plates are joined at the anterior and posterior ends, with the anal ring lying in the middle; the two plates then appear to stand uptight rather like a crown. In Austrolichtensia, there is an additional square or rectangular plate immediately posterior to the anal ring with a group of setae which are possibly hypopygial setae (see under ano-genital fold below). Females of several genera posses a small plate or sclerotisation between the anal plates at their anterior end; this is almost certainly part of the crescentic anal sclerotisation (see above) and may be homologous to similar structures in the Eriochitonini (Eriococcidae), Lecanodiaspididae and Cerococcidae (Hodgson, 1995a). Various setae are found on the anal plates, the number and position of which are of taxonomic importance (see Fig. 1.1.3.1.5). The setae along the inner margin are referred to as the inner margin setae. In the more primitive genera (e.g., Eriopeltis and Filippia), there are two setae on each inner margin. These setae are usually setose, but when the inner margins are divergent, they are usually spinose (although they appear to be fleshy in Eutaxia). In addition, the number of setae can be far greater - up to 19 on each margin in Vitrococcus conchiformis (Newstead). In slide preparations in which the anal plates are slightly open, care is required in identifying the inner margin setae as they can appear to be located more dorsally, away from the margin. Apical and/or
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subapical setae are invariably present, and there may also be setae along the posterior margin, which are sometimes referred to as subdiscal setae. There may also be others on the dorsal surface and, in most species of the Myzolecaniinae, these setae are particularly abundant. In a few genera, such as Alecanochiton, Saissetia and Udinia, there is a single seta on the posterior half of each plate which is distinctly enlarged and is referred to as the discal seta, situated in the discal position. The possible evolution of the anal plates in the Coccidae was discussed by Hodgson (1995a), who showed that they had almost certainly evolved from anal lobes which had migrated anteriorly. Hodgson considered that the anal plates of the Eriochitonini (Eriococcidae) probably evolved in a similar manner as also did the single median dorsal plate of the Aclerdidae. However, Hodgson (1995a) considered that the sclerotised 'anal' plates in the Le~anodiaspididae and Cerococcidae were not derived in the same way. Ano-genital fold (Figs 1.1.3.1.5) This fold, which lies at the anterior end of the anal cleft, separates the anus on the dorsum from the vulva on the venter, and is at right-angles to the long axis of the body. There is usually at least a single seta at each comer of the fold and sometimes there is a line of setae; these setae were referred to as anterior margin setae by Hodgson (1994a) but have been referred to as fringe setae by many other authors. In addition, there is often a group of setae just anterior to the ano-genital fold on the ventral surface which are called hypopygial setae. Most anal plates have thicker areas of sclerotisation along their inner margins and these form the lateral margins of the anal cleft at the anterior end, these sclerotised bars appear to extend anteriorly into the insect's body and it is likely that they are apodemes for the attachment of the muscles for movement of the anal plates. These sclerotisations have been referred to as ventral thickenings (Thro, 1903; Williams and Kosztarab, 1972) and supporting bars (Hodgson, 1994a). The lateral margins of the anal fold also generally have a few setae, particularly along the outer margins of the supporting bars; these often appear to be ventral. They have been referred to as subapical setae by several authors but, because they can form a line along the entire margin of the supporting bars, Hodgson (1994a) considered this term inappropriate and called them lateral margin setae, he restricted the term subapical setae to those near the posterior apex of the anal plates, generally on the dorsal surface. Anal ring (Fig. 1.1.3.1.5) This is the sclerotised ring, composed of two lateral crescents, which surrounds the anal opening. Almost invariably it has one or more rows of wax-secreting pores and generally 3-4 pairs of long setae, called anal ring setae, although the number of setae is variable and there are 16 pairs in Halococcus formicarii Takahashi. In a few genera, such as Physokermes and Rhodococcus, the anal ring is highly modified and lacks both setae and wax pores, although some Rhodococcus spp. have small setae and the anal ring of some Physokermes spp. can have short, spine-like projections. In Austrolichtensia, there are no wax pores and the setae occur in a group along the posterior margin of the anal ring. The anal ring is usually situated at the inner end of a fairly long anal tube, but rarely this tube is very short, as in Pseudopulvinaria. The design of the anal plates, anal ring and anal tube appears to have been to facilitate the expulsion of honeydew droplets, as described by Williams and Williams (1980) (see also Sections 1.1.2.6 and 1.2.2.1. The anal tube is usually retracted but is everted between the anal plates when eliminating the honeydew. Some Coccidae which have short anal tubes, such as many members of the Myzolecaniinae, live within stem cavities of plants and rely on ants for
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Systematics the removal of their honeydew and in these species the reduction in the length of the anal tube is probably secondary.
STRUCTURES ASSOCIATED WITH THE MARGIN
Margin The margin of most Coccidae is quite distinct and is marked by the presence of marginal setae. In a very few genera, this demarcation between the dorsum and venter has been lost by extensive swelling of the venter (as in Cissococcus) or at least obscured (as in Cyclolecanium and Lecanochiton). In most genera, the margin itself is relatively characterless but in a few it is folded in a highly characteristic manner, as in Alecanium and Xenolecanium, in which it is described as crenulate. Stigmatic clefts (Fig 1.1.3.1.2) These may be present or absent. When present, they may be represented by very shallow indentations but they can be quite deep and distinct, as in the Paralecaniini, where the base of each cleft is sclerotised on the dorsum; this may even be ornamented, as in Anthococcus. In a few genera, the clefts can be exceptionally deep, extending medially almost to the spiracles, as in Cryptostigma, Houardia and Myzolecanium. It is here suggested that there should be a clear distinction between the terms used for structures associated with the spiracle and those with the margin and it is recommended that the term stigmatic should be used for those associated with the margin. Thus, the sclerotisation at the base of the stigmatic cleft is here referred to as the stigmatic sclerotisation rather than the spiracular sclerotisation (Qin and Gullan, 1989), clearly separating it from any of the sclerotisations associated with the spiracles themselves. The term stigmatic spines also seems preferable to spiracular spines, which has occasionally been used by some authors. In species in which stigmatic clefts are absent, it is sometimes necessary to refer to this point on the margin (when discussing stigmatic spines for instance) and Hodgson (1994a) suggested the term stigmatic area for this point on the margin. Marginal setae (Figs 1.1.3.1.3) These typically occur in a line along the margin or, less frequently, as a band several setae wide. They are usually distinctly differentiated from other setae and are frequently abundant (although entirely absent in Cissococcus). They may be flagellate (finely setose), spinose, flattened apically (spatulate), or may have a divided (fimbriate) or swollen (clavate) apex; they may be long and thin or short and stout; broad at the base or constricted basally; straight or sharply bent; and, although they generally arise at fight angles to the margin, in a few genera they lean posteriorly, as in Mametia. Most marginal setae are hollow but lack a pore at their apex; in a few genera, such as Megapulvinaria and Pulvinarisca, there is a distinct opening at the apex through which wax is probably secreted. Generally, marginal setae are present around the entire margin but in Scythia and ldiosaissetia they are concentrated at each end of the body. In many genera, one or more of the marginal setae on the anal lobes tend to be considerably longer than the others and these are called anal lobe setae. In addition, more than one type of marginal seta may be present, as in Alecanium and Eulecanium and, even more particularly, in Inglisia in which spinose and clavate setae frequently alternate. In most genera, marginal setae are absent from the margins of the anal cleft but occasionally they extend along the entire cleft, as in Bodenheimera, or part of the cleft (as in Lagosinia and Petutularia). Occasionally the setae along the anal cleft margin are differentiated from the marginal setae, as in Filippia and Scythia. The number and shape of the marginal setae are highly significant taxonomic characters; their
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frequency is generally given as the number of setae between the stigmatic clefts on one side or, less frequently, between the anterior clefts. In some descriptions by earlier authors, the distance between setae was used as a diagnostic character but, as this distance increases with the expansion of the adult female, it is unreliable. Each seta articulates with a basal socket. This is usually well developed but occasionally may be narrow and ill-defined, as in Bodenheimera. In a few species, the shape is distinctive (as in Pseudopulvinaria and Udinia). The function of marginal setae is unclear but Hodgson (1994a) suggested that the basal sockets may secrete wax rods around each seta, as suggested for the Pseudococcidae by Cox and Pearce (1983). The basal sockets of the larger marginal spines in Pulvinarisca have pore-like openings.
Stigmatic spines (Figs 1.1.3.1.3) In most genera, a few marginal setae are differentiated from the other setae in each stigmatic area (see under stigmatic clefts above). When differentiated from marginal setae, they are invariably more spinose and are referred to as stigmatic spines (even though they are strictly setae because they have basal sockets). Typically there are three stigmatic spines, set slightly onto the dorsum, the median spine usually slightly longer than the two lateral spines. However, the marginal setae in the stigmatic areas may be undifferentiated, as in Hemilecanium, or there may be only a single spine barely different from the marginal setae, as in Stotzia. At the other extreme, the stigmatic spines can occur in large groups in each stigmatic area, as in Ericeroides, Richardiella and the Ceroplastinae; in the latter subfamily, the group of spines may extend onto the dorsum, as in Gascardia. Whilst most genera have only a single type of stigmatic spine, Waxiella has two, those along the margin being spinose and clearly differentiated from those on the dorsum, which are conical; while, in some specimens of Alecanochiton marquesi Hempel, one of the two lateral spines may be fimbriate and the other spinose. When stigmatic clefts are present, stigmatic spines may be absent or present, either along the margins (as in Neoplatylecanium and Paracardiococcus) or at the base as in the Paralecaniini. In the absence of a stigmatic cleft, the stigmatic spines can be set well up onto the dorsum, as in Akermes and Pendularia. The number, shape and relative lengths of the stigmatic spines are important taxonomic characters. As with the marginal setae, the basal sockets of stigmatic spines are usually well developed. Frequently those for the marginal setae and stigmatic spines are similar, but occasionally they differ, as in the Coccinae, where the basal sockets of the lateral spines may be much narrower than those of the median spine. The taxonomic significance of these differences is unknown. Eyespots (Fig. 1.1.3.1.2) In the Coccidae, the two eyespots are usually present just dorsad to the margin, each consisting of a single lens. They can be hard to distinguish, but are perhaps most easily detected when viewed using phase-contrast illumination. In genera in which they are more or less marginal, they can be located at about 45 o anterolaterally from the bases of the antennae. In most genera they are close to or even amongst the marginal setae, but in a few genera, notably those in the Paralecaniini, they are displaced some distance onto the dorsum, even lying dorsad to the base of each antenna in some genera. Eyespots are thought to be typically absent in the Cissococcinae and Myzolecaniinae and possibly also in the Cyphococcinae.
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Systematics
STRUCTURES ON THE VENTER Derln
Unlike that of the dorsum, the derm of the venter is thin and membranous in most genera, although it may occasionally show some signs of sclerotisation in old individuals (e.g., in Neoplatylecanium and Paractenochiton). Distinct features which are usually visible are (i) grooves which run from the margin to each peritreme, sometimes called stigmatic grooves or stigmatic furrows, in which most of the spiracular disc-pores lie, and (ii) shallow grooves from the base of each antenna to the point on the margin where the eyespots are located.
Dermal spinules (Fig. 1.1.3.1.5) These are minute tooth- or spine-like projections from the derm. They are probably present in all Coccidae and may occur almost anywhere on the venter although they are possibly absent from the dorsum, at least in the adult female; they appear to be most abundant medially and perhaps around the anal cleft and genital opening. They have been little studied, probably because of their minute size, but their distribution might be of some importance at the specific level, as was found for the Odonaspidini (Diaspididae) (Ben-Dov, 1988).
Segmentation (Fig. 1.1.3.1.2) This is usually distinct medially on the abdomen where there are six visible segments between the vulva and the metathoracic coxa. These are currently numbered using the system of previous authors in other families, e.g., Miller (1984) with the Eriococcidae; Beardsley (1984) and Williams (1985) with the Pseudococcidae. These workers considered that the 1st abdominal segment is represented by an area laterad to the metathoracic legs so that the first visible segment ventrally is the 2nd. Using this system, the pregenital segment in female Coccidae is the 7th. The segmentation on the thorax is usually discernable, as is that between the thorax and head, where the intersegmental line runs from near each procoxa posteriorly to the labium. No segmentation is visible on the head. In many genera, the mediolateral part of each abdominal segment is modified into a pair of small lobes, often dividing the segmental bands of pregenital disc-pores into median and lateral groups; these lobes were referred to as the mediolateral abdominal folds by Hodgson (1994a). In the Ceroplastinae, these lobes become conspicuously enlarged in the posterior segments. The position of the vulva is usually uncertain in this subfamily but is unlikely to lie beneath the anus in the caudal process, because it is hard to see how the eggs could then reach the space beneath the concave venter. It probably lies at the very posterior end of the venter, covered by the mediolateral lobes which are here enlarged and extend medially, meeting under the last few pregenital segments. These lobes are sometimes present in other species (e.g., in Lecanochiton minor Maskell) but rarely as conspicuously as in the Ceroplastinae. Ventral pores Three. types of pore are frequent on the venter: disc-pores, microducts and preantennal pores. (i) Disc-pores. Each disc-pore has a central loculus which is usually round but may be oval, surrounded by a number of identical loculi or pores, the complete disc-pore looking rather like a wheel with spokes. Each disc-pore usually has 5 to 12 or more loculi in the outer ring and these pores are, therefore, known as multilocular disc-pores. Only very occasionally does this pore structure vary, as in Akermes bruneri Cockerell in which the distribution of the loculi is more or less random. Multilocular disc-pores can be divided into two groups: (a) pregenital disc-pores and (b) spiracular disc-pores.
Taxonomic characters - adultfemale
129
(a) Pregenital disc-pores (Figs 1.1.3.1.2,5). Pregenital disc-pores are usually 5-8gm in diameter and are primarily located on the immediate pregenital segments, hence the name. However, in many genera, they are also found across the more anterior abdominal segments and, less frequently, medially on the thorax and head. They are, however, entirely absent in some genera, such as Saccharolecanium and Xenolecanium. The number of loculi in each pore and the distribution of these pores on the venter are important taxonomic characters. Thus, in the Paralecaniini, pregenital disc-pores are almost entirely restricted to the pregenital segment, whilst in the Eulecaniinae they are typically abundant across all the abdominal and thoracic segments and also frequently occur near the bases of the antennae. In addition, they may be found laterad to the coxae, most frequently the metacoxae. They may also extend laterally around the genital opening and along the margins of the anal cleft. An extreme example of the latter distribution is Lecaniococcus ditispinosus Danzig, which has a large group of disc-pores replacing the submarginal tubular ducts on the anal lobes. In Stenolecanium esaldi Takahashi and Melanesicoccus myrmecariae Williams and Watson, they occur submarginally throughout the venter. In some taxa, the pregenital disc-pores are restricted to a few on either side of the genital opening or near the margins of the anal cleft and then each pore tends to have five loculi (as in many Cardiococcinae). Other groups, such as some Pulvinariini, tend to have seven or eight loculi in each pore, whilst the most frequent number of loculi per disc-pore is 10. The number of loculi per pore tends to be highly specific and, as stated above, is an important taxonomic character at all levels. In electron-microscopy studies, the three-dimensional structure of these pores has been shown to be very varied between genera and species and their microscopic structure may be taxonomically important (Foldi, 1991; Takagi, 1990, 1992; Qin and Gullan, 1992). Disc-pores have been shown to secrete short, curved wax filaments which are thought to prevent the eggs from sticking together (Hamon et al., 1975). They are, therefore, least frequent in viviparous species, particularly in the Coccinae (D.J. Williams, personal communication). In a few species there may be two distinctly different types of pregenital disc-pore, as in Perilecanium where the disc-pores in the three pregenital segments each has 10 loculi, but in which there is also small groups of 5-1ocular disc-pores on either side of the mouthparts. (b) Spiracular disc-pores (Figs 1.1.3.1.5). This term is restricted to the band of discpores which lie in the stigmatic furrow between the stigmatic area on the margin and the spiracles. These disc-pores secrete short, curved, wax filaments, which are thought to assist in the ventilation of the stigmatic furrows (Tamaki et al., 1969) and this wax is frequently conspicuous even in the thick wax covering the Ceroplastinae, as it has a different composition and can appear white against the darker body wax. As with pregenital disc-pores, the distribution and frequency of spiracular disc-pores and the number of loculi in each pore are important taxonomic characters. In most genera, each pore has five loculi and most authors refer to them as quinquelocular pores. However, in a few genera, these pores have more than five loculi (e.g., Allopulvinaria, Gascardia and Paralecanopsis) and so the term spiracular disc-pores seems more appropriate; indeed in Paralecanopsis turcica Bodenheimer, each pregenital disc-pore has mainly seven loculi, whilst each spiracular disc-pore has mainly 10 loculi, even though the diameter of the latter pores is (as usual) smaller than that of the pregenital disc-pores. In a few genera, the pore bands widen at the margin and the number of loculi in each pore increases, as in Didesmococcus and Paracardiococcus. In Psilococcus, the disc-pores form a broad marginal band but remain mainly 5-1ocular. In Pseudopulvinaria there is also a band of marginal 5-1ocular pores, but these appear to
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Systematics
be dorsal disc-pores which have extended onto the venter. Most spiracular disc-pores are about 4-6/xm wide, but they range in size from 2.5#m in Platylecanium to over 8#m in Pseudopulvinaria. In some genera, the band of spiracular disc-pores is incomplete, with groups either near the margin or near the peritreme or both (e.g., in Schizochlamidia); in Cyclolecanium, the anterior band is restricted to a group around the spiracle although the posterior band is complete; in Inglisia, Lecanochiton, Messinea conica De Lotto and Physokermes hemicryphus (Dalman), the anterior band is complete and it is the posterior band that is represented by a few disc-pores near each peritreme. In most Coccidae, the opening of the peritreme faces more laterally than ventrally, producing a cavity in the venter just laterad to each peritreme, the peritreme cavity (Fig. 1.1.3.1.6). Frequently there is a concentration of spiracular disc-pores in this cavity, as in Hadzibejliaspis, Platinglisia and Scythia. In Allopulvinaria, the cavity has become a highly specialised structure and contains five or more bands of 12-1ocular disc-pores. In some Myzolecaniinae, the structure of the spiracular groove and peritreme cavity has been much modified and all the spiracular disc-pores are located within an invaginated tube (see under spiracle below). Each band of spiracular disc-pores may be one pore wide, as in Maacoccus, Stictolecanium and Tillancoccus, or very broad, as in the Ceroplastinae and Myzolecaniinae. In many genera, the pore bands also extend medially past the spiracle for a short distance, but in Suareziella and Trijuba the extension from the posterior band is much longer, ending mesad to the mesocoxae. Generally the number of disc-pores on each side of the insect is approximately similar, but in a few species and genera in which the adult female is asymmetrical, the spiracles may be nearer the margin on one side and in these the number of spiracular disc-pores is usually fewer on the narrower side (e.g., as in Podoparalecanium). (ii) Ventral microducts (Figs 1.1.3.1.3). Like dorsal microductules, the oval, sclerotised pore of each ventral microduct is found at the base of a short, outer duct. However, in these microducts the pore opening is across the widest part of the pore and the nonstaining inner ductule is not filamentous, but is usually broad and skirt-like. Occasionally this inner ductule has a different and distinctive structure, as in Cryptes and Myzolecanium. Ventral microducts are probably present in all Coccidae (with the possible exception of Paralecanium and Podoparalecanium), and were considered by Hodgson (1994a) to be an distinctive character of this family. Each pore is usually about 2-3#m wide, but they are minute (or even perhaps absent) in some Paralecaniini. Generally they are present more or less throughout the venter, although usually most frequent submarginally. However, occasionally they have a distinctive distribution, as in Antandroya, in which they are restricted to a group between the antennae, and in Eulecanium tiliae (Linnaeus) in which they form a distinct band just mesad to the submarginal band of ventral tubular ducts. In the Ceroplastinae and Cardiococcinae, the microducts nearest the margins sometimes appear to be slightly larger. In the Ceroplastinae and Messinea the pore opening appears to be cruciform. The function of the wax secreted by the ventral microducts is unknown but, in addition to reducing water loss, it may stick the insect to the substrate. (iii) Pre-antennal pores (Figs 1.1.3.1.4). These are small convex pores which are present just anterior to each scape. In most genera, there is only a single pair, but in some they are more abundant, with up to six pairs in Poaspis jahatutiezi (Balachowsky). Their taxonomic significance is unknown, although those in the Eriococcidae appear to be funnel-shaped while those in the Coccidae are convex and so their shape may be of some significance.
Taxonomic characters - adultfemale
131
(iv) Other ventral pores. Other types of pore on the venter are infrequent and may, therefore, be useful taxonomic characters. Simple pores, similar to those on the dorsum, are occasionally present; they are most frequently associated with the margin (as in Poaspis and Umwinsia) but may be found throughout (as in Allopulvinaria). In other genera, oval to round fiat pores with a granular surface may be associated with the pregenital disc-pores, as in Alecanopsis and Trijuba, or with the spiracular disc-pores, as in Didesmococcus. In Anthococcus, these pores are round and convex, subequal in size to the pregenital disc-pores, while in Halococcusformicarii Takahashi they are oval and fiat and are found widely in the mediolateral areas of all or many segments. Ventral tubular ducts (Figs 1.1.3.1.5) The structure of the ventral tubular ducts is similar to that of the ducts on the dorsum and, like them, their structure and distribution are important taxonomic characters. In those genera which have only one type of dorsal and one type of ventral tubular duct, their structure is usually identical. The most frequent distributions of the ventral tubular ducts are as follows: (a) present more or less throughout the venter, as in many Eriopeltinae, Filippiinae and some Pulvinariini; (b) restricted to a more or less complete submarginal band, as in most Eulecaniinae, Cardiococcinae and Pulvinariini, or (c) present in a group on either side of the genital opening, as in most Paralecaniini and Myzolecaniinae. Most Myzolecaniinae have only a single type of ventral duct, whilst the Pulvinariini usually have three or four. The separation of the genera included by Hodgson (1994a) in the Pulvinariini from those in the Eriopeltinae and Filippiinae is difficult, but is based primarily on the structure and distribution of the tubular ducts. In the Eriopeltinae and Filippiinae, dorsal ducts are always present and, even in those which have two to four types of ventral duct, the tubular ducts in both the ventral submarginal ring and on the dorsum are quite large and usually have well-developed inner ductules and terminal glands; in the Pulvinariini, on the other hand, dorsal tubular ducts are frequently absent but, when present, both the dorsal ducts and those forming the ventral submarginal band are usually small, with filamentous inner ductules and no terminal gland. In addition, the Pulvinariini typically have a large type of duct in which the inner and outer ductules are both broad and subequal in width; these are most common medially on the thorax but alternatively may be present in the submarginal ring amongst the smaller ducts. This type of duct is absent or has a different distribution in the Eriopeltinae and Filippiinae. A few other genera and species have tubular ducts with very broad inner ductules (e.g., Acantholecanium, Cajalecanium, Eutaxia, Stictolecanium, Saissetia coffeae (Walker) and some Ceroplastinae). Ventral setae (Figs 1.1.3.1.3) Most ventral setae are short and flagellate, but a few are longer and these can be of some taxonomic significance. The most frequent distribution of the longer setae is a pair medially on the pregenital segment and usually pairs medially on the preceding two segments, referred to as the pregenital setae. In addition, there are usually two or three pairs of long setae just mesad to each coxa and one to three pairs of long setae between the antennae, these latter being called the inter-antennal setae. In a few genera, such as Poaspis, long ventral setae may be much more abundant, with up to 70 present between the antennae and one or more pairs on each abdominal and thoracic segment. Ventral setae can be helpful in separating species within a genus. For instance, Pulvinaria regalis Canard has long setae on all abdominal segments, while the rather similar P. vitis (Linnaeus) has only the usual three pairs of pregenital setae. In most species of the Cardiococcinae and Myzolecaniinae, the pairs of long setae on the pregenital segments have been replaced by groups or segmental rows of short, generally rather spinose, setae
Section 1.1.3.1 references, p. 136
132
Systematics and in these subfamilies the inter-antennal setae are generally also fewer and shorter than in the other subfamilies. Most of the other ventral setae appear to be randomly distributed, with the exception of the submarginal setae which usually form a single row just mesad to the margin. However, in a few genera, the ventral submarginal setae are almost as long as the marginal setae (e.g., in Leptopulvinaria, Sphaerolecanium and Vittacoccus), whilst in some Myzolecaniinae they are undifferentiated from the marginal setae and form a broad band of peg-like setae (e.g., in Cryptostigma and Cyclolecanium). The number of the submarginal setae may be a useful taxonomic character at the species level. A few genera have long ventral setae elsewhere, as in Couturierina, which has groups of long setae submarginally, and in Cissococcus which has long setae throughout much of the venter. Spiracles (Figs 1.1.3.1.6) There is considerable variation in the structure of the spiracle within the family and this probably justifies more attention (see Hodgson (1995b) who described some of this variation). Each spiracle is composed of a sclerotised, funnel-shaped outer peritreme, which opens through the spiracular opening or atrium into the tracheae. The size of this opening is controlled by an immovable dorsal valve and a movable ventral valve. The size of each peritreme may be important at the subfamily level; most are 40-80#m wide but in the Myzolecaniinae each peritreme is usually much wider than the length of a coxa, i.e. 100#m or more wide. Laterad to each peritreme is a cavity, the peritreme cavity, formed by the lips of the stigmatic furrow extending around the peritreme. These cavities are usually membranous and indistinct but frequently there is a concentration of spiracular disc-pores in this area and in some genera the cavities are heavily sclerotised. In a few genera, the bands of spiracular disc-pores appear to extend into the peritreme (e.g., in Platinglisia and Pseudopulvinaria) but this is due to the sunken nature of the peritreme; disc-pores are possibly always absent from the peritreme itself. In a few genera, the stigmatic furrow appears to be absent and in these species, the aperture between the peritreme cavity and the exterior may be quite small, with many of the spiracular disc-pores lying within the cavity (Fig. 1.1.3.1.6 Sz, S3). In most Coccidae, a few spiracular disc-pores are present on the venter just mesad to the spiracles, but in most genera in the Myzolecaniinae, these disc-pores, which are frequently abundant, are in an internal, finger-like invagination which extends medially between the venter and the spiracle. In addition, the ventral lips of the stigmatic furrow have become fused in some genera, so that the spiracles are at the end of an internal tube lined with spiracular disc-pores, as in Cribrolecanium and Halococcus. In genera such as Houardia, this tube opens at the margin, but in Cribrolecanium and Halococcus, the opening is situated well onto the dorsal surface. The most extreme modification is possibly found in Cryptostigma inquilina (Newstead), in which the spiracle has become completely inverted and opens through the dorsal surface at a point well in from the margin (Hodgson, 1995b). In some other subfamilies, particularly the Cardiococcinae, there are dense areas of sclerotisation around each spiracle and this condition is particularly pronounced in genera like Neolecanochiton and Pseudokermes, although in other genera and species (e.g., Chloropulvinaria psidii (Maskell)) it may take the form of a lightly sclerotised bar around the anterior part of the spiracle. This sclerotisation was called the sclerotic plate by Hamon and Williams (1984) and the sclerotised spiracular plate by Hodgson (1994a). Legs (Figs 1.1.3.1.6) When present, the legs are normal insect legs, each with five segments, although they are generally slightly small in proportion to the size of the body. In most species, the anterior legs are slightly smaller than the other two pairs but this difference is greatly accentuated in a few genera (e. g., in Kilifia). The coxae are attached to the venter along their width and, in particular, articulate with a sclerotisation at their lateral comer; this
Taxonomic characters - adult female
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Fig. 1.1.3.1.6. Taxonomic characters of adult female soft scales: legs: L1 = posterior view of metathoracic leg, showing separate tibia and tarsus but no tibio-tarsal articulation ofarticulatory sclerosis, and with one claw digitule narrower than the other and a denticle on the claw (setae on anterior surface shown dashed); 1,2 = posterior view of well-developed metathoracic leg, with a tibio-tarsal articulation and articulatory sclerosis, and with claw digitules similar (setae on anterior surface shown dashed); L3 = reduced leg but still showing all the segments; claw digitules dissimilar; IA = leg reduced to a single segment and claw. Where: as = articulatory sclerosis; c = coxa; cd = claw denticle, cl = claw; cld = claw digitules; cp = coxal process; f = femur; ta = tarsus; tad = tarsal digitules; ti = tibia; tr = trochanter. Spiracles: ventral views of left hand spiracles, where SI = normal spiracle with large peritreme; $2 = spiracle with a group of spiracular disc-pores in a distinct peritreme cavity (as in Paralecanopsis turcica)" $3 = typical spiracle with heavily sclerotised spiracular plate, and $4 = spiracle with a spiracular tube (as in Halococcus formicariO. Where: a = atrium; p = peritreme; pc = peritreme cavity; sdp = spiracular disc-pores; ssp = sclerotised spiracular plate; st = spiracular tube; t r = trachea. Mouthparts" ventral views: M1 = typical mouthpart and M2 mouthparts of Saccharolecanium krugeri showing enlargement of the clypeolabral shield. Where: cl = clypeolabral shield; la = labium and st = stylets. Antennae: A1 = ventral view of typical leR antenna; A2 = dorsal view of apical three segments; A3 = ventral view of let~ antennae, showing reduced segmentation (as in Paralecanopsis turcica); A4 = dorsal view of the same; A5 = antenna reduced to two segments (as in Paractenochiton sutepensis) and showing increased numbers of fleshy setae, and A6 = reduced antenna showing annular segmentation. Where as = apical segment; bs = basiconic sensilla; cp = campaniform pore; fs = fleshy setae; is = intersegmental sensilla; pd = pedicel and sc = scape.
Systematics
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is often most obvious in legs which are much reduced (e.g., as in Alecanium hirsutum Morrison and Pseudokermes nitens (Cockerell)). From this sclerotisation arise internal sclerotised processes or plates which could be referred to as coxal processes, as suggested for the Pseudococcidae by Williams and Granara de Willink (1992, p. 167). These vary considerably in size and may be of taxonomic significance; for instance, they are particularly broad in Paralecanopsis and Phyllostroma and rather long in
Cissococcus. The structure of the coxae is very similar throughout the Coccidae, but in Kilifia the coxae of the middle and hind legs are much enlarged. Neither is there much variation in the structure of the trochanter and femur. Each trochanter has a pair of campaniform sensilla on each side (whose function is unknown) and one or two long setae on its ventral surface; the taxonomic significance of this difference is also unknown. In addition, the relative widths of the femora are usually similar between legs within an individual, but occasionally that of the front leg may be broader, as in Mesembryna fasciata De Lotto. In Allopulvinaria, some of the setae on the coxa are distinctly spinose, while the trochanter and femur appear to be fused in some specimens of Neoplatylecanium cinnamomi Takahashi. The tibia is always longer than the single tarsus and the proportions of all three pairs of legs are usually similar, although in Etiennea cacao Hodgson the tibia and tarsus of the front legs are significantly thinner than those of the hind legs. The tibia lacks the campaniform sensilla typically present in many other families (Koteja, 1974a); the absence of this sensilla is a major taxonomic character of the Coccidae (otherwise only known in the Aclerdidae (Section 1.1.3.4), Conchaspididae, the genus Callococcus (Asterolecaniidae?) and Steingelia gorodetskia Nassanov (Margarodidae) (Koteja, 1974a)) although two species of soft scales are now known from New Zealand which do possess these campaniform pores (C.J. Hodgson and R. Henderson, unpublished data). There is usually an articulatory sclerosis between each tibia and tarsus; the presence or absence of this sclerosis is also of taxonomic importance. It is absent in the Eulecaniinae, even though their legs are otherwise well developed. In Kilifia, the ventral side of the tibia of each meso- and metathoracic leg forms a spur which extends down the side of the tarsus. In a few genera, the tarsus can appear to be 2-segmented, particularly in the front leg, as in Exaeretopus and Hadzibejliaspis, due to the presence of a thickening in the derm of the dorsal surface and, as this is often associated with a bend in the tarsus, the latter can look as though it has an articulation. The frequency, distribution and length of the setae on the tibia and tarsus may also be of some taxonomic significance - Koteja (1979) used this character for separating some species of Poaspis. At the distal end of the tarsus is a pair of thin digitules, the tarsal digitules; these do not vary much in adult females in either size or structure other than in proportion to the length of the claw or claw digitules. The claw and claw digitules show several features of taxonomic importance. The claw may be short and broad or long and thin, and may or may not have a small denticle near the apex (this is particularly pronounced in some Ceroplastodes spp.). In a few genera and species, the claw has a denticle on its widest part, as in Megapulvinaria, Melanesicoccus kleinhoviae Williams and Watson and Pulvinarisca; this character is likely to be of importance at the generic level. In Eulecanium tiliae, the claw is often typically carried at fight-angles to the tarsus. There are always two claw digitules and each usually has a broadened or knobbed apex; in some genera they are both very broad (e.g., in most Cardiococcinae) but they may both be narrow and more or less similar to the tarsal digitules or of distinctly dissimilar width. Fine, setose claw digitules are generally associated with a reduction in the size of the legs, but in the Eulecaniinae the claw digitules are never both broad even though the legs are otherwise well developed. The legs may be absent, as in Houardia, or greatly reduced, as in Platinglisia where they are represented by small areas of sclerotisation on the derm. The first indication of a reduction in the structure of a leg appears to be the loss of the tibio-tarsal articulation and the presence of setose claw digitules or digitules of unequal width; with
Taxonomic characters - adult f e m a l e
135
further reduction, all five segments seem to become more or less equally reduced, the articulation between the segments becoming reduced or lost and both claw digitules becoming setose; perhaps the last part of the legs to be lost is the claws, as in Platylecanium cribrigerum (Cockerell and Robinson). On legs which have been much reduced, both the claw and tarsal digitules may lack their terminal dilations or knobs (e.g., as in Acantholecanium). In species in which the body shape is highly asymmetrical, the legs may either be placed symmetrically, as in Perilecanium, or asymmetrically, as in Podoparalecanium.
Antennae (Figs 1.1.3.1.6) The structure of the antennae is of considerable taxonomic importance. The basic structure of most fully developed antennae is remarkably constant. The basal segment (the scape - segment 1) is well developed and invariably has three setose setae, as illustrated by Thro (1903), but these setae are spinose and spatulate in Allopulvinaria. Segment 2 (the pedicel) has one long and one shorter seta on its ventral surface and a campaniform sensilla on the dorsal surface. At the apex of each antenna are three segments (sometimes referred to as the flagellum) which are also remarkably constant in structure. The apical segment has about eight flagellate setae and three fleshy setae (these can be very flagellate in some genera), three on the ventral surface and one on the dorsal; in most species the terminal seta is setose or flagellate and long. The apical segment also has one or more basiconic sensillae. The subapical segment has a single fleshy seta on the ventral surface and a flagellate seta laterally, whilst the third segment from the apex has only a single fleshy seta ventrally (except in Marsipococcus marsupialis (Green) and Paralecanopsis turcica (Bodenheimer) in which it appears to be absent). Between the basal two segments and the terminal three segments there are usually one to four further segments. Almost invariably only the segment nearest the apical three segments has setae and then three flagellate setae are present. However, a few genera do have small, setose setae on these middle segments (e.g., Lichtensia, Megapulvinaria and Pulvinarisca). The number of segments can be very constant within a species, as in Coccus hesperidum where there are always seven, or it can be rather variable as in Kilifia acuminata (Signoret) which may have 6-8 segments; when six segmented, the third segment is very long. In the Coccini, the apical segment is sometimes unusually long, as in Eucalymnatus and to a lesser extent in Coccus. In many primitive Coccoidea, intersegmental sensillae are present between some of the segments but these were not noted in the Coccidae by Koteja (1980), although they were thought to be present in Paralecanopsis turcica Bodenheimer by Hodgson (1994a). However, many genera show a strong reduction in the number of antennal segments - indeed, antennae are absent in the gall-forming Cissococcus. In species with five antennal segments, such as Halococcusformicarii Takahashi, it is generally the third of the terminal segments which appears to be the first to disappear (as in Akermes and Cyphococcus); this is followed by segment 3 and then perhaps segment 2. The last segment to be retained is the apical segment, as in Houardia, Paracardiococcus and Schizochlamidia, where the antennae are represented by simple, knob- or plate-like structures. One of the features associated with the reduction in segmentation is an increase in the number of fleshy setae on the apical segment so that all the setae are fleshy on those species with only one-segmented antennae. Mouthparts (Figs 1.1.3.1.6) On the whole, the structure of the mouthparts is remarkably constant throughout the Coccidae, varying mainly in size, as indicated by the length or width of the labium (although these measurements may not be very reliable as they will vary depending on
Section 1.1.3.1 references, p. 136
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136
how much the labium has been squashed during preparation). The labium is 1-segmented (sometimes indistinctly 2-segmented in nymphs of some species) and coneshaped, usually with four pairs of setae (Koteja, 1974b), although these are difficult to observe in many specimens. The only feature of the mouthparts to vary significantly is the shape of the clypeolabral shield, which may therefore have some taxonomic significance at the genetic level. In Saccharolecanium and Waricoccus, this shield is expanded anteriorly, making it about twice as long as in most Coccidae. In Saccharolecanium, there are also two lateral areas of sclerotisation on the tentoria supporting the shield. The reasons for these modifications are unknown. Vulva The derm surrounding the opening of the vulva is thin and membranous and the opening is usually obscured by the anal tube. However, it can be seen occasionally in good preparations just anterior to the ano-genital fold in the fifth visible segment (segment VI). It appears to have no taxonomic significance.
REFERENCES Beardsley, J.W., 1984. List of terms, and comments on morphological terminology used for descriptions of scale insects. The Scale, 10 (1): 50-52. Ben-Dov, Y., 1988. A taxonomic analysis ofthe armoured scale tribe Odonaspidini of the World (Homoptera: Coccoidea: Diaspididae). United States Department of Agriculture, Agricultural Research Service Technical Bulletin, No. 1723: v + 142 pp. Boratyfiski, K., 1970. On some species of Lecanium (Homoptera, Coccidae) in the collection of the Naturhistorisches Museum in Vienna; with description and illustration of the immature stages of Parthenolecanium persicae. Annales des Naturhistorisches Museum, Wien, 74: 63-76. Borchsenius, N.S., 1957. Sucking Insects, Vol. IX. Suborder mealybugs and scale insects (Coccoidea). Family cushion and false scale insects (Coccidae). Fauna USSR. Zoologicheskii Institut Academii Nauk SSSR, Novaya seriya, 66:493 pp. Borchsenius, N.S., 1959. Contribution to coccid fauna of China. VI. Descriptions of new genera and species of coccids of the family Eriococcidae and Coccidae (Scientific results of the Chinese-Soviet Expeditions of 1955-1957 in South-western China). Entomologicheskoe Obozrenie, 38: 164-175. Brain, C.K., 1918. The Coccidae of South Africa - II. Bulletin of Entomological Research, 9: 107-139. Cox, J.M. and Pearce, M.J., 1983. Wax produced by dermal pores in three species of mealybug (Homoptera: Pseudococcidae). International Journal of Insect Morphology and Embryology, 12: 235-248. De Lotto, G., 1971. On some genera and species of wax scales (Homoptera: Coccidae). Journal of Natural History, 5: 133-153. Ebeling, W., 1938. Host-determined morphological variations in Lecanium corni. Hilgardia, 11: 613-631. Foldi, I., 1991. The wax glands in scale insects: comparative ultrastructure, secretion, function and evolution (Homoptera: Coccoidea). Annales de la Socirt6 Entomologique de France (N.S.), 27: 163-188. Gill, R.J., 1988. The Scale Insects of California Part 1. The Soft Scales (Homoptera: Coccoidea: Coccidae). Technical Services in Agricultural Biosystematics and Plant Pathology, California Department of Food and Agriculture, Vol. 1: xi + 132 pp. 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. Hamon, A.B. and Williams, M.L., 1984. Arthropods of Florida and Neighbouring Land Areas. Vol. 11. The Soft Scales Insects of Florida (Homoptera: Coccoidea: Coccidae). Florida Department of Agriculture & Consumer Services. Contribution 600. Florida Department of Agriculture, Gainesville. 194 pp. 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. Hodgson, C.J., 1969. Notes on Rhodesian Coccidae (Homoptera: Coccoidea): Part III. Arnoldia (Rhodesia), 4(4): 1-42. Hodgson, C.J., 1994a. The Scale Insect Family Coccidae: An Identification Manual to Genera. CAB International, Wallingford. vi + 639 pp. Hodgson, C.J., 1994b. Enochiton and a new genus of the scale insect family Eriococcidae (Homoptera: Coccoidea). Journal of the Royal Society of New Zealand, 24: 171-208. Hodgson, C.J., 1995a. The possible evolution of the plate-like structures associated with the anal area of the lecanoid Coccoidea. Israel Journal of Entomology, 29: 57-65. Hodgson, C.J., 1995b. A brief review of the structure of the spiracle in the family Coccidae. Israel Journal of Entomology, 29: 47-55.
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Kosztarab, M., 1996. Scale Insects of Northeastern North America. Identification, Biology and Distribution. Virginia Museum of Natural History, Special Publication No. 3. Martinsville, Virginia, viii + 650 pp. Kosztarab, M. and Koz,,ir, F., 1988. Scale Insects of Central Europe. Series Entomologica, Vol. 41. W. Junk, Dordrecht. 456 pp. Koteja, J., 1974a. The occurrence of campaniform sensillum on the tarsus in the Coccinea (Homoptera). Polskie Pismo Entomologiczne, 44: 243-252. Koteja, J., 1974b. Comparative studies on the labium in the Coccinea (Homoptera). Zeszyty Naukowe Akademii Rolniczej w Krakowie, 27: 1-162. Koteja, J., 1979. A revision of the genus Poaspis Koteja (Homoptera, Coccidae). Polskie Pismo Entomologiczne, 49:451-474. Koteja, J., 1980. Campaniform, basiconic, coeloconic and intersegmental sensilla on the antennae in the Coccinea (Homoptera). Acta Biologica Cracoviensia, Series Zoologia, 22: 73-88. Koteja, J. and Lubowiedzka, A., 1976. On some changes of the cuticle in the female Saissetia hemisphaerica Targioni Tozzetti (Homoptera, Coccinea). Acta Biologica Cracoviensia. Series Zoologia, 19: 71-77. Miller, D.R., 1984. Terminology. The Scale, 10: 47-49. Qin, T.K. and Gullan, P.J., 1989. Cryptostigma Ferris: a coccoid genus with a strikingly disjunct distribution (Homoptera: Coccidae). Systematic Entomology, 14: 221-232. Qin, T.K. and Gullan, P.J., 1992. A revision of the Australian pulvinariine sof~ scales (Insecta: Hemiptera: Coccidae). Journal of Natural History, 26: 103-164. Steinweden, J.B., 1929. Bases for the generic classifications of the coccoid family Coccidae. Annals of the Entomological Society of America, 22: 197-245. Takagi, S., 1990. Disc pores of the Diaspididae: microstructure and taxonomic value (l-lomoptera: Coccoidea). Insecta Matsumurana (New Series), 44: 81-112. Takagi, S., 1992. A contribution to conchaspidid systematics (Homoptera: Coccoidea). Insecta Matsumurana (New Series), 46: 1-71. Tamaki, Y., Yushima, Y. and Kawai, S., 1969. Wax secretion in a scale insect, Ceroplastes pseudoceriferus Green (Homoptera: Coccidae). Japanese Journal of Applied Entomology and Zoology, 4: 126-134. Thro, W.C., 1903. Distinctive characteristics of the species of the genus Lecanium. Bulletin of Cornell University Agricultural Experiment Station, Ithaca, N.Y., 209: 205-221. Williams, D.J., 1985. Australian Mealybugs. British Museum (Natural History), London. iv + 431 pp. Williams, D.J. and Granara de Willink, M.C., 1992. Mealybugs of Central and South America. CAB International, Wallingford. 635 pp. Williams, J.R. and Williams, D.J., 1980. Excretory behaviour in soft scales (Hemiptera: Coccidae). Bulletin of Entomological Research, 70: 253-257. 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 of the Virginia Polytechnic Institute and State University, Blacksburg, 74: viii + 1-215.
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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.
139
1.1.3.2 Taxonomic Characters Adult Male JAN H. GILIOMEE
INTRODUCTION The adult males of the Coccidae present many characters that can be used for taxonomic purposes. Thus, comparative studies of the males of more than 50 species by Giliomee (1967) and Miller (1991) showed that these characters can be used to separate the various species, genera and species-groups within the Coccidae and to separate the Coccidae from related families. This Section is based mainly on the studies of these two workers. In general it appears that adult male Coccidae are morphologically homogeneous (Giliomee, 1967; Miller, 1991) and that there are no major differences between subdivisions, as was found by Ghauri (1962) for the males of the Diaspididae. In the Coccidae individual characters appear to be very variable. Thus the number of setae, especially the fleshy setae, occurring in the different body regions usually varies within the species and major characters such as the number of antennal segments and simple eyes, the tubular or non-tubular structure of the scutellum, the presence or absence of halteres and the number of sclerites on the abdomen vary within the family. The number of simple eyes even varies within the genus Eulecanium (Miller, 1991). As a result very few characters are sometimes available to distinguish between the different taxa. Thus, Neolecanium cornuparvum (Thro) could only be separated from Toumeyella liriodendri (Gmelin) by comparing the length of antennal segments III-V and the metatibia in relation to other body structures (Miller, 1991; Miller and Williams, 1995). Also the number of characters separating the species-groups defined by Giliomee (1967) and by Ray and Williams (1983) were reduced, even to single characters, as the males of more species were studied (Miller, 1991). This is also true for the number of characters separating the families of the Coccoidea and in producing a key to the families (Giliomee, 1995) surprisingly few characters were available. The taxonomic characters of the adult male Coccidae, which are discussed here, are illustrated in Fig. 1.1.2.2.2 of Section 1.1.2.2.
HEAD The shape of the head can be used to separate the Eriopeltis-group from the other groups of species. In lateral view, it appears flattened in the Eriopeltis-group but dorsoventrally elongated or rounded in other groups. This character is, however, difficult to see in slide-mounted specimens. The degree of development of the
Section 1.1.3.2 references, p. 142
140
Systematics
midcranial ridge varies considerably within the family and the absence of the dorsal part, the lateral arms and the posterior extension of the ventral part can be used to separate genera. The length of the preocular ridge also varies considerably: in some genera and species-groups it reaches the midcranial ridge ventrally, but in others it does not extend much below the articulation with the scape. Similarly, the development of the postocular ridge can be used to separate genera or species-groups. It is absent dorsally in the Protopulvinaria-group and vestigial ventrally in the Philephedra-group, while it forks below the ocellus in all species examined by Giliomee (1967), except those of the Eriopeltis-group. The latter are also characterized by the presence of a strong interocular ridge, but unfortunately both the interocular ridge and the forking of the postocular ridge are difficult to see in slide-mounted specimens. The preoral ridge shows little variation but is absent in some species. The cranial apophysis varies in size and in the shape of its apex (truncate, bifurcate or trifurcate) and this character can be used to separate species and genera. The simple eyes are very conspicuous and, since their number varies between four and ten, it is a very useful character. It is not constant for groups but can be used to separate closely related genera or species. The large size of the dorsal and lateral eyes is characteristic of the Philephedra- and Inglisia-groups respectively. The number of antennal segments can be used to separate the Toumeyella-group from all other species-groups: in this group the antennae have nine segments (eight in some apterous forms) compared to ten in all other groups (Ray and Williams, 1983; Miller, 1991). Other structural characters of the antennae that can be used to separate genera are its length in relation to some other body structures, the length and width of the first three segments and the shape of the terminal segment.
THORAX The thorax provides a few structural characters that can be used for identification and classification. The emargination of the mesoprephragma and the length to width ratio of the mesothoracic scutum can be used to separate genera and species, while the size of the scutellar foramen can serve as a genetic character or to separate some species-groups from other groups. Pleurally, a well developed basalare (joining the pleural wing process with the mesepisternum) separates the Eulecanium-, Philephedra-, Eriopeltis- and Sphaerolecanium-groups from the Coccus-, Protopulvinaria- and Toumeyella-groups, where it is vestigial (Miller, 1991). Ventrally the development of the median ridge of the basisternum can be used to separate genera where it is complete, from those where it is absent or incomplete.
WINGS The shape of the fore wings is an important character and can be used to separate the
Eriopeltis-group, where the wing is more than 2.75 times longer than wide, from the other groups. Within other groups, the length to width ratio can be used to separate genera. The halteres are absent in the winged males of all species-groups, except the Eulecanium-group as redefined by Miller (1991), where they are present and serve as an exclusive species-group character.
LEGS The appearance of the legs is fairly constant within the family, but the relative length of the legs, and the length to width ratio of the hind femur and hind tarsus can be used to differentiate amongst species-groups, genera and species.
Taxonomic characters - adultmale
141
ABDOMEN The abdomen is largely membranous, but bears a number of useful taxonomic characters. The degree of sclerotization is variable and even the pleural sclerotization, which was considered to be absent in the Eulecanium-group (Giliomee 1967), was later found to be present in one species of the genus Eulecanium (Miller, 1991). The absence or presence of some of the tergites, especially the IXth, can be used at the genetic and specific levels. However, care should be taken in using the sclerites as diagnostic characters as their appearance is affected by the degree to which the specimens are stained. A prominent caudal extension on segment VII is characteristic of the Coccusand Toumeyella-groups, while the shape of the caudal extension on segment VIII (cylindrical, rounded, geniculate, mammillate etc.) is characteristic for species, genera or species-groups. The presence of a cicatrix on the distal part of this extension or lobe is the only exclusive character of the Coccus-group (Miller, 1991). Another conspicuous structure on segment VIII is the glandular pouch with its multilocular pores and setae. It is absent in all the genera so far studied in certain species-groups (Protopulvinaria and Toumeyella), but in the Coccus-group it is only absent in one species of the genus Ceroplastes. The structures of the genital segment vary in size at the genetic and specific level and this can be expressed in ratios such as length of penial sheath to body length, length of basal rod to length of aedeagus, length of aedeagus to length of penial sheath and length of aedeagus to length of basisternum. The absence of the basal rod separates Mesolecanium nigrofasciatum Pergande from all other species.
DERMAL STRUCTURES The location, number and shape of the setae are important taxonomic characters. The number of setae, especially the fleshy setae, varies intraspecifically, but differences in the ranges of each species may be used to discriminate interspecifically. The value of the setae as species-group characters has diminished as more species became known. Thus, fleshy dorsal head setae and ventral head setae were absent in 11 species of the Eulecanium-group studied by Giliomee (1967) and present in most other species-groups. However, Miller (1991) found a single fleshy seta on both locations in one of the three Eulecanium-species studied by him, indicating that these characters can even vary within a genus. Similarly the presence of dorsal ocular setae seemed to be an exclusive character of the Coccus group, but were then found to be present in the genus Ctenochiton of the Eulecanium-group (Giliomee, 1967). More recently, Miller (1991) found that they were absent in one of the four species of Pulvinaria but present in all the other species of the Coccus-group to which Pulvinaria belongs. The genal setae are absent in all the species of some species-groups studied, Eulecanium, Philephedra, Sphaerolecanium and Eriopeltis and present in others Coccus and Protopulvinaria. In the Toumeyella-group, however, they are present in all the species, but in Mesolecanium nigrofasciatum may be either absent or present (Miller and Williams, 1995). On the antennae, the absence of the capitate subapical setae is characteristic of the Philephedra-group, while in other groups deviation from the regular number of three can be used to separate genera. The length of the fleshy antennal setae relative to the length or width of the associated segments appears to be a species specific character in some genera. Some of the thoracic setae are fairly constant in number and it appears that variations can be used to differentiate between species-groups, genera and species. Examples are the medial pronotal, posttergital, prosternal, scutal, postmesospiracular, basisternal, antemetaspiracular, dorsometaspiracular, postmetaspiracular, anterior metasternal and
Section 1.1.3.2 references, p. 142
Systematics
142
posterior metasternal setae. Thus, Miller (1991) regarded the presence of more than nine fleshy basisternal setae as unique to the monospecific Protopulvinaria-group. Hair-like basisternal setae have so far only been found in two genera, but unfortunately they are absent in some specimens and can therefore only be used as a supporting character. The presence or absence of scutal and tegular setae was used to separate genera by Giliomee (1967), while Miller (1991) used the presence of hair-like scutellar setae to distinguish Toumeyella cerifera Ferris from the other species in this genus. The latter also used the presence of circular pores on the posttergite and scutellum to separate two species of the genera Toumeyella and Philephedra respectively. The wings and legs possess a number of characters of genetic and specific significance. On the wings, the presence of alar setae and the number of haltere setae are important, while examples on the legs are the presence and shape (capitate or not) of the coxal bristles, the length of the apical seta of the front coxa, the length of the apical seta on the front trochanter, the length of the tibial spur in relation to the length of the tarsus, the length of the fleshy setae in relation to the length of the tibia and the ratio of fleshy to hair-like setae on specific segments. The setae of the abdomen can also be used to separate groups, genera and species but because of individual variation, they serve mostly as supplementary characters. Thus, the absence of fleshy abdominal setae are characteristic of the Eulecanium- and Philephedra-groups, as defined by Miller (1991), while none of these setae are found on the IVth to VIIIth abdominal segments in the Sphaerolecanium-group. The presence of fleshy setae on the penial sheath distinguishes Ceroplastes ceriferus (Fabricius) from the other Ceroplastes species. The fleshy setae lateral to the glandular pouch on the VIIIth abdominal segment appeared to be characteristic for the genus Ceroplastes (Giliomee, 1967) but was found to be absent in C. ceriferus (Miller, 1991). The circular pores occurring dorsally on the 1st abdominal segment and in the ante-anal region seem to differ among genera and species.
REFERENCES Ghauri, M.S.K., 1962. The morphology and taxonomy of male scale insects (Homoptera: Coccoidea). British Museum (Natural History), London, 221 pp. 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. Giliomee, J.H., 1995. An annotated key to the families of scale insects (Homoptera: Coccoidea) based on the characters of the adult male. Israel Journal of Entomology, 29:11-17. 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, Alabama, USA. Miller, G.L. and Williams, M.L., 1995. Systematic analysis of the adult males of ToumeyeUa group, including Mesolecanium nigrofasciatum, Neolecanium cornuparvum, Psedophilippia quaintancii, and Toumeyella spp. (Homoptera: Coccidae) from America North of Mexico. Contributions of the American Entomological Institute, 28(4): 1-68. 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.
Soft Scale hlsects - Their Biology, Natural Enemies and Control
Y. Ben-Dovand C.J. Hodgson(Editors) 9 1997 Elsevier Science B.V. All rights reserved.
1.1.3.3
143
Taxonomic Characters - Nymphs
MICHAEL L. WILLIAMS and GREG S. HODGES
INTRODUCTION In spite of the fact that the taxonomy of the immature stages has proven to be very helpful in determining relationships within the armored scales (Diaspididae) (Howell and Tippins, 1990), the study of the immature stages of the Coccidae is in its infancy. Most of the research has been conducted on the first-instar nymphs, with little attention being paid to the other immature stages. This section, therefore, deals mainly with the taxonomic characters of the first-instar nymphs. For a discussion of the morphological characteristics of the other immature stages, see Section 1.1.2.3, Morphology of the Immature Stages.
TAXONOMIC CHARACTERS OF FIRST-INSTAR NYMPHS Tables 1.1.3.3.1 and 1.1.3.3.2 present a summary of the various character-states seen in first-instar nymphs of the Coccidae. The higher classification system used in the tables follows that presented by Hodgson (1994) based on adult male and female characters. The body of first-instar nymphs are usually oval to elongate-oval, 300-1100/xm long and 200-700 #m wide. The derm is membranous and usually relatively smooth. However, in first instars of the Cardiococcinae the derm is rugose or papillate. This condition is also seen in Pseudopulvinaria sikkimensis (Atkinson) (Hodgson, 1991), and Ctenochiton aztecas Townsend and Cockerell. According to Hodgson (1970), the dorsal surface of L a g o s i n i a vayssierei (Castel-Branco) is membranous, but thrown into small distinct folds. Characteristics of the derm may be helpful both at the subfamily and species level.
DORSAL STRUCTURES Dorsal setae. Dorsal body setae (Fig. 1.1.3.3.1-B) are present in only 30% of the species which have been studied (Table 1.1.3.3.1). When present, there are usually four pairs of slender, bristle-like body setae in the thoracic region, although in Alichtensia orientalis Lahille, these setae are larger and stouter. Dorsal pores. The most common pores on the dorsum are simple disc pores (Fig. 1.1.3.3. I-C), bilocular pores (Fig. 1.1.3.3.1-F,G) and trilocular pores (Fig. 1.1.3.3.1-1)). Generally, pore groupings are located in rows submarginally, submedially and/or medially. Bilocular pores are categorized as small (1-2 #m) or
Section 1.1.3.3 references, p. 156
144
Systematics
1t
,...
.
2
6 A
B L
_
k
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I
1
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O Fig. 1.1.3.3.1. Variations in setae, pores and ducts on first-instar nymphs of Coccidae. (A1-6): marginal setae: 1 - Eriopeltis festucae; 2 - lnglisia patella; 3 - ToumeyeUa mirabilis; 4 - Ceroplastodes dugesii; 5 Paralecanopsisformicarum; 6 - Coccus hesperidum. (111-3): body setae. (C1-4): simple disc pores: 1 - C. hesperidum; 2,3 - I. patella; 4 - Pseudokermes nitens. 0)1-2): dorsal trilocular pores: 1 - P. f o r m i c a n o n ; 2 - C. hesperidum. (E): invaginated biloeular tubercles on Pseudophilippia quaintancii. (F1-2,G)" bilocular pores: 1 - Parthenolecanium quercifex; 2 - Parthenolecanium coral, P. quercifex. (H): dorsal microduct. (I): dorsal tubular duct. (J1-12): ventral pores: 1,2 - lO'lifia americana; 3,4 - Protopulvinaria pyriformis; 5 , 6 , 7 - C. hesperidum; 8 , 9 - I. patella; 10,11,12- P. formicarum. (K1-3): ventral microducts.
Taxonomic characters - n y m p h s
145
large (4-8 #m). Both the size and arrangement of dorsal pores are useful in separating species. For example, on Parthenolecanium quercifex (Fitch), the bilocular pores are of two sizes (Fig. 1.1.3.3.1-F~,F2), while on P. corni (Bouch6), they are all small (Fig. 1.1.3.3.1-F2) (Hedges, 1996). Many species have a pair of trilocular pores (Fig. 1.1.3.3.1-D) on the head just anterior to or above the antennal bases. Several genera and species have pores which are unique. The woolly pine scale, Pseudophilippia quaintancii Cockerell, has large invaginated bilocular tubercles (Fig. 1.1.3.3. I-E), each containing two quinquelocular pores, scattered over the dorsum (Ray and Williams, 1980). On Toumeyella parvicornis (Cockerell), the bilocular pores occur in clusters (Fig. 1.1.3.3.1-G) arranged submarginally around the body (Sheffer and Williams, 1990). The simple disc pores on Inglisia patella Maskell are of two types, the common type (Fig. 1.1.3.3.1-C3) and a larger, more dense, simple disc pore (Fig. 1.1.3.3.1-C2) which is located in a marginal row just dorsal to the marginal setae. The type and arrangement of dorsal pores are important taxonomic characters for identifying genera and species. Dorsal tubular ducts. Structures that some authors have called tubular ducts are found on the dorsum (Fig. 1.1.3.3. I-I) but are currently only known on species of the genera Ceronema and Kozaricoccus. On Ceronema banksiae Maskell, they form two submedian longitudinal rows, and also a row submarginally around the body (Morrison and Morrison, 1922). It is more likely that these pores are highly modified dorsal microductules. Dorsal microductules. Microductules (previously referred to as dorsal microducts) on the dorsum (Fig. 1.1.3.3. I-l-I) have only been detected on a few species, e.g., Inglisia patella, Protopulvinaria pyriformis (Cockerell) and an undescribed species of Parafairmairia. The taxonomic significance of this character has yet to be determined. Anal plates. Two well-developed, triangular anal plates are usually present (Fig. 1.1.3.3.2-A,E). The presence of anal plates is generally used as a diagnostic character for the family Coccidae, but they are absent on the first instar of Bodenhiemera rachelae (Bodenheimer) (Fig. 1.1.3.3.2-C) (Ben-Dov, 1969; Hodgson, 1994), Kozaricoccus bituberculatus (Brain) (Hodgson, 1971), Mallococcus sinensis (Maskell) (Lambdin and Kosztarab, 1973) and Paralecanopsis turcica Bodenheimer (Hodgson, 1994). In Pseudopulvinaria sikkimensis, the anal plates are located at the apex of the abdomen (Fig. 1.1.3.3.2-D) and resemble the sclerotized anal lobes of some Eriococcidae (Hodgson, 1991). Hodgson (1995) presents evidence which strongly supports the view of earlier workers that the anal plates of Coccidae, in fact, evolved from the anal lobes. On Paralecanopsis formicarum (Newstead), the anal plates are fused at the anterior end, and appear as a single arched plate over the anal cleft (Fig. 1.1.3.3.2-10. Each anal plate generally has three to four setae present, typically with three apically and one on the mesal margin. The median apical seta of each plate is greatly enlarged, usually being 1/3 to 1/2 as long as the entire body, and is a good diagnostic character for the first instar. One ventral subapical seta is present per plate and the ano-genital fold has one pair of fringe setae. Qin and Gullan (1989) figured 10-14 setae on the dorsum of each anal plate for Cryptostigma endoeucalyptus, and stated that the plates were sometimes unequal in shape, one being narrow and the other half-oval. The dorsal plate surface may be reticulated or have a shingle- or scale-like pattern (Fig. 1.1.3.3.2-A,E). Sheffer and Williams (1990) found these plate patterns to be useful in separating species of the genus Toumeyella.
Section 1.1.3.3 references, p. 156
146
Systematics
A n a l r i n g . This is subcircular, circular or hexagonal in shape (Fig. 1 . 1 . 3 . 3 . 2 - B ) and a l w a y s has 6 setae and 10-14 irregularly shaped pores. T h e r e is g e n e r a l l y little difference in the shape or size o f the anal ring between species within genera.
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Characteristic structures of the anal area of first-instar Coccidae.
A: anal plates of
Mesolecanium nocturnum. B: anal ring of Pseudophilippia quaintancii. C" anal lobes of Bodenhiemera rachelae. D: anal lobes of Pseudopulvinaria sikkimensis. E: anal plates of Kilifia americana. F: anal plates of Paralecanopsis formicarum.
Taxonomic characters nymphs
147
-
MARGINAL STRUCTURES Eyespots. These are composed of a single facet and are located on the margin or slightly dorsal, at about 45 degrees to the base of each antenna. Marginal setae. These vary in shape from slender and hairlike to stout, conical or lobate (Fig. 1.1.3.3. l-A). Most commonly, they number 32 around the body, generally distributed as follows: eight anteriorly between the eyes, two on each side between the eyes and the spiracular setae, two on each side between the anterior and posterior spiracular setae and eight on each side of the abdomen. Marginal setae occur in a single row except on Cryptostigma endoeucalyptus Qin and Gullan, where they are in a double row. Variations in the number of marginal setae range from 32 in most species, up to 350 on C. endoeucalyptus (Qin and Gullan, 1989). Other species with high numbers include: 42 in Philephedra ephedrae (Cockerell); 44 in Physokermes hemicryphus (Dalman); 46 in Cryptes baccatus (Maskell); 56 in Cyclolecanium hyperbaterum Morrison; 62 in Cryptostigma biorbiculus Morrison; 64 in Cryptostigma inquilina (Newstead) and 120 in Inglisia patella. Several unusual types of marginal setae are found in first-instar Coccidae. Such types include: truncate marginal setae
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Fig. 1.1.3.3.3. Margin of body in area of the spiracular setae of first-instar Coccidae. A: Toumeyella parvicornis. B: Paralecanopsisformicarum. C" Cyclolecanium hyperbaterum. D: Inglisia patella.
Section 1.1.3.3 references, p. 156
Systematics
148
(Fig. 1.1.3.3.1-A~), which occur in the head region of species of Eriopeltis; bulbous marginal setae (Fig. 1.1.3.3. I-A:) which are found around the entire body on Inglisia patella, while on Ctenochiton aztecus, the marginal setae are long at the apex of the head and small and lanceolate around the rest of the body. In Paralecanopsis formicarum, the marginal setae between the anterior and posterior spiracular furrows are slender but are broad at the base and tapering to a slender point around the rest of the body (Figs. 1.1.3.3.1-As and 1.1.3.3.3-B). Spiracular (stigmatic) setae. The shape, size and number of spiracular setae are important characteristics at both the generic and specific levels. Most commonly, the spiracular setae are differentiated from the marginal setae and occur in groups of three, with the median seta being longer than the lateral setae. On some species, however, the spiracular setae are not differentiated from the marginal setae, as on Toumeyella parvicornis (Fig. 1.1.3.3.3-A) and Inglisia patella (Fig. 1.1.3.3.3-D). Various forms and arrangements of spiracular setae in first instars are illustrated in Figs. 1.1.3.3.3 and 1.1.3.3.4. Different numbers of spiracular setae also occur, as seen on the following: Inglisia vitrea Cockerell (Fig. 1.1.3.3.4-H) with a single long seta at the apex of each spiracular furrow; Tectopulvinaria loranthi Froggatt with two long setae at each furrow; Mallococcus sinensis with two at each anterior furrow and three at each posterior furrow and Cyclolecanium hyperbaterum with three at each anterior furrow and four at each posterior furrow (Fig. 1.1.3.3.3-C).
9
|
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:
H
Fig. 1.1.3.3.4. Variations in spiracular setae of first-instar Coccidae. A: ToumeyeUa mirabilis. B" Kilifia americana. C: Parthenolecanium quercifex. D: Ceroplastes ceriferus. E: Vinsonia stellifera. F: Luzulaspis luzulae. G: Ceroplastodes dugesii. H: Inglisia vitrea.
149
Taxonomic characters - nymphs
Spiracular (stigmatic) clefts. These are generally not well developed but, in some species of Cryptostigma, the spiracular clefts are distinct.
VENTRAL STRUCTURES Ventral setae. Body setae are usually short and bristle-like, and their size and arrangement usually do not offer a reliable means of separating taxa. However, on Inglisia patella, there are a pair of long slender setae near the anterior margin of the head, which appear to be unique for this species. The number and position of most setae does not appear to vary much with, for instance, all known species having one pair of interantennal setae. The number of ventral submedian setae, on the other hand, may prove to be a useful character. Most species have three pairs, but on many species in the Cardiococcinae, on several of the Eulecaniinae and on Ctenochiton aztecus and Pseudopulvinaria sikkimensis, there are six pairs. Furthermore, on Kilifia acuminata (Signoret) and Filippiafollicularis (Targioni-Tozzetti), there are two pairs and there is only one pair present on species in the Ceroplastinae and on Lagosinia vayssierei. Ventral pores. Disc-pores occur only in the spiracular furrows or in and around the peritreme of the spiracle. These pores may be trilocular (Fig. 1.1.3.3.1-Ji.5), as seen on Protopulvinaria pyriformis, Kilifia americana, lnglisia patella, Milviscutulus mangiferae (Green) and Parasaissetia nigra (Nietner); quadrilocular (Fig. 1.1.3.3.1-J6.7), as on Akermes cordiae Morrison, Coccus hesperidum L., Neolecanium cornuparvum (Thro), Pseudophilippia quaintancii and on species of Toumeyella; quinquelocular (Fig. 1.1.3.3.1-Js.~0) as on most other species of Coccidae; or multilocular (Fig. 1.1.3.3.1-Jll.lz) as on Paralecanopsis formicarum which has 7-1oculed pores. Disc-pores are usually arranged in a row running between each spiracle and the spiracular setae but, on P. formicarum, they occur in clusters near the peritreme of the spiracles, with a few pores even appearing to be within the peritreme itself. Normally only one type of pore occurs, but sometimes both four- and five-locular spiracular discpores occur on a single species. On Physokermes hemicryphus, the spiracular furrows have a mixture of trilocular and multilocular disc-pores (Hodges, 1996). Ventral microducts. Ventral microducts (Fig. 1.1.3.3.1-Ki.3) have been found on most species studied. The number and arrangement of the ducts may differ somewhat between species, and the shape of the microduct orifice may also vary, but this has not been used much as a diagnostic character. Ventral tubular ducts. nymphs of soft scales.
Ventral tubular ducts are absent in all known first-instar
Antennae. The antennae are mostly 6-segmented (Fig. 1.1.3.3.5-A), but in almost all species of the Myzolecaniinae they are 5-segmented (Fig. 1.1.3.3.5-B). There is always a simple sensory pore on the second segment, and fleshy sensory setae usually occur on the last three segments of 6-segmented antennae and the last two segments of 5-segmented antennae. Mouthparts. The mouthparts vary little between species and have not been used much as a diagnostic feature. Canard (1965) used measurements of the stylet loop length in first instars as a supplementary character for separating six species of Pulvinariini. Spiracles. In Ctenochiton aztecus, the spiracle is surrounded by a sclerotized area, but in most species such sclerotizations are absent.
Section 1.1.3.3 references, p. 156
150
Systematics
9.'....,..: // .
:!i
A
B
--.,,.. : .~ 9 ....
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G
Fig. 1.1.3.3.5. Antenna, leg and claw variations on first-instar Coccidae. A: 6-segmented antennae. B: 5-segmeated antennae. C: leg of Kilifia americana. D" leg of Ceroplastodes dugesii. E: claw of Alecanium hirsutum. F: claw of Coccus hesperidum. G: claw of Toumeyella sonorensis. M: Microcteaidia.
Taxonomic characters - nymphs
151
Legs. The legs are well developed and 5-segmented in all the species studied. Characteristics of the legs which may be important as taxonomic characters include: a) leg length in relation to body size, as in most species of the Cardiococcinae, where the legs are extremely long; b) the number and length of setae on the trochanter, e.g., one long seta on the trochanters of Coccus hesperidum, two long setae on the trochanters of Eulecanium tiliae (L.) and one long and one short seta on each trochanter of Ceroplastodes dugesii (Signoret); c) presence of an extremely long seta on the femur which extends to near the apex of the leg (Fig. 1.1.3.3.5-C), as seen on Etiennea petasus Hodgson, Kili.fia americana Ben-Dov, Milviscutulus mangiferae and Protopulvinaria pyriformis, and d) presence or absence of microctenidia (Fig. 1.1.3.3.5-M) at the apex of the tibia. There are also some differences in shape and size of the claw, e.g., short and stout on Alecanium hirsutum Morrison (Fig. 1.1.3.3.5-E) and long and slender on Coccus hesperidum (Fig. 1.1.3.3.5-F) and Toumeyella sonorensis (Cockerell and Parrott) (Fig. 1.1.3.3.5-G). Variations in the claw digitules may also prove to be useful as more species are studied.
CONCLUSIONS The classification system used in Table 1.1.3.3.1 is based on characteristics of the adult male and female, but one can make some assumptions about the relationships of species within the different subfamilies based on characters of the first-instar nymphs studied and listed in Table 1.1.3.3.1. Characters shared by the genera and species in the Cardiococcinae include" rugose or papillate derm, presence of six pairs of ventral submedian setae, long legs (at least 2/3 the body length), quinquelocular pores in the spiracular furrows, and dorsal pore patterns which include simple disc, bilocular and trilocular pores. Inglisia patella does not belong in this group. The Coccinae is a large group which is split into three tribes. For the most part, they share the following characteristics: six antennal segments, one trochanter seta, smooth derm, 32-34 marginal setae, absence of dorsal ducts, three spiracular setae per group with median seta longest and three pairs of ventral submedian setae. Questions arise about the genera Etiennea, Kilifia, Milviscutulus and Protopulvinaria. All differ from other members of the Coccinae in possessing: a) a long femoral seta (as long as or longer than the tibia and tarsus combined), b) long anal plates, c) dorsal pore patterns which are similar and d) trilocular pores in the spiracular furrows (except Etiennea which has quadrilocular or quinquelocular pores). These genera seem to be closer to each other than to other members of their respective tribes. Perhaps they should be grouped as a separate tribe or maybe even subfamily. Also note that Pseudokermes nitens of the Cardiococcinae has this unusual long femoral seta. Another question concerns the genus Lagosinia which has only one spiracular seta and only one pair of ventral submedian setae instead of the usual three pairs, a character which is also seen in the Ceroplastinae. Members of the Eulecaniinae have smooth derm, two trochanter setae and six pairs of ventral submedian setae. The genus Sphaerolecanium does not fit here and probably belongs with the Coccinae in the tribe Saissetiini. The Filippiinae seem to be a collection of genera and species which have a variety of characteristics. Most have two trochanter setae, quinquelocular pores in spiracular furrows and three pairs of ventral submedian setae, but other characteristics vary. Most of the species tend to have an elongate body shape (except Filippia). Filippiafollicularis also has only one trochanter seta. The two genera and species studied in the Ceroplastinae, Ceroplastes ceriferus and Vinsonia stellifera, show definite relationships with each other.
Section 1.1.3.3 references, p. 156
TABLE 1.1.3.3.1 Character-states in first-instar nymphs of soft scale insects (Homoptera: Coccidae). Where Ant. - antennae; Don. -dorsal; Fem. - femur; le - length; Marg. - marginal; segs. - segments; spir. - spiracular; Troch. - trochanter; and where: Rt - reticulated; sh - shingled; Lb - lobed; Sm - smooth; Ru - rugose; Pap - papillated; D - simple disc pore; B - bilocular pore; T - trilocular pore; L - long; S - short; Nd - not differentiated; Se - subequal; V M ducts - ventral median ducts; V W setae - ventral submedian setae; (+) - present; (-) - absent, except for leg length where (+) - legs approximately 213rds body length and (-) - legs approximately 113rd body length. Taxon
Ant. seg.
Leg le
Troch. setae
+ + +
1L 1L 2us 1L
Fern. setae
Anal plate
Derm
Marg. setae
Rt Sh,Rt Rt Sh,Rt
Sm Ru Pap
Dors. setae
Dors. pores
Dors. ducts
Spir. setae
Spir. pores
DT DBT BT DBT
+
Nd 111L Nd lllL
3
Ru
120 32 32 34
Sm Sm Sm Sm Sm
34 32 64 32 34
DBT BT ? BT BT
313Ls 313LS 313LS 313Ls 313Ls
4 5 5 3 5
Sm Sm Sm Sm Sm Sm
32 32 32 32 32 38
? BT DT BT DT DT
lllL 313LS 313Se 313LS 313LS 212L
5
VM
ducts
VSM setae
CARDIOCOCCINAE Inglisia patella I. vitrea Ceroplasrodes dugesii Pscudoketmes nirens
COCCINAE coccini Coccus hesperidum Eucalymnarus fessellatus KiliJia acuminara K. americana Mesokcanium nocrumum
PUlVinariiai Logosinin vayssierei M i l v i ~ ~ ~ tmangverae ~lus Neopulvinaria innumerubilis Proropulvinaria pyrifonnis Pulvinaria acericola Tecrooulvinaria loranrhi
6 6 6
6
6 6
6 6 6 6 6 6 6 6 6
1L 1L 1L
1L 1L 1L 1L 1L 1L 1L 1L
-
+
+ + + +
Rt Rt ?
Sh Rt ?
Rt Sh,Rt Rt Sh Sh
+
+ + + +
+
3 6 6 6
5 5 5
3
5
3
5
5.4
+ + ? + + + + + + +
3 3 2 3 3 1 2 3 2 3
3
TABLE 1.1.3.3.1 (continued) Taxon
Ant. seg.
Leg le
Tmh. setae
Fem. setae
Anal plate
Derm
Marg. setae
6 6 6 6 6 6
1L 1L 1L 1L 1L 1L
+
Rt Sh,Rt Sh,Rt Sh,Rt Sh,Rt Sh,Rt
Sm Sm Sm Sm Sm Sm
32 32 32 32 32 34
6 6 6 6 6
2UL ?
-
Sm
32 46
2UL
-
-
Rt ? Sh Sh Sh
-
Sh
Sm Sm Sm Sm
Don. setae
Don. pores
Don.
ducts
Spir. setae
Spir. pores
VM
VSM setae
3l3LS 313LS 313LS 3l3LS 3l3LS 3l3LS
5,4 3 5 5,4 5
+ + + + +
3 3 3 3 3 3
313Se 212Se
5 5
ducts
COCCINAE (continued) Etiennea petasus Parasaissetia nigra Parrhenolecanium corni P. qurrcifu Saissetia cofleae S. oleac
EULECANIINAE
Eukconiwn riliae Crypus baccatus Physokcwnes hcmicryphus SphaerolecMium prunastri Rhodococcus perornorus
FILIPPIINAE
Alichtensia orientalis Cemnema banktiae Filippia follicularis Kozaricoccus bituberculatus Philephedra ephedrae M a l l o c o c c ~sinensis Merapulvinaria lycii
CEROPLASTINAE
Ccmplastes ceriferus Vinsonia stellifera
1L 2UL
2us
?
Sm Sm Sm
Sm
6 6 6 6 6 6 6
1L 4(1U3S) 2us 2us 2UL -
Sh,Rt Lb Sh,Rt Sh,Rt
Sm
6 6
1L 1L
Sh Sh
Sm
?
?
Lb
Sm
Sm
Sm
+ +
D DT
BT BT D D
+
DBT
32 36
+ +
DT DBT DBT
36 ? 34 26 42 32 34
+ + + +
44
34 32
?
?
D
Nd
3l3Se 212Se
+ + +
DBT
lllL Nd 3l3Se 3l3Se 313Se 213LS 313Se
DT DT
313Se 313Se
?
DT D DT
B
5
-I-
+ + +
3
5 5
5 ?
6 2(?) 6 3 6
3 ?
?
5,4 5,3 5,4 5 5
-
+ + +
2 3 3 3 3
5
+ +
1 1
5
~
TABLE 1.1.3.3.1 (continued) Taxon
ERIOPELTINAE
Enopcltis festucae Luzulaspis luzulae
MYZOLECANIINAE
Akrnnes cordiae Alecanium hirsurum Cryprostigma biorbiculur C. inquilina Qclolecanium hyperbaterum Megasaissctia inflatum Neolecanium comuparvum Pseudophilippia quaintancii Toumcyclla mirabilis T. sonorensis
PSEUDOPULVINARIINAE
Pseudopulvinana sikkimensis
UNPLACED
Crenochiton viridis Crenochiton azrecus Paralecanopsis fonnicanun Parafainnairia wacilis
Ant. seg.
Leg le
Truch. setae
6 6
1L 1L
5 6
1L 2UL 1L 2UL 1L 1L 1L 1L 1L 1L
5
6 5 5 5
5
6 6 6
6 6 6 6
+ +
Fem. setae
-
Dem
Marg. setae
Don. setae
pores
Sh,Rt Sh
Sm Sm
36 36
+ +
DT DT
Sh,Rt Rt Rt Sh Sh,Rt Sh,Rt Sh,Rt Sh,Rt Sh,Tt
Sm Sm Sm Sm Sm Sm Sm Sm Sm Sm
32 34 62 64 56 32 34 34 34 32
+ + + + +
DT DT BT D DB BT DB DB DBT DBT
Sh -
Don.
Anal plate
Don. ducts
+
Spir. setae
Spir. pores
VM
ducts
VSM setae
Nd 2l2Se
5 5
+ +
3 3
+ + + + + + + + + +
3 3 3 3 3 3 3 3 3 3
3l3LS 3l3LS 3l3LS
IL
+
3/3LS 3l3LS 3l3LS 3l3Se 3l3LS 3l3LS
4
5 5 5 5
5,4 4 4 4 4
2us
-
1
Sm,Ru
36
D
Nd
5
6
2us 2us 1L 2us
-
Sh,Rt Rt Rt Rt
Sm Ru Sm Sm
34 34 34 34
D BT DT DT
lllL lllL Nd 2l2L
5 5 7 5
3 6 5 3
-
+
+ +
TABLE 1.1.3.3.2 Summary of character-su I in first-instar nymphs of subfamilies and tribes of soft scale insects (Hornoptera: Coccidae). Where: Ant. at nnae; Don. - dorsal; Fem. -femur; le - .ngth; Marg. - marginal; Segs. - segments; s i r . - spiracular; Troch. - tmhanter; and where: Rt - reticulated; Sb - shingled; Lb - lobed; Sm -smooth; Ru - rugose; Pap - papillated; D - simple disc pore; B - bilocular pore; T - trilocular pore; L long; S - short; Nd - not differentiated; LS - one long seta and one sholr seta; Se - subequal; VM ducts - ventral median ducts;
-
-
V S M setae - ventral submedian setae; (+) - present,
(-) - absent except for leg length where (+) - legs approximately 213rds body length and (-) -legs approximately 113rd body length. ~~
Taxon
Ant. Segs.
Cardiococcinae Coccinae COCCiIli PUlVinariini SaiSSetiini Eulecaniinae Fdippiinae Ceroplastinae Eriopeltinae Myzolecaniinae Pseudopulvinariinae
6 6 6 6 6 6 6 6 6 5 6
Leg le
Tmh.
Fem.
Anal
setae
setae
Plate
+
1L,2US 1L 1L 1L 1L 2UL, 1L 2US,UL 1L
+ + ,-
Rt Rt Sh,Rt Sh,Rt Sh,Rt Rt Rt
+
9-
1L lL,2UL 2us
9-
+ + +
9-
9-
7-
Derm
Marg. setae
Dors. setae
Dors. Pores
32-120 32-64 32-64 32 32-34 32-46 26-42
+,+,-
Rt Rt Rt
Ru,Pap,Sm Sm Sm Sm Sm Sm Sm Sm Sm Sm
DBT DBT DBT DBT DBT DBT DBT DT
?
Sm,Ru
36
32-34 36 32-64
+,+,-
+,+,+,-
+
+,-
DT DBT
D
Dors. Ducts
Spir. setae
Spir. Pores
VM Ducts
VSM setae
-
Nd,lllL 3I3LS,Se 313LS 3/3LS,Se 313LS 3/3Se 3I3LM 3/3Se
5,3 5,493
+
5,473 5,4,3 5,4,3 5
+ + +
6 3 3
-
-
-
+,-
-
+,-
32.1 3 6
+
Nd,2/2Se 3I3LS,Se
5,473 5 5 5 94
+ + +
2,3 1 3 3
Nd
5
-
6
7-
156
Systematics
Representatives of only two genera (Eriopeltis and Luzulaspis) were studied in the Eriopeltinae. They share most features but differ in the number and shape of spiracular setae and the fact that, in Eriopeltis, large truncate setae are present on the margin of the head. The Myzolecaniinae are characterize~ by having 5-segmented antennae, but Toumeyella sonorensis is an exception with 6-segmented antennae. Generally only one trochanter seta is present, but there are two on the species of Alecanium and Cryptostigma studied. Known species of Cryptostigma also have 62-64 marginal setae, while other representatives in the subfamily have only 32-38 marginal setae. Within the unplaced genera, Ctenochiton aztecus fits within the Cardiococcinae in that the derm is rugose, the legs are 2/3 the body length, it has two trochanter setae (as in Ceroplastodes) and six pairs of ventral submedian setae. Ctenochiton viridis has a smooth derm, no bilocular pores on the dorsum and only three pairs of ventral submedian setae. C. viridis seems to be more similar to Alichtensia orientalis in the Filippiinae than to Ctenochiton aztecus or other members of the Cardiococcinae. Paralecanopsis formicarum has five pairs of ventral submedian setae, spiracular disc-pore clusters on the venter which are septilocular, and oddly shaped marginal setae. This species does not fit in any of the current subfamilies. Parafairmairia gracilis has two trochanter setae, a smooth derm, two spiracular setae (which are subequal), three pairs of ventral submedian setae and quinquelocular disc-pores in the spiracular furrows. P. gracilb may fit within the Eriopeltinae, or possibly the Filippiinae because of its elongate body shape. It is concluded that characteristics seen in the immature stages are useful in determining relationships between and among taxa. As more immature stages are studied and their characteristics are used in conjunction with characters of the adult stages, a more sound classification system will result.
REFERENCES Ben-Dov, Y., 1969. A generic diagnosis of Bodenheimera Bodenheimer (Homoptera: Coccidae) with redescriptions of B. rachelae (Bodenheimer). Proceedings of the Royal Entomological Society of London, (B) 38: 70-74. Canard, M., 1965. Observations sur une Pulvinaire peu connue du midi de France: Eupulvinaria hydrangeae (Steinweden) (Coccoidea-Coccidae). Annales de la Soci~t~ Entomologique de France (N.S.), 1:411-419. l-lodges, G.S., 1996. A morphological and systematic study of first instar nymphs of the family Coccidae found in North America (north of Mexico). Masters thesis. Auburn University, Auburn AL. 138 pp. Hodgson, C.J., 1970. A new species of Coccus (Homoptera: Coccoidea) from Malawi. Entomologists Monthly Magazine, 106: 35-53. Hodgson, C.J., 1971. The species assigned to the genus Ceroplastodes (Homoptera: Coccoidea) in the Ethiopian Region. Journal of Entomology (B), 40: 49-61. Hodgson, C.J., 1991. A redescription of Pseudopulvinaria sikkimensis Atkinson (Homoptera, Coccoidea), with a discussion of its affinities. Journal of Natural History, 25: 1513-1529. Hodgson, C.J., 1994. The scale insect family Coccidae: an identification manual to genera. CAB International Press. Wallingford. 640 pp. Hodgson, C.J., 1995. The possible evolution of the plate-like structures associated with the anal area of Lecanoid Coccoidea. Israel Journal of Entomology, 29: 57-65. Howell, J.O. and Tippins, H.H., 1990. The immature stages. In: Rosen, D. (ed.), Armored Scale Insects, Their Biology, Natural Enemies and Control. World Crop Pests 4A. Elsevier. pp. 29-42. Lambdin, P.L. and Kosztarab, M., 1973. A revision of the seven genera related to Lecanodiaspis (Homoptera: Coccoidea: Lecanodiaspididae). Studies on the morphology and systematics of scale insects. No.5. Virginia Polytechnic Institute, Research Division Bulletin 83:1-110. Morrison, H. and Morrison, E.R., 1922. A redescription o f ht e type species of the genera of Coccidae based on the species originally described by Maskell. Proceedings of the United States National Museum. Washington, 60: 1-20. Qin, T.K. and Gullan, P.J., 1989. Cryptostigma Ferris: a coccid genus with a strikingly disjunct distribution (Homoptera: Coccidae). Systematic Entomology, 14: 221-232. Ray, C.H. and Williams, M.L., 1980. Descriptions of immature stages of Pseudophilippia quaintancii (Homoptera: Coccoidea: Coccidae). Annals of Entomological Society of America, 73: 437-447. Sheffer, B.J. and Williams, M.L., 1990. Descriptions, distribution and host-plant records of eight first instars in the genus Toumeyella (Homoptera: Coccidae). Proceedings of the Entomological Society of Washington, 92: 44-57.
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.
157
1.1.3.4. Classification of the Coccidae and Related Coccoid Families CHRIS J. HODGSON
INTRODUCTION The family group name Coccides was introduced by Fall6n in 1814 and, according to Williams (1969), the first mention of the family Coccidae was by Samouelle (1819). The first subdivisions of the Coccidae (i.e. the Coccoidea of today) were introduced by Targioni Tozzetti (1868) and Signoret (1869). Targioni Tozzetti (1868) divided the family into four 'tribes': (a) Orthezites, incorporating Orthezia and relatives, (b) Coccites, comprising mainly the mealybugs, (c) L~anites, which included a variety of scale insects including the soft-scales, and (d) Diaspidites, equivalent to the family Diaspididae of today. The Lecanites were further subdivided into seven groups, of which four are referable to present day soft-scales; the other three 'tribes' included the Kermesidae (and Physokermes), Pollinia and the Asterolecaniidae. The classification of Signoret (1869) was rather similar, dividing the Coccidae into four 'sections': (a) the Diaspides (as above), (b) the Coccides, which contained the bulk of the scale insects including the mealybugs, (c) the Brachyscelides (now the eriococcid subfamily Apiomorphinae) and (d) the Lecanides, which appears to have contained two distinct groups, (i) the I.exzaniodiaspites, which are the Asterolecaniidae and Lecanodiaspididae of today and (ii) a group which contained the soft-scales but also Aclerda and Carteria (= Kerria), now in the families Aclerdidae and Tachardiidae respectively. Much later, on the basis of male structure, Balachowsky (1942, 1948) proposed three main groups in the evolution of the Coccoidea - the margarodoid, lecanoid and diaspidoid groups. These three levels of morphological evolution in the Coccoidea have also been confirmed by studies on the chromosome (Brown, 1977) and symbiont systems (Tremblay, 1977). It is generally accepted that the margarodoid group (previously referred to as the Archeococcoidea) is the most primitive, while the rest of the superfamily are considered to be more advanced (and were placed in the Neococcoidea, and were assumed to have evolved from the Archeococcoidea). Within the more advanced group, the lecanoid group is considered to be the most primitive and to have given rise to the diaspidoid group. Exactly how the various families within each of these groups are related is still unclear (but see the phylogenetic study, Section 1.1.3.7). There have been about 10 different phylograms proposed for the Coccoidea in the last 35 or so years: Borchsenius, 1958 (based mainly on adult female characters); Boratyrlski and Davies, 1971 (based on adult male characters); Koteja, 1974b (based on the structure of the adult femzle mouthparts); Miller and Kosztarab, 1979 (a version of Boratyriski and Davies (1971) modified on the basis of more recent descriptions of males); Danzig, 1986 (using the morphology of the
Section 1.1.3.4 references, p. 198
158
Systematics adult female, adult male and crawler and also life history characters); Miller, 1984 (based on a wide range of characters), Koteja (in Kosztarab and KozAr, 1988), Miller and Miller, 1993b, 1993c (which considered the affinity of the Kermesidae and Puto in relation to a range of other taxa) and Miller and Williams, 1995 (which considered the affinity of the Micrococcidae in relation to 11 other taxa). There is broad agreement in these phylograms as to which families fall within the lecanoid group, but there is less agreement as to their relationships. Most consider that the Pseudococcidae are the most primitive and that they and the Eriococcidae and Kermesidae probably arose from a mutual ancestor (although Boratyriski and Davies (1971), on the basis of male structure, and Brown (1977) on the basis of chromosome structure, postulated that the neococcids are polyphyletic, and considered that the pseudococcids developed separately). All but Miller and Kosztarab (1979) considered the Coccidae (along with the Aclerdidae) to be the most advanceA lecanoids and many workers also consider that the Tachardiidae belong to this group. The remaining families, namely the Lgcanodiaspididae, Cerococcidae, Asterolecaniidae and Cryptococcidae, are believed to have evolved from ancestors which were extant before those from which the advanced lecaniids evolved but after the appearance of the ancestors to the Pseudococcidae, Eriococcidae and Kermesidae. Thus, there appears to be general agreement that the Aclerdidae, Asterolecaniidae, Cerococcidae, Cryptococcidae, Eriococcidae, Kermesidae, l..ex~anodiaspididae, Micrococcidae and Tachardiidae are probably the families most closely related to the Coccidae. These all belong to the lecanoid group and the adult females can be separated by the characters in Table 1.1.3.4.1 and by the keys in Balachowsky (1948), Howell and Williams (1976), Ben-Dov (1985), Danzig (1986) and Kosztarab and KozAr (1988). In addition, Tables 1.1.3.4.2 and 1.1.3.4.3 compare some of the major characters of the lst-instar nymphs and adult males of these families respectively. A brief discussion of each of these families is given below while their phylogeny is discussed further in Section 1.1.3.7.
- Flat Grass Scales The Aclerdidae are a small group, with perhaps three genera and about 50 species (McConnell, 1953, 1956; Howell, 1972; Ben-Dov, 1977). The family was introduced by Teague (1925) and, apart from the two species in Rhodesaclerda McConnell, is remarkably homogeneous and known mainly from graminaceous plants. Past workers (e.g. Femald, 1903; Balachowsky, 1942) considered the family to be close to the Coccidae based on the presence on the adult female of (i) an anal plate, (ii) an anal cleft, (iii) marginal spinose setae, (iv) tubular ducts with a stout outer ductule and a filamentous inner ductule, (v) ventral microducts with a sunken pore opening and a short broad inner ductule and (vi) a telescoping anal tube. In addition, adult female Aclerdidae (Fig. 1.1.3.4.1)are usually elongate oval as are most adult female Coccidae and the structure of their ventral microducts is similar to that of the Coccidae. The main differences between the adult females of the Aclerdidae and Coccidae are that, in the former, (i) the anal plate is only a single structure lying dorsad to the anal ring, although it is cleft in some species (and considered by Hodgson (1995) to have arisen from the anal lobes, as in the Coccidae), (ii) the posterior half of the abdomen is usually differentially sclerotised, (iii) the derm of the posterior part of the abdomen is characteristically furrowed or ridged, and (iv) the anal ring lacks wax pores. First-instar crawlers of Aclerda spp. have been described by McConnell (1953) and Howell (1973) (Fig. 1.1.3.4.2). They are characterised by the presence of (i) a distinct anal cleft (except in Rhodesaclerda), (ii) distinct anal lobes, each with a long terminal ACLERDIDAE
TABLE 1.1.3.4.1
Comparison of the character-states of some characten on the adult females of some lecanoid Coccoidea, where Acler - Aclerdidae, Aster - Asterolecaniidae, Cero - Cemoccidae, Cocc -Coccidae, Crypt - Cryptococcidae, Dact - Dactylopiidae, Erio - Eriococcidae, Kerm - Kermesidae, k a n - Lecanodiaspididae, Tach - Tachardiidae and Pseud Pseudococcidae; and where A - absent and B - present, unless otherwise stated. Data taken from Afifi (1968), Bullington & Kosztarab (1985), D e Lotto (1974), Perez Guerra & Kosztarab (1992), Hodgson (1973), Howell (1972), Howell & Kosztarab (1972), Kosztarab (1968), Lambdin & Kosztarab (1973, McConnell (1953), Miller & Miller (1993a), Munting (1965) and Williams (1985).
Acler
Aster
Cero
Cocc
Crypt
Dact
Erio
Kerm
Lecao
Form of test: B = absent, F = felted, G = glassy, PW = powdery wax, V = various
G N
G N
PW
V
F
F
F
BIPW
W
Posterior margin of abdomen emulated:
B
A
A
AIB
A
A
A
A
A
A
A
A
Dorsal setae:
A
AIB
AIB
AIB
B
B
B
B
AIB
B
A
B
Dorsal tubular ducts:
B
B
B
AB
B
B
B
A
B
A
A
AIB
Microtubular ducts:
B
A
A
AIB
B
A
B
A
A
A
A
A
Cribriform plates:
A
A
B
AIB
A
A
A
A
AIB
A
B
A
Cluster-pore plates:
A
A
A
A
B
A
A
A
A
A
B
A
Brachial plates:
A
A
A
A
A
A
A
A
A
A
B
A
Medial dorsal spine:
A
A
A
A
A
A
A
A
A
A
B
A
Anal cleft: A = absent, B = present, S= shallow
B
S
B
B
A
A
B
A
B
S
A?
AIB
Number of anal plates dorsad to anal ring:
1
0
1
2
0
0
0
0
1
(2)
(2)
0
Anal ring: A= absent; P= pores; R = sclerotized
SR
RISPR
SPR
(R)ISPR SPR
AIR
SPR
SPR
SPR
SPR
SPR
SPR
nt
Micr
Tach
Pseud
F
F
W
TABLE 1.1.3.4.1 (continued) Acler
Aster
Cero
Cocc
Crypt
Dact
Erio
Kerm
kan
Micr
Tach
Anal tube:
B
B
B
B
A
A
B
A
A
A
B
Distinct band of differentiated marginal setae:
B
A
B
B
A
A
A/B
A
B
A
A
Large bilocular (%shaped) pores:
A
B
B
A/B
A
A
A
A
B
A
A
Stigmatic spines:
A
A
A
AIB
A
A
AIB
A
B
A
A
Spiracular disc-pores: A = not in distinct bands; B = in distinct bands
A
B
B
A/B
A
A
A/B
A
B
A
A
Multilocular disc-pores:
A
A
B
A/B
A
B
A/B
A/B
A
A
A
A/B
Pregcmital disc-pores:
A
A
B
A/B
B
B
B
B
B
A
A
B
Ventral microducts: A = absent; C = coccid -type; E = eriococcid type; T = trilocular
C
E
E
C
A
A
E
A
E
E
E
T
Ventral tubular ducts:
B
A
B
A/B
B
B
B
B
B
B
A
A/B
Legs: A = well-developed; B= reduced or absent
B
B
B
A/B
B
A
A
B
B
A
A/B
A@)
A
B
B
B
B
A
B
B
A
A
B
A
A
A
A
A
T
d campanifom pores:
coxal pores: Number of ant&
segments:
Number of lab& segments:
-
Spiracles size of anterior and posterior peritreme: A = similar; B = dissimilar
Pseud
1
1
1
0-9
1 6
6-7
6-7
2-9
1-5
2-3
7-9
1-9
1
1
3
1
3
3
3
3
2
1
1
3
A
A
A
A
A
A
A
B
A
A
B
A
TABLE 1.1.3.4.2 Comparison of the character-states of some characters on 1st-instar nymphs of some lecanoid Coccoidea, where Acler - Aclerdidae, Aster - Asterolecaniidae, Cero Cerococcidae, Cocc Coccidae, Crypt - Cryptococcidae, Dact - Dactylopiidae, En0 - Eriococcidae, Kerm - Kermesidae, b a n - Lecanodiaspididae, Tach - Tachardiidae and Pseud Pseudococcidae; and where A - absent and B present, unless otherwise stated. Data taken from Baer & Kosztarab (1985), Hamon & Kosztarab (1979), Hamon et al. (1976), Howell (1973), Miller (in O’Brien, 1992), Miller et al. (1992), Perez G u e m and Kosztarab (1992) and Williams (1985).
-
-
Acler
Aster
Cero
Cocc
Crypt
Dact
Eno
Kerm
Lecan
Dorsal setae:
B
A
B
NB)
B
B
B
B
A/B
A
B
Dorsal simple pores: Dorsal eight-shaped pores: Anal lobes:
B
B
B
B
A
A
A
B
B
A
AIB
A
B
B
AIB
A
A
A
A
B
A
A
B B
A
B
B
A
A
B
B
B
A?
A?
B
B
B
B
A
B
B
B
B
B
B
B
B
A
A
B
B
B
B
B
A
B B?
B
A
A
A
AIB
A
B
B?
A
A
A
A
B
A
A
AIB
A
A
BI
A
A
A
A
A
Anal ling: Anal ling pores and setae: Median anal plate: Paired anal plates domad to anal ring: Sclerotised margia to anal cleft
Tach
Pseud
B
B
A?
A
B
A
A
Stigmatic spines:
A
A
B
B
A
A
A
A
A
A
A
Marginal setae differentiated from dorsal setae:
B
AIB
B
B
A
A
AIB
B
B
B
A
spiracular disc-pores:
B
B
B
B
B
A
A
B
B
B
A
E?
C
B
E
E
E
B
B
A
B
B
B
B
B
Ventral microdwts: B = absent; C = Coccid E = Eriococcid; P = pseudococcid (trilocular)
Tarsal campanifom pores: Tarsal digitules: A = similar; B
= dissimilar
A
B
A
A
A
A
A
Claw digitules: A = similar; B = dissimilar Claw dmticle: No. of labial segments: No. of antennal segments
B
AIB
A
A
A
A
A
A
B
B
B
B
B
B
1
1
3
3
3
2
1
5-6
6
5
6
6
6
6
Systematics
162
T A B L E 1.1.3.4.3 Comparison of the character-states of some characters on adult males of some lecanoid Coccoidea, where A c l - Aclerdidae, A s t - Asterolecaniidae, Coc -Coccidae, Dac - Dactylopiidae, E r i - Eriococcidae, K e r - Kermesidae, Lec - Lecanodiaspididae, and P s e - Pseudococcidae; and where A - absent and B - present, unless otherwise stated. Data based mainly on Koteja & Zak-Ogaza (1972) with additional information from Howell (1976), Loubser (1966) and Perez Guerra & Kosztarab (1992). Data for male Cerococcidae, Cryptoeoccidae, Tachardiidae not available; all known males of Micrococcidae are apterous.
Acl
Ast
Coc
Dac
Eri
Ker
Lec
Pse
Male p u p a r i u m : A = fluffy waxy threads; B = glassy waxy plates; C - other structure
B
C
B
A
A
A
B
A
Body: A - robust B = slender
A
A
AB
A
A
A
A
B
Fleshy setae on body:
B
A
AB
B
A
A
A
AB
Disc-pores: (other than those associated with the glandular pouch)
B
A
AB
A
A
A
A
AB
H e a d in lateral view: A = rounded; B = B = flattened dorsoventrally; C = elongated dorsoventrally
?
A
ABC
A
A
A
A
AB
Dorsomedial p a r t of epicranium: A = sclerotised; B = not sclerotised
B
B
AB
A
A
B
A
A
Postoccipital ridge:
A
B
AB
A
B
B
B
B
Vestiges of occiput:
A
B
A
A
A
B
B
A
Midcranial ridge dorsally:
A
A
A
B
B
A
A
AB
I r e - and postocular ridges: A = separated; B = fused
A
A
AB
A/B
A
A
A
AB
P r e o c u l a r ridge ventrally: A = very strong, continuous from side to side; B = weak orabsent
B
B
B
B
B
A
B
B
O c u l a r sclerite dorsally: A = sclerotised throughout; B = only sclerotised around eyes
A
B
A
A
A
B
A
A
No. of simple eyes: A = more than 2 pairs; B --- two pairs only
B
B
AB
B
B
A
B
B
M o u t h tubercle:
A?
A
A
A
AB
B
A
A
CraniaJ apophysis: A = truncate; B = furcated
?
A
AB
B
AB
B
A
A
Oceili:
B
B
A
A
A
A
B
A
O c u l a r setae:
A
A
AB
A
B
A
A
AB
Genae:
B
B
A
A
B
AB
B
B
Genal setae:
A
A
AB
B
B
A
A
B
3 r d antennal segment: A = longest srgment; B -- shorter than another segment
A?
?
B
A
A
A
?
A
9th antenna i segment: A = barrel-shaped; B = cylindrical
B
B
B
A
A
A
B
B
10th antennal segment: A = barrel-shaped" B = cylindrical; C = apically constricted
B
?
BC
C
C
A
B
C
M e m b r a n o u s a r e a on scutum: A = absent or very narrow; B = as wide as prescutum
B
B
B
A
A
B
B
A
Mesepimeron:
B
A
AB
B
B
A
B
B
Median ridge of b a s i s t e m u m :
B
A
AB
A
A
A
B
A
M e t a s t e r n a l apophysis:
A
A
A
B
B
B
A
B
A = unsclerotised B = sclerotised
163
Classification of the Coccidae and related families T A B L E 1.1.3.4.3 (continued)
Acl
Ast
Coc
Dac
Eri
Ker
Lec
Pse
M e t a s t e r n a l plate: A = large; B = vestigial
B
A
AB
B
B
A
A
B
Scutellar setae:
A
A
AB
B
B
B
B
A
M e t a s t e r n a l setae:
A
A
AB
B
B
B
B
B
Hamulahalterae:
A
A
AB
A
B
B
B
B
Tar sus: A = 2-segmented; B = 1-segmented
B
B
B
B
A
A
B
A
Apical spurs on tibia: A = 2; B = 1 only; C - absent or not differentiated
B
C
B
?
A
A
B?
A
T r o c h a n t e r a n d f e m u r fused:
A
A
A
A
A
A
B
A
Tergites on abdominal segments II-VII: A = large plates on all segement; B = absent or weak
B
AB
B
B
A
B
B
Sternites on abdominal segments II-VII: A = large plates on all segement; B = only on some or absent
A
AB
B
B
A
B
B
Pleurites on abdominal segments IV-VII:
A
AB
A
A
B
B
A
8th abdominal sternite: A = large plate; B = 2 small plates or absent
B?
A
A
A
B
A
A
B
8th abdominal sternite: A = with strong lateral ridges and anterior transverse ridge; B = weak or absent
A?
B
B
B
B
AB
B
B
Ventral setae on abdomen: A = more numerous B than dorsal setae; B = subequal or fewer
A
A
B
B
A
A
B
G l a n d u l a r pouch or plate:
A
AB
B
B
BB
A
B
Ratio width to length of penial sheath: A = thick (1:3 or less); B = slender (1:4 or more)
A
B
B
A
A
B
B
A
Style of penial sheath: A = subequal or shorter than basal capsule; B = much longer
B
B
B
A
A
B
B
A
Tergite IX & X: A = represented by a separate plate; B = fused with genital capsule
B
B
B
B
B
B
B
A
Aedeagus: A = arising immediately behind basal ridges of genital capsule; B = arising at a B great distance
B
B
A
B
B
B
A
Aedeagus: A = subsequal to or longer than style; B = shorter than style
A
B
A
A
A
A
A
B
B
A
A
B
B
A
B?
Aedeagus in lateral view: A = curved; B = straight Anal opening: A = opens backwards, slit-like; B = rounded, well defined, opening upwards; C = indistinct, opening upwards
B?
C
C
?
B
C
C
A
Dorsal setae on genital capsule on each side: A = more than 2 ; B = 2 ; C = I ' D = 0
D
C
D
A
B
C
D
A
Ventral setae on genital capsule on each side: A = more than 1; B = 1; C = 0 setae
A
B
C
A
A
A
C
A
Section 1.1.3.4 references, p. 198
,
Fig. 1.1.3.4.1. Aderdidae. Aclcrah McConnell, 1953).
subterruneu Signoret,
adult female.
(From
1,
7
*
,
,' /
Fig. 1.1.3.4.2 Aclerdidae. Aclerah fillmrdriae Howell, crawler. (From Howell, 1973).
165
Classi.[icatien of the Coccidae and relatedfamilies
seta and a sclerotised projection on the inner margin, (iii) each anal lobe with a group of spinose setae dorsally, (iv) a distinct band of spinose marginal setae, (v) an anal ring with a pair of pores and some very short stubby setae, (vi) a submarginal band of sunken ventral microducts not unlike those in the Coccidae, (vii) a 1-segmented labium and (viii) absence of any anal plate sclerotisations. Koteja (1974a) apparently did not study the Aclerdidae for the presence of a campaniform pore on the tarsus. However, tarsal campaniform pores are absent (Hodgson, unpublished data), a character-state otherwise almost restricted to the Micrococcidae and Coccidae. The males of Aclerdidae have been described by Howell (1976) and Nada et al. (1976). In a comparison of the presence or absence of seven or eight male characters in the Aclerdidae, Coccidae, Asterolecaniidae and Lecanodiaspididae, Howell (1976)concluded that the Aclerdidae (on the basis o f Aclerda tillandsiae Howell (Fig. 1.1.3.4.3)) shared more characters with the Asterolecaniidae than with the Coccidae and Lecanodiaspididae. The males of A. tiUandsiae differ from those of the Asterolecaniidae in the presence of (i) a well-differentiated apical spur on the tibia and (ii) a distinct preoral ridge. The males of these three families can be separated from male Coccidae by the absence of ocelli and the lack of sclerotisation of the gena. In addition, the Lecanodiaspididae are separable by the presence of fused trochanter and femur.
de-
"/--~.
,-"
Pf ....
leg-,'
"_~po
"
~ -'
.pit
P"
eps,
._pi
~J
r
J~-
~
--mpv
/
-pc
--
I
-,~-~
I
-
-
_. .... I
- - pns . . . . . . . . . . . . . . . . . te ....
Fig. 1.1.3.4.3. Aclerdidae. Aclerda tiUandsiae Howell, adult male. (From Howell, 1976). The Aclerdidae are generally considered to be a sister group to the Coccidae and this was confirmed by the phylogenetic study of Miller and Williams (1995) when they concluded that the Aclerdidae, Micrococcidae and Coccidae formed a well-defined group (see also Section 1.1.3.7).
Section 1.1.3.4 references, p. 198
Fig. 1.1.3.4.4. Asterolecaniidae. Astemlecuniwn profeue Giliomee & Munting, adult female. (From Giliomee & Muting, 1968).
Fig. 1.1.3.4.5- Asterokaniidae. Asrerdecmium profeue Giliomee & Muting,crawler. (From Giliomee & Muting,1968).
167
Classification of the Coccidae and related families
A S T E R O L E C A N I I D A E - Pit Scales The composition of the family Asterolecaniidae is ill-def'med even without the Le,canodiaspididae and Cerococcidae, which it used to include. The Asterolecaniidae are sometimes considered to be close to the diaspidoid group (Ben-Dov, 1990) due to the reduced state of some structures on the adult female, namely the one-segmented antennae, absence of legs, morphology of the mouthparts and the presence of a detachable glassy test over the dorsum of the female. However, Giliomee (1968), after studying the males of some Asterolecaniidae, considered this family closer to the lecanoid line but more specialised, exhibiting little resemblance to the specialised diaspidoids. More recently, Miller and Williams included this group in their phylogenetic analysis of the relationships of the Micrococcidae and concluded that the Asterolecaniidae, Cerococcidae and Lecanodiaspididae formed a discrete group and were probably a sister group to another group formed by the Coccidae, Aclerdidae, Micrococcidae and Tachardiidae.
r
",..U~]
":"i
~ H
q /
CO~'G ABHJ.
.Icx:~ - ~r~O~
Fig. 1.1.3.4.6. Asterolecaniidae. Asterolecanium proteae Giliomee& Munting, adult male. (FromGiliomee & Munting, 1968). Important characters of adult female Asterolecaniidae (Fig. 1.1.3.4.4) are the presence of (i) eight-shaped pores, frequently in a continuous row around the ventral margin but also often present dorsally, (ii) a row of quinquelocular disc-pores just mesad to the band of eight-shaped pores, (iii) small to minute anal lobes, although these are often absent, (iv) antennae represented by small, one segmented tubercles with few setae, (v) bands of stigmatic quinquelocular disc-pores between the spiracle and margin, the posterior bands not branched, (vi) distinctive dorsal tubular ducts, without a cup-shaped invagination, but sharply bent at the inner end of the outer ductule and without a
Section 1.1.3.4 references, p. 198
168
Systematics
filamentous inner ductule, (vii) an anal ring at the end of a short anal tube, which is either simple, without pores or setae, or has pores and setae; and the absence of (viii) an anal cleft, (ix) eribriform plates, (x) ventral microducts (although a few are occasionally present on either side of labium and are similar to those in the Eriococcidae rather than the Coccidae), and (xi) stigmatic spines. In addition, the dorsum is usually covered by a glassy test. This family differs from the closely related ~ o d i a s p i d i d a e and Cerococcidae in the structure of the tubular ducts, absence of any form of anal plate and the fact that the Asterolecaniidae do not secrete honeydew. The main features of lst-instar crawlers (Fig. 1.1.3.4.5) are the absence of (i) dorsal setae and stigmatic spines, and (ii) anal plates, and the presence of (iii) a one-segmented labium, (iv) a very shallow anal cleft, (v) anal lobes absent or very poorly developed, (vi) ventral microducts of the eriococcid type, and (vii) presence of eight-shaped pores dorsally. The male of Asterolecanium proteae Giliomee and Munting was studied by Giliomee (1968) (Fig. 1.1.3.4.6) who concluded that the Asterolecaniidae were more specialised than the Coccidae and Lecanodiaspididae, but that it was unlikely that they and the Diaspididae had a common asterolecaniid-like ancestor. Later, as part of their study of the male of Kermes quercus (L.), Koteja and Zak-Ogaza (1972) compared the Kermesidae with the Asterolecaniidae, Pseudococcidae, Eriococcidae, Coccidae and Lecanodiaspididae and concluded that the Asterolecaniidae were closest to the Lecanodiaspididae when all shared characters were included in the analysis, but were not very close to any other family when only primitive characters were used.
- Ornate Pit Scales. The taxa currently placed in the Cerococcidae were originally included in the Asterole~aniidae but Koteja (1974b) placed them in a separate family based on his study of the labium. This interpretation was confirmed by Lambdin and Kosztarab (1977) when they revised the group baseA on the adult females of most of the known world species, then numbering 55 ~ i e s in three genera. They conducted an Hennigian-type study on the major characters of the adult females and compared these with those found in the Eriococcidae, Asterole~aniidae and Lecanodiaspididae. They concluded that the family Cerococcidae was least close to the Eriococcidae but was about equally close to the other two families. More recently, Miller and Williams included this group in their phylogenetic analysis of the relationships of the Micrococcidae and concluded that the Cerococcidae, Lcganodiaspididae and Asterolecaniidae formed a discrete group, which was probably a sister group to a clade formed by the Coccidae, Aclerdidae, Micrococcidae and Tachardiidae. It is likely that the Cerococcidae are not very close to the Coccidae for, although they share (i) anal plates, (ii) an anal cleft, (iii) tubular ducts with a stout outer ductule and a filamentous inner ductule, and (iv) a telescoping anal tube, they differ in numerous characters. Thus, the main features of the adult female Cerococcidae (Fig. 1.1.3.4.7) are (after Lambdin and Kosztarab, 1977) (i) a pyriform body, (ii) prominent anal lobes with stout apical setae and short fleshy or spine-like setae on the dorsal and ventral surfaces, each lobe sclerotised on its inner margin, (iii) a single dorsal anal plate (not homologous to the paired anal plates of the Coccidae according to Hodgson (1995a)), (iv) eight-shaped pores irregularly or evenly spaced in a swirl or lacelike pattern on dorsum, (iv) venter distinguished by numerous bilocular pores [microducts] on the cephalothoracic region (which are not sunken as in the Coccidae), (v) posterior spiracular furrows, bifid on several species, (vi) short, unsegmented antennae, with a cluster of disc-pores at their base, (vii) legs, when present, unsegmented and (viii) most species with segmental transverse rows of multilocular disc-pores and eight-shaped pores on the venter of the abdomen. Some of these features are shared by a very few Coccidae but, taken as a group, clearly separate the Cerococcidae from the Coccidae. CEROCOCCIDAE
Fig. 1.1.3.4.7. Cenmccidae. Cerococcus quercur Cornstock, adult female. (From Lambdin & Kosztarab, 1977).
Fig. 1.1.3.4.8. Cerococcidae. Cerococcus quercus Comstock, crawler. (From Hamon & Kmtarab, 1979).
170
Systematics
The crawlers of many species of Cerococcus were described by Hamon and Kosztarab (1979) (Fig. 1.1.3.4.8) and these appear to differ from those of the Coccidae mainly in (i) the structure of the ventral microducts (similar to the adults and of the eriococcidtype), (ii) in having a three-segmented labium, (iii) in the presence of the rows of eight-shaped pores on the dorsum (only known in the Coccidae in the genera Mallococcus Maskell and Bodenheimera Bodenheimer) and (iv) in the presence of a welldeveloped sclerotised plate dorsad to the anal ring. In addition, both the crawlers and adult females have tarsal campaniform pores (Koteja, 1974a), unknown in the Coccidae. No males of Cerococcidae have been described (however, for some characters see the matrix in Section 1.1.3.7). The endosymbionts of Cerococcidae are of the asterolecaniid-type (Buclmer, 1965).
CRYIrI'OCOCCIDAE - Bark-crevice Scales. The genera Cryptococcus Douglas and Kuwanina Cockerell were placed into a distinct family, the Cryptococcidae, by Kosztarab (1968) although this has not been recognised by such workers as Williams (1985), Danzig (1986) and Miller and Miller (1993a), who still include these genera in the Eriococcidae. It is a small family with six known species in two genera. The adult females of the Cryptococcidae (Fig. 1.1.3.4.9) are characterised by (i) an almost circular body, (ii) legs either completely absent or reduced to unsegmented stubs, (iii) antennae reduced to one to five segments, (iv)a threesegmented labium, (v) a pair of structures present just posterior to the posterior spiracle (referred to as oval cluster pore plates by Kosztarab (1968) and metathoracic leg flaps by Williams (1985)), (vi) a heavily sclerotised anal ring, generally without pores but usually with four to six short setae, (vii) the absence of anal lobes, (viii) the presence of tubular ducts, with a broad outer ductule and a filamentous inner ductule, in a sparse submarginal ring ventrally and scattered throughout dorsally, and (ix) by the presence of a white waxy test. Adult females of this family are restricted to bark crevices. First-instar crawlers (Fig. 1.1.3.4.10) have the following characters (i) short, three to five segmented antennae (all other families appear to have six-segmented antennae), (ii) legs rather thick, with a relatively short tibia and tarsus, (iii) claw without a denticle, (iv) ventral microducts absent, (iv) a campaniform pore on each tarsus (Koteja, 1974a), (v) anal lobes poorly developed, (vi) anal ring without well-defined pores and setae, (vii) absence of marginal and stigmatic spines, and (viii) presence of quinquelocular disc-pores dorsally. No males of this family are known. Kosztarab (1968) considered the Cryptococcidae to be most closely related to the Eriococcidae and Kermesidae. Koteja (1974b) agreed but considered that Kuwanina might form a separate group. As indicated above, some workers (Williams, 1985; Danzig, 1986; Miller and Miller, 1993a) still include these two genera in the Eriococcidae. A study of the endosymbionts of Cryptococcus showed that they were of the eriococcid-type (Walczuch, 1932).
DACTYLOPI[DAE - Cochineal Scales. This small family includes only the genus Dactylopius O. Costa which contains nine species, all restricted to the Cactaceae. Originally more genera were included in this family (e.g., Ferris, 1955) but these have since been transferred to other families, mainly the Eriococcidae and Kermesidae. The family has been revised by De Lotto (1974) and Perez Guerra and Kosztarab (1992). The main characters of the adult females (Fig. 1.1.3.4.11) are the presence of (i) thick truncate dorsal setae, often with sharply broadened bases, (ii) clusters of broad-rimmed quinquelocular disc-pores on the dorsum, generally with an associated tubular duct, (iii) the anal opening appearing as a transverse slit, (iv) short legs, (v) antennae reducexl to six to seven segments,
_-
._
Fig. 1.1.3.4.9. Cryptococcidae. Crypiococcus fa&ugu Lindinger, adult female. (From Williams, 1985).
Fig. 1.1.3.4.10. Crypococddae. Williams, 1985).
Cryplococcus fagisugu
Lindinger, crawler. (From
Fig. 1.1.3.4.11. Dactylopiidac. Dclclyropius coccus Cash, adult female. (From Perez Guerra and Koszhrab,l!XQ).
Fig. 1.1.3.4.12. Dactylopiidae. Doctylopius coccus Costa, crawler. (From Perez Guerra & Kosztarab, 1992).
173
Classification of the Coccidae and related families
(v) a three-segmented labium, (vi) tubular ducts with a broad outer ductule and a fairly broad inner ductule, and (vii) absence of dorsal and ventral microducts. Based on adult female characters, most workers have considered the Dactylopiidae to be close to the Eriococcidae and possibly also to the Kermesidae. First-instar crawlers (Fig. 1.1.3.4.12) were studied by Perez Guerra and Kosztarab (1992) who showed that the main characters were (i) truncate dorsal setae present marginally and in three longitudinal lines, (ii) legs well developed, (iii) antennae well developed, with six segments, (iv) small groups of quinquelocular disc-pores present submarginally near the truncate dorsal setae, (v) ventral microducts apparently absent, (vi) anal lobes absent, (vii) long setae normally associated with anal lobes also absent, and (viii) anal opening present as a transverse slit. In addition, Koteja (1974a) showed that a campaniform pore was present on each tarsus. The male of D. coccus Costa was briefly described by Perez Guerra and Kosztarab (1992) (Fig. 1.1.3.4.13). Loubser (1966) had previously described two species and had concluded that the males of the Dactylopiidae were (i) closest to the Eriococcidae, (ii) more closely related to the Coccidae than to the Pseudococcidae, and (iii) that they were only distantly related to the Kermesidae. Boratyrlski and Davies (1971) considered that the Dactylopiidae and Eriococcidae were both derived from the Pseudococcidae. No symbionts are known from the dactylopiids and these cannot therefore be used to indicate relationships (Tremblay, 1977). : ~
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Section 1.1.3.4 references, p. 198
Fig. 1.1.3.4.14. E r i m i d a e . Eriococcus bmi (Fonscolombe), adult female. (From Williams, 1985).
Fig. 1.1.3.4.15. Eriococcidae. Acmlococcut droseroe Miller, Liu 8r Howell, crawler.
(From Miller et al., 1992).
175
Classification of the Coccidae and related families
to define due to the diversity of its morphological characteristics; indeed Cox and Williams (1986) considered this family to be paraphyletic. The main characters of the adult females (Fig. 1.1.3.4.14) are the presence of (i) well-developed legs in most species, the coxae often with translucent pores, (ii) antennae usually five to seven segmented, located near the body margin, (iii) a three-segmented labium, (iv) tubular ducts (sometimes referred to as macrotubular ducts), with a broad outer ductule, filamentous inner ductule and a cup-shaped invagination, (v) microtubular ducts (otherwise only known in the Cyphococcinae (see below) in the Coccidae), (vi) ventral microducts not sunken (frequently even slightly convex) and often appearing bilocular (here referred to as the eriococcid-type), (vii) dorsal and marginal setae often conspicuously spiniform, (viii) an anal ring which is rarely reduced but is normally sclerotised, with pores and six to eight setae, (ix) and anal lobes usually present and well developed with a long terminal spine; also the (x) absence of diagnostic pseudococcid characters such as ostioles, cerarii, circuli and trilocular pores, and (xi) adult females partially or completely enclosed in a dense, felted test. On the basis of female characters, most authors have placed the Eriococcidae close to the Pseudococcidae, Kermesidae and Dactylopiidae. One of the main differences between almost all adult females of the Eriococcidae and the Coccidae is the absence of paired anal plates in the former and their (almost) constant presence in the latter. However, in some species of Eriococcidae the anal lobes do become sclerotised (see Miller and Gonz~lez, 1975) and these have moved anteriorly in Eriochiton Maskell, in which they form two distinct anal plates that cover the anal opening, as in the Coccidae (Hodgson, 1995a). dhS
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Section 1.1.3.4 references, p. 198
176
Systematics
The first-instar crawlers (Fig. 1.1.3.4.15) are characterised by the presence of (i) welldeveloped anal lobes each with a long apical seta, (ii) a well-developed anal ring with pores and setae, (iii) marginal setae generally present and spinose but stigmatic spines absent, (iii) anal plates almost invariably absent, (iv) a three-segmented labium present, (v) presence of ventral microducts of the eriococcid-type, and (vi) presence of tarsal campaniform pores (Koteja, 1974a). Adult males (Fig. 1.1.3.4.16) have been described by Afifi (1968) and Miller and Gonz~lez (1975). On the basis of the information available to him, Afifi (1968) considered that the Eriococcidae shared more characters with the Pseudococcidae than with the Coccidae. Koteja and Zak-Ogaza (1972), when describing the male of Kermes quercus, compared the males of a number of families including the Eriococcidae and Pseudococcidae and considered, on the basis of all shared characters, that the Eriococcidae were closest to the Pseudococcidae but, when only primitive characters were considered, suggested that the Eriococcidae were closest to the Kermesidae. Boratytiski and Davies (1971) considered that the Eriococcidae were derived from the Pseudococcidae along a different, divergent line to that which gave rise to the other lecanoid groups.
KERMESIDAE - Gall-like Scales. The Kermesidae are considered to include about 70 species in 9 genera, but the status and relationships of some of these genera are doubtful. The genus Kermes has recently been revised by Bullington and Kosztarab (1985), although some new species have been added from China by Hu Xingping (1987). The main characters of the adult females of this family (Fig. 1.1.3.4.17) are (i) pores which appear to be eight-shaped but which are quite different in structule to those of the I.ex~anodiaspididae, Cerococcidae and Asterolecaniidae and which were referred to as 'spinescent eight-shaped pores' by Bullington and Kosztarab (1985), (ii) the extension of the dorsal derm ventrally to form a false venter, (iii) presence of two sizes of tubular duct, i.e. large (macrotubular) ducts, with a broad outer ductule and a filamentous inner ductule, which form a marginal band of large ducts on the dorsum, and small (microtubular) ducts (quite different in structure to the microtubular ducts of the Eriococcidae) which are smaller and present throughout the dorsum, (iv) presence of a three-segmented labium with 12-14 setae, (v) absence of a spiracular band ofquinquelocular disc-pores, (vi) absence of stigmatic spines, (vii) anal ring present or absent, when present with many pores and three pairs of setae, (viii) absence of ventral microducts, and (ix) generally with a group of multilocular disc-pores near the base of each antenna. Recently, Miller and Miller (1993b) transferred three species previously included in the Eriococcidae to a new genus, Eriokermes, which they placed in the Kermesidae. First-instar crawlers (Fig. 1.1.3.4.18)were described by Baer and Kosztarab (1985) and Hu Xingping (1987) and are characterised by the presence of (i) a three-segmented labium, (ii)anal lobes which are partially or wholly sclerotised, (iii)antennal segment I with two setae, (iv) a trilocular pore near the base of each antenna, (v) ventral microducts of the eriococcid-type, and (vi) the absence of stigmatic spines. In addition, Koteja (1974a) showed that there was a campaniform pore on each tarsus. The male of Kermes quercus (L.) was studied in detail by Koteja and Zak-Ogaza (1972) (Fig. 1.1.3.4.19) and are also illustrated by Hu Xingping (1987). Koteja and Zak-Ogaza considered that this species has three unique characters - (i) a very strong preocular ridge ventrally, which is continuous from side to side, (ii) the reinforcement of the VIIIth abdominal stemite by two strong longitudinal ridges and with another
\ 4
a
1
Fig. 1.1.3.4.17. Kermesidae. Aflokenneskingi (Cockerell), adult female. (From Hamon et
al., 1976).
Fig. 1.1.3.4.18. Kermesidae. Affu&ermesking; (Cockerell), crawler. (From Hamon er
al., 1985).
Systematics
178
transverse ridge anteriorly (these ridges articulate with the genital capsule) and (iii) a barrel-shaped 10th antennal segment. However, neither Hu Xingping (1987) nor Hamon et al. (1976), who studied Kermes kingi Cockerell, noted the first two (most distinctive) features. Koteja and Zak-Ogaza (1972) also analyzed the phylogenetic relationships of the Kermesidae along with five other lecanoid families. They concluded that the Pseudococcidae and Eriococcidae were the two most primitive families and that the Coccidae, Lecanodiaspididae and Asterolecaniidae were the most advanced, with the Kermesidae in between. However, they concluded that the Kermesidae probably evolved from the Eriococcidae at an early stage. Giliomee (1968), using data from Borchsenius (1960) for the Kermesidae, had concluded that the Kermesidae were closest to the Coccidae and ~ o d i a s p i d i d a e . More recently, Miller and Miller (1993b, 1993c) did two cladistic studies, one (1993b) including the Pseudococcidae, Eriococcidae, Kermesidae and Coccidae which suggested that the Kermesidae were closest to the Coccidae and the Eriococcidae to the Pseudococcidae, while the other (1993c), which included the Kermesidae, Eriococcidae, Phenacoleachiidae and Pseudococcidae, suggested that the family Eriococcidae was closer to the Kermesidae than to the Pseudococcidae. The phylogenetic analysis of Miller and Williams (1995) also concludes that the Kermesidae and Eriococcidae are closely related. No symbionts are known from the kermesids and therefore they cannot be used to indicate relationships (Tremblay, 1977).
- Ornate Pit Scales. The ~ o d i a s p i d i d a e include 10 genera (Williams and Watson, 1990) and about 80 species and is mainly tropical but with a few species in temperate regions. It has been revised by Howell and Kosztarab (1972), Hodgson (1973), Lambdm and Kosztarab (1973), Lambdin et al. (1973) and Howell et al. (1973). The genus Mallococcus Maskell, previously included in this family, is now considered to belong to the Coccidae (Lambdin and Kosztarab, 1973; Hodgson, 1994a). The main characters of the adult female Lecanodiaspididae (Fig. 1.1.3.4.20) are the presence of (i) a 'bow-tie'- or 'butterfly'-shaped anal plate which is triangular laterally and which lies ventral to the anal opening, (ii) a narrow, arched plate which lies dorsal to and appears to partly surround the anal opening and which is sometimes fused with the ventral plate, forming a complete sclerotised ring around the anal opening, (iii) an invaginated anal ring, usually with pores and 6-18 setae, (iv) cribriform plates on the dorsum, (v) generally well-developed antennae of six to nine segments, (vi) legs rather variable in size, and (vii) posterior bands of spiracular disc-pores often divided. This family is generally considered to be close to the Cerococcidae and both families used to be included in the Asterolecaniidae. However, Borchsenius (1959) removed it from the latter and raised it to family rank. It is rather similar in general appearance to the Cerococcidae but, in the Lecanodiaspididae, (i) the anal lobes are rounded (or even absent in some genera (e.g., Anomalococcus Green)) and lack a long apical seta, (ii) the medial anal plate lying over the anal ring is much wider than long, while (iii) there is also a ventral plate lying along the ano-genital fold ventrally, (iv) there are no groups of multilocular disc-pores at the base of each antenna, (v) bands of eight-shaped pores are absent across the abdomen ventrally and (vi) the labium is one- or two-segmented rather than three-segmented as in the Cerococcidae. The l.,ecanodiaspididae are generally considered to be close to the Coccidae with which the adult females share the following characters: presence of (i) anal clefts, (ii) reduced
LECANODIASPIDIDAE
\
Fig. 1.1.3.4.19. Kermesidae. K e r n s quercus (L.),adult male. (From Koteja O p , 1972).
Fig. 1.1.3.4.20. Lecanodiaspdidae. LecModiaspiS mimasne (Maskell), adult female. (From Hodgson, 1973).
Fig. 1.1.3.4.21. Lecancdiaspididae. L e c ~ o d i a r p i rmimosue (Maskell), crawler. (From Williams & Kosztarab, 1970).
Fig. 1.1.3.4.22. Lecanodiaspididae. LecModiapis elytropqpi Muting & Giliomee, adult male. (From Muting & Giliomee, 1%7).
Classification of the Coccidae and relatedfamilies
181
anal lobes, (iii) anal plates, (iv) labium with one or two segments, (v) stigmatic spines in the type genus, (vi) marginal setae in some species, (vii) anal ring with pores and long setae, (viii) well-developed antennae, and (ix) the form of the tubular ducts. The Lecanodiaspididae differ from the Coccidae in (i) the form of the ventral microducts which are of the eriococcid-type, (ii) the form of the anal plates, (iii) the presence of eight-shaped pores (otherwise only known in the genera Mallococcus and Bodenheimera in the Coccidae and in the Asterolecaniidae and Cerococcidae), (iv) the form of the cribriform plates and (v) the presence of a campaniform pore on each tarsus (Koteja, 1974a). The lst-instar crawlers (Fig. 1.1.3.4.21) are characterised by the presence of (i) welldeveloped anal lobes, each with a long apical seta, (ii) margin of dorsum with a row of eight-shaped pores and with two partial rows medially (the former are absent in the crawlers of Bodenheimera), (iii) margin with marginal setae and frequently with stigmatic spines, (iv) a one-segmented labium, and (v) a median sclerotised plate dorsad to the anal ring and with a further pair of sclerotised plates, one on either side of the anal cleft. Males of five Lecanodiaspis species (Fig. 1.1.3.4.22) have been described by Munting and Giliomee (1967), Afifi and Kosztarab (1969) and Amin et al. (1976). The one exclusive character that these five species share is the complete fusion of the trochanter and femur to form a trochantofemur (otherwise only known in Newsteadia floccosa De Geer (Ortheziidae) (Koteja, 1986)). Giliomee (1967) investigated the relationships of the male of L. elytropappi Munting and Giliomee and concluded that the family Lecanodiaspididae was more closely related to the Coccidae than to the Pseudococcidae. Koteja and Zak-Ogaza (1972) considered that the Lecanodiaspididae was closest to the Coccidae and Asterolecaniidae when all characters were considered, but that it shared more primitive characters with the Pseudococcidae, Eriococcidae and Kermesidae than with the former two families. The phylogenetic analysis of Miller and Williams (1995) concluded that the Lecanodiaspididae, Cerococcidae and Asterolecaniidae formed a discrete group which may represent the sister-group to those families nearest the Coccidae. Studies on the endosymbionts of the lecanodiaspids have shown that they are of the asterolecaniid-type (Walczuch, 1932; Buchner, 1965).
MICROCOCCmAE This family has been recently revised (Marotta et al., 1995; Miller and Williams, 1995). It contains two genera, Micrococcus with seven species known only from the Mediterranean region and Molluscococcus which is monospecific and only known from Zimbabwe. All appear to be hypogeic and appear to be restricted to the crowns and rootlets of grasses or have been collected from ant's nests. Because of its unusual combination of characters, it had previously been placed in the Eriococcidae (Ferris, 1957), Coccidae (Balachowsky, 1942b)and Pseudococcidae (Silvestri, 1939), but was raised to family status by Koteja (1974). This status was accepted by both Marotta et al. (1995) and Miller and Williams (1995). The main characters of the adult females (Fig. 1.1.3.4.23) are: (i) antennae with fewer than four segments, (ii) a I-segmented labium, with five pairs of setae, (iii) well-developed legs, without translucent pores, (iv) tarsal campaniform pore absent, (v) anal ring well developed with numerous setae and pores, (vi) vulva situated on segment VI, (vii) spiracles with numerous spiracular disc-pores in peritreme, (viii) ventral microducts of the eriococcid-type, (ix) tubular ducts ventrally, (x) closed simple pores (discoidal pores) with an usually thick rim, (xi) anal ring without an invaginated anal tube, and (xii) anal lobes modified into two anal plates placed laterally to the anal ring.
Section 1.1.3.4 references, p. 198
Fig. 1.1.3.4.23. Micmcmcidae. Micrococcus syluestrii Leonardi, adult female. (From h4arotta et al., 1995).
Fig. 1.1.3.4.24. Micromccidae. (Miller and Williams, 1995).
Mkrococcur bodenheimori Bytinski-Sah, crawler.
Classification of the Coccidae and relatedfamilies
183
The lst-instar nymphs (Fig. 1.1.3.4.24) have: (i) anal lobes sclerotised, forming anal plates in later instars, (ii) antennae five-segmented, (iii) ventral microducts absent, (iv) multilocular disc-pores without central loculus, (iv) microtubular ducts present on venter of abdomen, with conspicuous dermal orifice, (v) legs without tarsal campaniform pores, and (vi) one tarsal digitule on front legs filamentous, the other normal. All known males (Fig. 1.1.3.4.25) are apterous, without any constrictions marking head, thorax and abdomen and with non-functional mouthparts and are basically neotenic like the adult female but with a well-developed, broad penial sheath. Miller and Williams (1995) made a phylogenetic study based on 38 characters and concluded that the Micrococcidae were most closely related to the Aclerdidae, and also that the Micrococcidae, Aclerdidae, Coccidae and Tachardiidae formed a well-def'med clade.
TACHARDIIDAE - The Lac insects. This family has been known in the past as the Kerriidae and the Lacciferidae. It is widely distributed throughout most of the tropics and subtropics and contains about eight genera and approximately 60 species. The adult females of this group for the world were revised by Chamberlin (1923, 1925), whilst those from South Africa were studied by Munting (1965, 1966). Recently, Zhang (1993) has described some new species from China. The main characters of adult female Tachardiidae (Fig. 1.1.3.4.26) are (i) the reduction of the legs to small tubercles, (ii) the enlargement of the anterior spiracles in comparison with the normal-sizeA posterior spiracles, (iii) the presence of a pair of pore-bearing plates (called brachial plates) on the dorsum of the thorax, which may or may not be borne on a pair of fleshy processes, (iv) an anal opening borne on the apex of an anal tubercle, which is a prolongation of the posterior end of the abdomen, (v) an anal ring with pores and long setae, (vi) the dorsum usually with a median, sclerotised, dorsal spine with an apical pore and (vii) the presence of a test of lac resin or shellac. The lst-instar crawlers have been illustrated by Miller (in O'Brien et al., 1991) and that of Tachardiafici Green is illustrated here (Fig. 1.1.3.4.27). It is clear that, if this species is typical of the family, there are a number of distinctive characters separating them from the crawlers of other lecanoid families. In particular (i) the anal ring is especially well developed and heavily sclerotised and has an additional outer sclerotised ring which bears the long setae generally found on the anal lobes, (ii) associated with the anterior spiracle is a group of quinquelocular pores on the dorsum, each group in a sclerotised area surrounded by a partial ring of setae, (iii) antennae with three very long setae on segment V and two spinose terminal setae on segment VI, (iv) presence of sunken duct-like pores around the margin, and (v) presence of a campaniform pore on each tarsus. None of these characters are similar to those in the first-instar of other families and, as indicated by Williams and Watson (1990), this family is difficult to place phylogenetically. The males have not been described (but some characters are given in the matrix in Section 1.1.3.7). The Tachardiidae were included in a recent phylogenetic study by Miller and Williams (1995), who considered that it was the sister-group to a clade formed by the Micrococcidae, Aclerdidae and Coccidae. However, confusingly, Walczuch (1932) and Buchner (1965) have shown that the endosymbionts of the Tachardiidae can be divided into two groups, one with a unique type of symbiont and the other with an eriococcid-type.
Section 1.1.3.4 references, p. 198
Fig. 1.1.3.4.25. Miuococcidae. Micrococcus bodenheimeri Bytinski-Salz, adult male. (Miller and Williams, 1995).
Fig. 1.1.3.4.26. Tachardiidae. Tachardiu ufluens Brain, adult female. (From Muting,
1%5).
Classification of the Coccidae and related families
185
COCCIDAE - The Soft Scales The family Coccidae is the third largest family within the Coccoidea, with approximately 1100 species in about 160 genera (Ben-Dov, 1993; Hodgson, 1994a). A typical adult female soft scale is characterised by the presence of: (i) a pair of more or less triangular anal plates (except in Physokermes), (ii) a deep anal cleft, (iii) sunken ventral microducts, (iv) an eversible anal tube to assist in honeydew elimination, (v) an anal ring composed of two sclerotised crescents, each with setae and pores, (vi) eyespots which, even when lying in the line of the marginal spines, appear to be slightly displaced onto the dorsum, (vii) a one-segmented labium, (viii) marginal setae, (ix) stigmatic spines (although sometimes absent), (x) pregenital multilocular disc-pores on the venter of the abdomen, (xi) a band of spiracular disc-pores between the margin and each spiracle, (xii) ventral tubular ducts, frequently present in a submarginal band, (xiii) legs and antennae usually well developed, and (xiv) only three setae on scape. Also in the absence of (xv) a campaniform pore on the tarsus (although an undescribed genus from New Zealand has recently been discovered which possesses these pores (Hodgson and Henderson, personal observations)), (xvi) microtubular ducts (except in the Cyphococcinae), and (xvii) true figure-of-eight pores (except in Bodenheimera and Mallococcus where they are present). Other significant features are that (i) adult females of most genera produce some sort of test, which may be woolly (as in the Filippiinae), glassy (as in the Cardiococcinae), thin wax (as in the Coccinae) or thick wax (as in the Ceroplastinae), (ii) the dorsum of the mature adult females of many species becomes heavily sclerotised at maturity, and (iii) the dorsum usually has dorsal setae, dorsal microductules and, frequently, preopercular pores, dorsal tubercles and tubular ducts. First-instar nymphs have much the same characters as the adults (but see also Section 1.1.2.3), except that pregenital disc-pores and tubular ducts are absent. In addition, dorsal setae are frequently absent and the tarsal digitules of the prothoracic leg are dissimilar, i.e. one lacking a terminal expansion. The adult males are discussed in Section 1.1.2.2.
CLASSIFICATION OF THE COCCIDAE Targioni Tozzetti (1868) and Signoret (1869) were probably the first to divide the taxa currently included in the family Coccidae into distinct groups. Within the division 'I.e,canites', Targioni-Tozzetti included seven groups, of which four are referable to present-day soft-scales: (i) the 'Eriophori demure folliculares', which contained Filippia and Luzulaspis (and the Eriococcidae), (ii) the 'Pulvinati', which included Pulvinaria (and Nidularia, now considered an eriococcid (Hoy, 1963)), (iii) the 'Ceriferi' including Ceroplastes, Columnea and Ericerus, and (iv) the 'nudi', with Lecanopsis and Lecanium. Later, Atkinson (1886) presented a classification based on that of Signoret (1869) but he divided the ~ i n a (= Lecanides of Signoret) into five distinct groups, (i) the Lecaniodiasparia, essentially the Lecaniodiaspites of Signoret (= Asterolecaniidae and l.,ecanodiaspididae of today), (ii) Signoretiaria, including Signoretia (= Luzulaspis), Eriopeltis and Philippia (= Filippia), (iii) Ceroplastaria, incorporating Ceroplastes and Vinsonia, (iv) Pulvinariaria, with Pulvinaria, and (v) Lecanaria, including Lecanium, Physokermes, Ericerus, Lecanopsis as well as Aclerda and Carteria. Apart from the inclusion of the last two taxa, groups (ii)-(v) are very similar to the modem groupings for these genera. Whilst Handlirsch (1903) may have been the first to use the superfamily Coccoidea (Williams, 1969), it was Steinweden (1929) who restricted the family Coccidae to the soft-scales as understood today. He studied the type species of 32 genera and proposed
Section 1.1.3.4 references, p. 198
TABLE 1.1.3.4.4
-
Comparison of some character-states of adult females in the tribes and subfamilies within the family Coccidae. Cardioc - Cardiococcinae, Ceropl - Ceroplastinae, Ciss Cissococcinae, Cocc -Coccini, Paralec - Paralecaniini, Pulvh - Pulvinariini, - Saissetiini, Cyphoc - Cyphococcinae, U e c - Eulecaniinae, Enop - Eriopeltiniae, Filip Filippiinae, Myzolec - Myzolecaniinae and Pseudo Pseodopulvinariinae; and where A absent and B - present, unless otherwise stated. Data from Hodgson, 1994a.
-
-
Cardioc Ceropl Ciss Ovisacltest: A = absent; F = felted; G = glassy; W = waxy Sclerotisation dorsum: 1=slight to 3 =heavy Dorsal setae: Dorsal tubular ducts: Dorsal microtubular ducts: Dorsal tubercles: Anal plates h e d posteriorly: Anal tube long: Eyespot: Stigmabcdefts: S = shallow; D = deep; A = absent Masetae: S = spinose; A = absent; B = setose Spiracular disc-pore band: B = broad; N = namw No. types of ventral tubular ducts: Pregdtal disc-pores: Most frequent number of loculi; A = absent Size of peritreme: N = normal; R = reduced Size of legs and antennae: N = normal; R = reduced Presence of tibio-tarsal articulation: Pregdtal setae: A = long, setose; B = shor~,spinose Claw digitules: A = both broad; B = at least one MITOW
G
Cocc
Paralec Pulvh Saiss
A
A
2
W 3
A
A A A A A B A
B A A A A B B
A B A A A A A B A A B? B A B
S
S
A
S
B
B
B
2
?
S
F
A
Cypboc U e c
Enop
Filip
G
F 1
3
l?
F
Myzol
Pseudo
3
A
F 2?
B AB A A A B B
B B A A A A A
B B A A B A A?
A
2
2
3
B A A A A
B B
B B A AB A B B
B A@) A AB A B B
AB A B AB A B A
B
B B A A A B B
D
s
s
A
AS
As
As
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Classificationof the Coceidaeand relatedfamilies
187
three groups: (a) the Coccus-group, including Coccus, Eulecanium, Lecanium, Protopulvinaria, Pulvinaria and Saissetia, (b) the Toumeyella-group, also including Neolecanium and Pseudophilippia, and (c) the Exaeretopus-group, with Exaeretopus, Parafairmairia, Philephedra and Luzulaspis. The other 19 genera were unplaced. With the possible exception of Parafairmairia, these groupings are accepted today. More recently, Bodenheimer (1953) divided the Coccidae into four subfamilies, the Ceroplastinae, Coccinae, Eriopeltinae and Filippiinae based primarily on the structure of the test secreted by the adult female. To a large extent, this arrangement was followed by Borchsenius (1957), except that he placed the Eriopeltinae in the Filippiinae and divided the Coccinae into two tribes, the Coccini and the Pulvinariini. Two further classifications of this family have now been proposed. The first, by Tang et al. (1990) and Tang (1991), who proposed a rather complex classification based entirely on female characters. It included four subfamilies: the Pseudopulvinariinae (introduced to include Pseudopulvinaria and Mallococcus) and the Filippiinae, Coccinae and Ceroplastinae. Each of the last three subfamilies was divided into tribes and subtribes. However, most of the genetic groupings suggested by Tang et al. (1990) are very different from those suggested by the studies of males and it is here considered unlikely that this classification will be generally accepted. The other classification was suggested by Hodgson (1994a) when he redescribed the adult females of the type species of all the known soft scale genera. This classification was based on the structure of the adult females and on male morphology as studied since about 1960. He divided the Coccidae into 10 subfamilies, with the Coccinae divided into four tribes, although he considered that the status of these groupings needed further study. This classification (based, as far as the adult females are concerned, on the type species of each genus only) is summarised in Table 1.1.3.4.4 and below.
I. CARDIOCOCCINAE Hodgson (Fig. 1.1.3.4.28). This subfamily, which might be loosely called the glassy scales, includes 16 genera. The adult females are characterised by" (i) the presence of a glassy test, (ii) the absence of dorsal setae, dorsal tubular ducts and dorsal tubercles, (iii) presence of spinose marginal setae, (iv) a distinctive distribution of dorsal pores, which occur in a distinctive pattern, often in a mid-dorsal line from the anal plates to the anterior margin of the head or forming a large reticulate pattern, (v) presence of pregenital disc-pores with typically five loculi, (vi) presence of a submarginal band of ventral tubular ducts, (vii) the inner margins of the anal plates often diverging posteriorly, with spinose setae along the inner margin in many genera, and (viii) absence of pairs of long setae medially on the pregenital segments, these replaced by bands of rather spinose setae. This subfamily is equivalent to the Inglisiagroup of Giliomee (1967). Based on the geographical distribution of the type species, the Cardiococcinae probably originated in the southern hemisphere.
II. CEROPLASTINAE Atkinson (Fig. 1.1.3.4.29). This subfamily includes all the genera related to Ceroplastes Gray. There is no general agreement as to the number of genera involved (see Qin and Gullan, 1995)) but the maximum at present would be nine, although several of these are clearly synonyms. This group of genera is very distinctive and the adult females can be recognised by the presence of: (i) a thick waxy test coveting the dorsum, mainly secreted by (ii) the distinctive dorsal Ceroplastes-type pores, (iii) a sclerotised caudal process, which lifts the anal plates above the thick wax cover, (iv) the presence of dorsal lobes or clear areas free from pores, (v) the form of the ventral microducts, which appear to have a cruciform opening and, to a lesser extent, (vi) the characteristics of the stigmatic areas. Although Giliomee (1967) considered
Section 1.1.3.4 references, p. 198
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Fig. 1.1.3.4.27. Tachardiidae. Tochordia fici Green,crawler. (Original).
Fig. 1.1.3.4.28. Coccidae: subfamily Cardiococcinae. Drepanococcus cajm' (Maskell), adult female. (From Hodgson, 1994a).
I
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Fig. 1.1.3.4.29. Coccidae: subfamily Ceroplastinae. Ceropfusfesjrneiremis(Gray), adult female. (From H o d p o , 1994).
Fig. 1.1.3.4.30. Coccidae: subfamily Cissococcinae. Cissococcmfilleri Cockerell, adult female. (From H o d p n , 1994a).
190
Systematics
members of this group to be close to Coccus, Hodgson (1994a) suggested that the characters of the female were sufficiently distinctive to justify their separation from the Coccinae. Based on their geographical distribution, the Ceroplastinae appear to be mainly Africa and South American in origin, although several species are now more widely distributed due to accidental introduction. III. CISSOCOCCINAE Brain (Fig. 1.1.3.4.30). The true relationships of this subfamily, which contains the monotypic genus Cissococcus Cockerell from South Africa, have been uncertain, although Hodgson (1994a) included it in the Coccidae on the strength of the paired anal plates, sunken ventral microducts and the possible absence of campaniform pores on the tarsi. However, from a recent study of the lst- and 2nd-instar nymphs and the pupa (see under Phylogeny (Section 1.1.3.7)), it is now clear that it is a true member of the Coccidae. Nonetheless, C. fulleri Cockerell has a number of unusual features and is the only member of the Coccidae known to produce a true gall (see Section 1.4.1.3). The main characters of the adult female are: (i) the reduction of the dorsum to a small area around the anal plates and their associated sclerotisations, the median areas of the venter becoming expanded, so that the legs, spiracles and mouthparts lie dorsally, (ii) possible complete absence of antennae, (iii) reduced legs, (iv) large spiracles, placed on the apparent dorsum with their atria facing medially, each with sparse bands of five-locular disc-pores also extending medially, (v) mouthparts also on the apparent dorsal surface, with the labium pointing anteriorly, (vi) presence of anal plates typical of the Coccidae, with numerous setae on their dorsal surface (as in the Myzolecaniinae), (vii) anal plates surrounded by a very large area of sclerotisation, which appears to be structurally quite different to that of other Coccidae, (viii) true venter covered in numerous long setae and 10-1ocular disc-pores, and (ix) absence of marginal setae and stigmatic spines.
IV. COCCINAE Fallrn. Hodgson (1994a) included 55 genera in four tribes in this subfamily but noted that, if groups such as the Eulecaniinae were to be given subfamily status, some of these tribes might also warrant similar status. The tribes were as follows: a. Coccini Fallrn (Fig. 1.1.3.4.31). Members of this tribe are typically characterised by: (i) lack of dorsal tubular ducts (except very sparsely submarginally in Coccus), (ii) absence of ventral tubular ducts or their restriction to medially in the thorax, (iii) lack of pocket-like sclerotisations, (iv) presence of eyespots, usually close to the margin, (v) stigmatic areas unsclerotised, (vi)presence of stigmatic spines differentiated from the marginal setae, and (vii) presence of pregenital disc-pores concentrated on the pregenital segment, never present medially on the thorax or head. As defined above, the Coccini contains 11 genera, the type species appearing to have a mainly tropical distribution, although many species now have a rather cosmopolitan distribution due to accidental introductions. b. P a r a l ~ i n i Williams (Fig. 1.1.3.4.32). Typical members of this tribe have (i) a distinct stigmatic cleft which is sclerotised on the dorsum at its base, (ii) no dorsal tubular ducts, (iii) ventral tubular ducts, when present, restricted to a group on either side of the genital opening, (iv) pregenital disc-pores restricted to the abdominal segments immediately anterior to the genital opening, and (v) eyespots displaced onto the dorsum, typically nearly dorsad to the base of each antenna. As def'med above the Paralecaniini include 12 genera but not all genera are distinctly separable from the Coccini. This group is restricted to South America, Australia and Asia.
Fig. 1.1.3.4.31. Coccidae: subfamily Coccinae: tribe Coccini. Coccus hesperidum Linnaeus, adult female. (From Hodgson, 1994a).
Fig. 1.1.3.4.32 Coccidae: subfamily Coccinae: tribe Paralecaniini. Puralewiumfienehii (Maskell), adult female. (From Hodgsoa, 19Wa).
,
1
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Fig. 1.1.3.4.33. Coccidae: subfamily Coccinae: tribe Pulvinariini. Pulvinurin M'& (Iinnaeus), adult female. (From Hodgson, 19Wa)
Fig. 1.1.3.4.34. Coccidae: subfamily Coccinae: tribe Saissetiini. Saisseria cofleoe (Walker), adult female. (From Hodgson, 1994a).
Classification of the Coccidae and related families
193
c. Pulvinariini Targioni Tozzetti (Fig. 1.1.3.4.33). Members of this tribe have: (i) a woolly ovisac secreted by the reproducing female from beneath the posterior end of the abdomen, often lifting the insect so that its body is held almost vertically above the head by the ovisac, (ii) ventral tubular ducts of generally three or four types (rarely two), including (a) a small duct with a fine inner ductule, generally occurring in a submarginal band, and (b) a larger duct with the inner and outer ductules of subequal width, these typically present medially in the head and thorax but occasionally elsewhere, (iii) no woolly test covering the dorsum, (or, if a mealy covering is present, this is very sparse), (iv) no dorsal tubular ducts, or if present, of one type only and typically similar to the smallest ventral ducts, (v) spinose dorsal setae, (vi) each leg with a tibio-tarsal articulation, (vii) no pocket-like sclerotisations, (viii) eyespots present near the margin, and (ix) shallow, unsclerotised stigmatic clefts. As restricted here, this tribe contains about 19 genera and appears to have an almost worldwide distribution. d. Saissetiini Hodgson (Fig. 1.1.3.4.34). Members of this tribe differ from other members of the Coccinae in: (i) presence of a broad submarginal band of ventral tubular ducts of one or two types, (ii) absence (typically) of dorsal tubular ducts, (iii) typically with dorsal tubercles and, often, also pocket-like sclerotisations, though both may be absent, (iv) presence of pregenital disc-pores, each usually with 10 loculi, extending medially onto thorax, (v) presence of eyespots near the margin, and (vi) presence of unsclerotised, shallow stigmatic clefts. The Saissetiini are rather similar to many species in the Eulecaniinae, but the type species of the genera in each group can be separated using the above combination of characters. Hodgson (1994a) included 13 genera, although the inclusion of some was tentative. On the basis of the type species, these genera appear to be centred mainly in Africa and South and Central America.
V. CYPHOCOCCINAE Hodgson (Fig. 1.1.3.4.35). This subfamily, which is currently restricted to Africa, contains only two distinctive genera. The females of this group are characterised by: (i) presence of microtubular ducts on the dorsum, otherwise unknown in the Coccidae, (ii) dorsum divided into two areas, the median area with few pores and no dorsal setae, the lateral areas with abundant pores and setae, (iii) these two areas separated by a sinuous line of strongly spinose setae, (iv) presence of pregenital disc-pores, each with six or seven loculi, frequent medially in all the abdominal and thoracic segments, (v) absence of preopercular pores, (vi) spiracular disc-pores present in broad bands, (vii) presence of spinose marginal setae, (viii) presence of tibio-tarsal pseudo-articulations, (ix) claw digitules both f'me, (x) absence of eyespots, and (xi) presence of a glassy test covering the median area of the dorsum.
VI. EULECANIINAE Koteja (Fig. 1.1.3.4.36). This is a fairly distinct group, characterised by: (i) pregenital disc-pores, each with 10 loculi, present medially on all the abdominal and thoracic segments and usually also on the head, (ii) presence of spinose or setose marginal setae, which are never fimbriate, (iii) absence of dorsal tubercles and pocket-like sclerotisations, (iv) typically with a complete ring of ventral tubular ducts present, (v) legs without a tibio-tarsal articulatory sclerosis, and (vi) even though the legs are well developed, the claw digitules are either both fine or dissimilar, never both broad. This subfamily is considered to contain 12 genera and, based on the distributions of the type species, the Eulecaniinae appears to be mainly centred in the Palaearctic Region, with a few species in the Holarctic Region.
Section 1.1.3.4 references, p. 198
Fig. 1.1.3.4.35. Coccidae: subfamily C y p h d n a e . Cyphococcur caesdpiniue Laing, adult female. (From Hodgson, 1994a).
Fig. 1.1.3.4.36. Coccidae: subfamily Eulecaniinae. Eufecrnium lifiae (Linnaeus), adult female. (From Hodgson, 1994a).
Classijicahn of the Coccihe and relared-families
( F ~ l o m ~ ) , Fig. 1.1.3.4.38. Coccidae: subfamily Filippiinae. Filippiufolliculurk (Targioni Tozzetti), adult female. (From Hodgson, 1994a).
195
Fig. 1.1.3.4.37. C m i d a e : subfamily Eriopeltinae. Eriope& f..t..m adult female. (From Hodgson, 1994a).
196
Systematics
VII. ERIOPELTINAE ,~ulc (Fig. 1.1.3.4.37). This and the Filippiinae form a rather heterogenous group and are not easily separable based on adult females characters. The main characters of adult female Eriopeltinae are: (i) body elongate, (ii) production of a felted ovisac over the whole or part of the dorsum, which is secreted by (iii) large tubular ducts on the dorsum, which are similar to the tubular ducts found submarginally on the venter, (iv) a membranous dorsum, without areas of dense sclerotisation, (v) each anal plate frequently with one or two setose or spinose setae along the inner margin, (vi) lack of stigmatic clefts, (vii) pregenital disc-pores each with 7-10 loculi, (viii) presence typically of two types of ventral tubular ducts, the larger submarginally, (ix) legs and antennae well developed, (x) presence of either 0 or two stigmatic spines in each stigmatic area, and (xi) lack of dorsal tubercles and pocket-like sclerotisations. In addition, members of this subfamily are usually restricted to monocotyledonous plants. As def'med here, the Eriopeltinae contains 14 genera and includes species with a cosmopolitan distribution.
VIII. F I L I P P ~ A E Bodenheimer (Fig. 1.1.3.4.38). The adult females of this group are very similar to the Eriopeltinae, although work on adult male morphology (Giliomee, 1967; Koteja, 1966, 1969, 1970; Manuwadu, 1986; Miller, 1991) suggests that the Filippiinae may include two or more groups. The Filippiinae mainly occur on dicotyledonous plants. The adult females are roundly oval in shape, sometimes have dorsal tubercles and pocket-like sclerotisations and have 0, one, two or three stigmatic spines in each stigmatic cleft. Otherwise they share most of the characters given above for the Eriopeltinae and, like them, have a rather cosmopolitan distribution.
IX. MYZOLECANIINAE Hodgson (Fig. 1.1.3.4.39). This subfamily contains about 16 genera, most or all of which have a very close and possibly sometimes obligatory relationship with ants. The main characters of the adult females are: (i) the lack of dorsal tubular ducts, (ii) absence of eyespots, (iii) presence of anal plates with typically numerous setae on the dorsal surface, (iv) particularly large and often somewhat modified spiracles (Hodgson, 1995b), with broad bands of spiracular disc-pores between the margin and the spiracle, (v) ventral tubular ducts of one type, frequently restricted to a group on either side of the genital opening, (vi) without median pairs of long pregenital setae but with segmental bands of short spinose setae, (vii) legs reduced, with both claw digitules fine, (viii) reduced antennae, and (ix) a short anal tube. Based on the type species, this subfamily occurs in all zoogeographic regions except China, the Palaearctic and New Zealand. The Myzolecaniinae is equivalent to the Toumeyellagroup of Ray and Williams (1983) based on the study of males.
X. PSEUDOPULVINARIINAE Tang, Hao, Xie and Tang (Fig. 1.1.3.4.40). As restricted by Hodgson (1991, 1994a) this subfamily is monotypic and is found only in the eastern part of the Himalayas. Although Tang et al. (1990) included the genus Mallococcus Maskell, this is here considered to be closely related to Bodenheimera Bodenheimer and belongs to the Filippiinae. The main characters of the adult female of this subfamily are: (i) the production of a dense, woolly test which covers the entire insect, probably secreted by (ii) abundant sclerotised, five-locular disc-pores or cribriform plates which cover the entire dorsum and also form a narrow submarginal band ventrally, (iii) anal plates which appear to be joined along both the dorsal and ventral margins, each plate rather triangular in shape, with long spinose setae, appearing rather like a crown, (iv) anal tube either very short or absent, (v) extremely large spiracles, (vi) dorsum lacking tubular ducts, but (vii) with one or two types of tubular duct ventrally, (viii) presence of strongly spinose marginal setae, but (ix) with the stigmatic spines undifferentiated and (x) legs and antennae more or less well developed.
fig. 1.1.3.4.39. Coccidae: subfamily Myzolexaniinae. Myrolemiurn kibarac Beccari, adult female. (From Hodgson, 1994a).
Fig. 1.1.3.4.40. Coccidae: subfamily Pseudopulvinariioae. Pseudopdvinaria sikmensis Atkinson, adult female. (From €Iodgson, 1991).
Systematics
198
Hodgson (1991) described the male of Pseudopulvinaria sikkimensis Atkinson and concluded that the characters of this genus were sufficiently different from others in the Coccidae to justify subfamily status. In addition to the above taxa, Hodgson (1994a) was unable to place Alecanochiton Hempel, Parafairmairia Cockerell and Pseudalichtensia Hempel in any of the above subfamilies.
REFERENCES Afifi, S.A., 1968. Morphology and taxonomy of the adult males of the families Pseudococcidae and Eriococcidae (Homoptera: Coccoidea). Bulletin of the British Museum (Natural History), Entomology Supplement, 137: 1-210. Afifi, S. and Kosztarab, M., 1969. Morphological and systematic studies on the adult males of some species of Lecanodiaspis (Homoptera: Coccoidea: Lecanodiaspididae). Virginia Polytechnic Institute Blacksburg, Research Division Bulletin, 36" 1-23. Amin, A.H., Afifi, S.A. and Nada, S.M.A., 1976. Taxonomy of four adult males of the family Lecanodiaspididae. Bulletin de la Soci6t6 Entomologique d'Egypte, 60: 153-169. Atkinson, E.T., 1886. Insect-pests belonging to the Homopterous family Coccidae. Journal of the Asiatic Society of Bengal. Natural History, 55: 267-298. Baer, R.G. and Kosztarab, M., 1985. A morphological and systematic study of the first and second instars of the Family Kermesidae in the Nearctic region (Homoptera: Coccoidea). Bulletin of the Virginia Agricultural Experiment Station, Virginia Polytechnic Institute and State University, Blacksburg, 85 (11): 119-261. Balachowsky, A., 1942. Essai sur la classification des Cochenilles (Homoptera-Coccoidea). Annales de Grignon E,cole National d'Agriculture (Series 3) 3" 34-48. Balachowsky, A., 1948. Les cochenilles de France, d'Europe, du Nord de l'Afrique, et du bassin M6diterran6en. IV. Monographie des Coccoidea; Classification- Diaspididae (Premiere pattie). Actualit6s Science et Industrie, Entomologie Appliqu6e, 1054: 243-394. Ben-Dov, Y., 1977. New species ofAclerda Signoret (Homoptera: Aclerdidae) from southern Africa. Journal of Natural History, 11: 371-376. Ben-Dov, Y., 1985. Coccoidea. In: 'Insects of Southern Africa', Scholtz, C.H. and Holm, E. (Editors). Butterworths, Durban. pp. 168-175. Ben-Dov, Y., 1990. Classification of the Diaspidoid and related Coccoidea. In: World Crop Pests. Armoured Scale Insects. Their Biology, Natural Enemies and Control. Vol. 4A. D. Rosen (F.xlitor). Elsevier Press. pp 97-128. Ben-Dov, Y., 1993. A Systematic Catalogue of the Soft Scale Insects of the World (Homoptera: Coccoidea: Coccidae) with data on geographical distribution, host plants, biology and economic importance. Flora and Fauna Handbook No. 9. Sandhill Crane Press, Inc., Gainesville, Florida, xxviii + 536 pp. 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. Boratyfiski, K. and Davies, R.G., 1971. The taxonomic value of male Coccoidea (l-lomoptera) with an evaluation of some numerical techniques. Biological Journal of the Linnean Society, 3: 57-102. Borchsenius, N.S., 1957. Sucking Insects, Vol. IX. Suborder mealybugs and scale insects (Coccoidea). Family cushion and false scale insects (Coccidae). Fauna SSSR, Novaya Seriya, 66:493 pp. (In Russian). Borchsenius, N.S., 1958. On the evolution and phylogenetic interrelations of the Coccoidea. Zoologicheskii Zhurnal, 37: 765-780. (In Russian). Borchsenius, N.S., 1959. Notes on coccid fauna of China. 7. A new family of soft scales Lecaniodiaspididae, Fam. N. (Homoptera: Coccoidea). Entomologicheskoe Obrozrenie, 38: (840)-846. Borchsenius, N., 1960. Fauna USSR: Homoptera 8. Suborder mealybugs and scales (Coccoidea), families Kermococcidae, Asterolecaniidae, Lecaniodiaspididae, Aclerdidae. Fauna SSSR, Novaya Seriya, No. 77, 283 pp. (In Russian). Brown, S.W., 1977. Adaptive status and genetic regulation in major evolutionary changes of coccid chromosome systems. Nucleus 20; 145-157. Buchner, P., 1965. Endosymbiosis of animals with microorganisms. Interscience Publ., John Wiley & Sons Inc., New York. 909 pp. Bullington, S.W. and Kosztarab, M., 1985. Revision of the Family Kermesidae (Homoptera) in the Nearctic Region based on adult and third instar females. Bulletin of the Virginia Agricultural Experiment Station, Virginia Polytechnic Institute and State University, Blacksburg, 85 (ll):vi+ 1-119. Chamberlin, J.C., 1923. A systematic monograph of the Tachardiinae or Lac Insects (Coccidae). Bulletin of Entomological Research, 14:147-212. Chamberlin, J.C., 1925. Supplement to a monograph of the Lacciferidae (Tachardiinae) or Lac Insects (Homopt., Coccidae). Bulletin of Entomological Research, 16: 31-41.
Classification of the Coccidae and related families
199
Cox, J.M. and Williams, D.J., 1986. Do the Eriococcidae form a monophyletic group? Bollettino del Laboratorio di Entomologia Agraria "Filippo Silvestri" Portici, 43 (suppl.): 13-17. Danzig, E.M., 1986. Coccids of the Far-Eastern USSR (Homoptera, Coccinea). Phylogenetic Analysis of Coccids in the World Fauna. Nauka Publishers, Leningrad, 1980. Translated from the Russian and published by the United States Department of Agriculture and the National Science Foundation, Washington, DC. xxv + 450 pp. De Lotto, G., 1974. On the status and identity of the cochineal insects (Homoptera: Coccoidea: Dactylopiidae). Journal of the Entomological Society of Southern Africa, 37: 167-193. Fernald, M.E., 1903. A catalogue of the Coccidae of the World. Bulletin of the Hatch Agricultural Experiment Station of the Massachusetts Agricultural College, 88: 1-360. Ferris, G.F., 1955. Atlas of the Scale Insects of North America, v. 7. The families Aclerdidae, Asterolecaniidae, Conchaspididae, Dactylopiidae and Lacciferidae. Stanford University Press, California. iii + 233 pp. Ferris, G.F., 1957. Notes on some little known genera of the Coccoidea. Microentomology, 22: 59-79. Gill, R.J., 1993. The Scale Insects of California Part 2. The Minor Families (Homoptera: Coccoidea). Technical Services in Agricultural Biosystematics and Plant Pathology, California Department of Food and Agriculture, Vol. 2: xii + 241 pp. 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. Giliomee, J.H., 1968. The morphology and relationships of the male of Lecaniodiaspis elytropappi Munting & Giliomee (Homoptera: Coccoidea). Journal of the Entomological Society of Southern Africa, 30:185-197. Giliomee, J.H. and Munting, J., 1968. A new species of Asterolecanium Targ. (Homoptera: Coccoidea: Asterolecaniidae) from South Africa. Journal of the Entomological Society of Southern Africa, 31:221-229. Handlirsch, A., 1903. Zur Phyiogenie der Hexapoden. Sitzungsberichte der Akademie der Wissenschatten in Wien, 112: 716-738. Hamon, A.B. and Kosztarab, M., 1979. Morphology and systematics of the first instars of the genus Cerococcus (Homoptera: Coccoidea: Cerococcidae). Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 146: vi+ 121. Hamon, A.B., Lambdin, P.L. and Kosztarab, M., 1976. Life history and morphology of Kermes kingi in Virginia (Homoptera: Coccoidea: Kermesidae). Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 111" 1-31. Hodgson, C.J., 1973. A revision of the Lecanodiaspis Targioni Tozzetti (Homoptera: Coccoidea) of the Ethiopian Region. Bulletin of the British Museum (Natural History), Entomology Supplement 27(8): 413-452. Hodgson, C.J., 1991. A redescription of Pseudopulvinaria sikkimensis Atkinson (Homoptera, Coccoidea), with a discussion of its affinities. Journal of Natural History, 25:1513-1529. Hodgson, C.J., 1994a. The Scale Insect Family Coccidae: An Identification Manual to Genera. CAB International, Wallingford. vi+639 pp. Hodgson, C.J., 1995a. The possible evolution of the plate-like structures associated with the anal area of the lecanoid Coccoidea. Israel Journal of Entomology, 29: 57-65. Hodgson, C.J., 1995b. A brief review of the structure of the spiracle in the family Coccidae. Israel Journal of Entomology, 29: 47-55. Howell, J.O., 1972. A new species of Aclerda from Spanish moss in Georgia (Homoptera: Coccoidea: Aclerdidae). Annals of the Entomological Society of America, 65: 1261-1264. Howell, J.O., 1973. The immature stages ofAclerda n'llandsiae (Homoptera: Coccoidea: Aclerdidae). Annals of the Entomological Society of America, 66: 1335-1342. Howell, J.O., 1976. The adult male ofAclerda tiUandsiae. Morphology and systematic significance. Annals of the Entomological Society of America, 69: 885-888. Howell, J.O. and Kosztarab, M., 1972. Morphology and systematics of the adult females of the genus Lecanodiaspis (I-lomoptera: Coccoidea: Lecanodiaspididae). Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 70: 1-248. Howell, J.O. and Williams, M.L., 1976. An annotated key to the families of scale insects (Homoptera: Coccoidea) of America, North of Mexico, based on characters of the adult female. Annals of the Entomological Society of America, 69: 181-189. Howell, J.O., Lambdin, P.L. and Kosztarab, M., 1973. Morphology and systematics of three species of the eucalypti group of the genus Lecaniodiaspis (Homoptera: Coccoidea: Lecanodiaspididae). Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 85:31-51. Hoy, J.M., 1963. A Catalogue of the Eriococcidae (Homoptera: Coccoidea) of the World. Bulletin of the New Zealand Department of Scientific and Industrial Research, 150: 1-260. Hu Xingping, 1987. Studies on gall-like scale insects, descriptions of three new species from Shandong, China (Homoptera: Coccoidea: Kermesidae). Entomotaxonomia, 5:299-316. Kosztarab, M., 1968. Cryptococcidae. A new family of the Coccoidea (Homoptera). The Virginia Journal of Science, 19: 12. Kosztarab, M. and KozAr, F., 1988. Scale Insects of Central Europe. Series Entomologica, Vol. 41. W. Junk, Dordrecht, 456 pp.
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Systematics
Koteja, l., 1966. Studies on morphology and biology of Luzulaspisfrontalis (Green) (Homoptera, Coccoidea). Polskie Pismo Entomologiczne, 36: 17-43. Koteja, J., 1969. Psilococcus parvus Borchsenius (Homoptera, Coccoidea) - morphology, biology and taxonomy. Acta Zoologica Cracoviensia, 14: 21-41. Koteja, J., 1970. Systematic position of the genus Vinacoccus Borchsenius (Homoptera, Coccidae). Polskie Pismo Entomologiczne, 40:223-231. Koteja, J., 1974a. The occurrence of campaniform sensillum on the tarsus in the Coccinea (Homoptera). Polskie Pismo Entomologiczne, 44: 243-252. Koteja, J., 1974b. Comparative studies on the labium in the Coccinea (Homoptera). Zeszyty Naukowe Akademii Rolniczej w Krakowie, 27: 1-162. Koteja, J., 1986. Morphology and taxonomy of male Ortheziidae (Homoptera, Coccinea). Polskie Pismo Entomologiczne, 56: 323-374. Koteja, J. and Zak-Ogaza, B., 1972. Morphology and taxonomy of the male Kermes quercus (L.) (Homoptera: Coccoidea). Acta Zoologica Cracoviensia, 17: 195-215. Lambdin, P.L. and Kosztarab, M., 1973. A morphological study on the adult female and two nymphal stages of MaUococcus sinensis (Maskell) with notes on its systematic position (Homoptera: Coccoidea: Coccidae). Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 85: 53-68. Lambdin, P.L. and Kosztarab, M., 1977. Morphology and systematics of the adult females of the genus Cerococcus (Homoptera: Coccoidea: Cerococcidae). Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 128: 1-252. Lambdin, P.L., Howell, J.O. and Kosztarab, M., 1973. Morphology and systematics of five species in the Quercus group of the genus Lecaniodiaspis (Homoptera: Coccoidea: Lecanodiaspididae). Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 85: 1-29. Loubser, H.J., 1966. A study on the morphology and taxonomy of the males of two Dactylopius species (Hemiptera: Coccoidea). M.Sc. Thesis, University of Stellenbosch, Republic of South Africa. 107 pp. McConneU, H.S., 1953. A classification of the family Aclerdidae. Bulletin of the Agricultural Experiment Station, University of Maryland A-75: 1-121. Manuwadu, D., 1986. A new species ofEriopeltis Signoret (Homoptera: Coccidae) from Britain. Systematic Entomology, 11 : 317-326. Marotta, S., Spicciarelli, R. and Tranfaglia, A., 1995. Diagnosis of Micrococcus Leonardi, redescription of its type species with discussion of the status of the family Micrococcidae (Homoptera: Coccoidea). Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', Portici, 50 (1993): 175-198. Miller, D.R., 1984. Phylogeny and classification of the Margarodidae and related groups (Homoptera: Coccoidea). Verhandlungen des Zehnten Internationalen Symposiums fiber Entomofaunistik Mitteleuropas (SIEEC X), 15-20 Aug. 1983, Budapest, pp 321-324. Miller, D.R. and Gon~lez, R.H., 1975. A taxonomic analysis of the Eriococcidae of Chile. Revista Chilena de Entomologia, 9: 131-163. Miller, D.R. and Kosztarab, M., 1979. Recent advances in the study of scale insects. Annual Review of Entomology, 24: 1-27. Miller, D.R., Liu, Tong-Xian and Howell, J.O., 1992. A new species of Acanthococcus (Homoptera: Coccoidea: Eriococcidae) from Sundew (Drosera) with a key to the instars of Acanthococcus. Proceedings of the Entomological Society of Washington 94:512-523. Miller, D.R. and Miller, G.L., 1993a. Eriococcidae of the Eastern United States (Homoptera). Contributions of the American Entomological Institute, 27: 1-91. Miller, D.R. and Miller, G.L., 1993b. Description of a new genus of scale insect with a discussion of relationships among families related to the Kermesidae (Homoptera: Coccoidea). Systematic Entomology, 18: 237-251. Miller, D.R. and Miller, G.L., 1993c. A new species of Puto and a preliminary analysis of the phylogenetic position of the Puto group within the Coccoidea (Homoptera: Pseudococcidae). Jeffersoniana, 4: 1-35. Miller, D.R. and Williams, D.J., 1995. Systematic revision of the family Micrococcidae (Homoptera: Coccoidea), with a discussion of its relationships and a description of a gynandromorph. BoUettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', Portici, 50 (1993): 199-247. Miller, G.L., 1991. Morphology and Systematics of the Male Tests and Adult Males of the Family Coccidae (Homoptera: Coccoidea) from American North of Mexico. Ph.D. thesis, Auburn University, Auburn, Alabama, USA. Munting, J., 1965. Lac insects (Homoptera: Lacciferidae) from South Africa. Journal of the Entomological Society of Southern Africa, 28: 32-43. Munting, J., 1966. Lac insects (Homoptera: Lacciferidae) from South Africa - U. Revue de Zoologie et Botanie Africaine, 74: 121-134. Munting, J. and Giliomee, J.H., 1967. A new species ofLecaniodiaspis Targ,. (Homoptera: Asterolecaniidae) from South Africa. Journal of the Entomological Society of Southern Africa, 29: 102-108. Nada, S.M.A, Afifi, S.A. and Amin, A.H., 1976. Taxonomic status of family Aclerdidae according to the adult males (Homoptera: Coccoidea). Bulletin de la Socirt~ Entomologique d'Egypte, 60: 133-140. Qin, Ting-kui, and Gullan, P.J., 1995. A cladistic analysis of wax scales (Hemiptera: Coccoidea: Coccidae: Ceroplastinae). Systematic Entomology, 20: 289-308.
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O'Brien, L.B., Stoetzel, M.B. and Miller, D.R., 1991. Order Homoptera. In: Immature Insects, Vol. 2. Ed. F.W. Stehr. Kendell/Hunt Publ. Co., Iowa, pp 66-111. Perez Guerra, G.P. and Kosztarab, M., 1992. Biosystematics of the Family Dactylopiidae (Homoptera: Coccinea) with emphasis on the life cycle of Dactylopius coccus Costa. Bulletin of the Virginia Agricultural Experiment Station, Virginia Polytechnic Institute and State University, Blacksburg, 92 (1):vi+ 1-87. 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. Samouelle, G., 1819. The Entomologist's Useful Compendium; or an Introduction to the Knowledge of British Insects. Thomas Boys, 7 Ludgate Hill, London, pp. 1-146 (not seen). Signoret, V., 1869. Essai sur les cochenilles ou gallinsectes (Homopt~res - Coccides), (3"- partie). Annales de la Socirt6 Entomologique de France (Srr. 4), 9: 97-104. Silvestri, F., 1939. Fam. Coccidae. Compendio di Entomologia Applicata. Parte Speciale. Tipografia Bellavista, Portici, 1: 618-860. Steinweden, J.B., 1929. Bases for the generic classifications of the coccoid family Coccidae. Annals of the Entomological Society of America, 22: 197-245. Tang, Fang-teh., 1991. The Coccidae of China. Shanxi United Universities Press, P.R. China. 377 pp. + 84 figs. Tang, Fang-teh, Hao, J., Xie, Y. and Tang, Y., 1990. Family group classification of Asiatic Coccidae (l-lomoptera, Coccoidea, Coccidae). Proceedings of the Vlth International Symposium of Scale Insect Studies, Cracow, Aug. 6-12th, 1990, Part II: 75-77. Targioni Tozzetti, A., 1868. Introduzioni alia seconda memoria per gli studj sulle Cocciniglie, e catalogo dei generie della specie delle famiglia dei Coccidi. Atti della Societh ltaliana di Scienze Naturali e del Museo Civico de Storia Naturale de Milano, 11: 694-738. Teague, M.M., 1925. A review of the genus Aclerda (Hemiptera; Coccidoidea). Annals of the Entomological Society of America, 18: 432-441. Tremblay, E., 1977. Advances in endosymbiotic studies in Coccoidea. Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 127: 23-33. Walczuch, A., 1932. Studien an Coccidensymbionten. ZeitschriR fiir Morphologie und ()kologie der Tiere, 25: 623-729. Williams, D.J., 1969. The family-group names of the scale insects (l-lemiptera: Coccoidea). Bulletin of the British Museum (Natural History), (Entomology), 23:317-341. Williams, D.J., 1985. The British and some other European Eriococcidae (Homoptera: Coccoidea). Bulletin of the British Museum (Natural History), Entomology Series 51 (4): 347-393. Williams, D.J. and Watson, G.W., 1990. The Scale Insects of the Tropical South Pacific Region, Part 3. The Soft Scales (Coccidae) and other Families. CAB International, WaUingford. 267 pp. Williams, M.L. and Kosztarab, M., 1970. Morphology and systematics of scale insects- no. 2. A Morphological and systematic study on the first instar nymphs of the genus Lecanodiaspis (Homoptera: Coccoidea: Lecanodiaspididae). Virginia Polytechnic Institute Blacksburg, Research Division Bulletin, 52: 1-96. Zhang, Zheng-Song, 1993. Four new species of lac insect of the genera Metatacharrlia and Kerria from China (Homoptera: Tachardiidae). Oriental Insects, 27: 273-286.
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Soft Scale Insects - Their Biology, Natural Enemies and Control
Y. Ben-Dovand C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.
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1.1.3.5 Intraspecific Variation of Taxonomic Characters EVELYNA M. DANZIG
INTRODUCTION Intraspecific variation of taxonomic characters is widespread in the Coccoidea in general and in the soft scales in particular. This variation in the soft scale species so far studied is favoured by their wide geographic distribution, by their polyphagy and because they reproduce by parthenogenesis. This intraspecific variation is shown by both morphological and biological characters. Thus, the variability in the biological characters is shown mainly by the range in types of parthenogenesis, the sex ratio and in the seasonal development; the greatest variation in morphology is shown by the number of dorsal submarginal tubercles. Some of these characters depend on the nutritive condition of the host plant, but some inter-population variation is also occasionally caused by parasitoids. Because intraspecific variation has been extensively studied in Parthenolecanium corni (Bouchr) and Pulvinaria vitis (L.), these two species are discussed in more detail below.
INTRASPECIFIC VARIABILITY IN POPULATIONS OF THE EUROPEAN FRUIT SCALE PARTHENOLECAMUM CORN/BOUCHIf:
Variability of morphological characters P a r t h e n o l e c a n i u m corni is widespread in both the Old and the New World and is highly polyphagous, with about 350 known host plant species (Kawecki, 1958; Ben-Dov, 1993). The great economic importance of this species has attracted much research, particularly on the morphological variation of many of its characters and the dependence of this variation on the species of host plant. Thus, the shape, size and colouration of the adult female all vary greatly between plant species, the extreme forms ranging from nearly round and strongly convex on Prunus to elongate and flattened on Robinia. This polymorphism has led to a wide synonymy (Borchsenius, 1957), to the extent that Sitvescu (1943, 1944) described 11 ecological forms off different host plants from Romania. Earlier, Marchal (1908) had accepted the existence of a variety of this species, L e c a n i u m corni var. robiniarum, living on Robinia, because he had found high mortality when the insects were transferred from this plant to other hosts, although such difficulties have not been noted with the same form by recent authors. Transfer experiments (Marchal, 1908; Sanders, 1909; Voukassovitch, 1930; Ebeling, 1938; Habib, 1957) have shown that P. corni easily adapts to a new plant and then changes its appearance to the form typical of the new host species. Along with extreme variations in its external appearance, P. corni also varies in microscopic characters, the most important of which is the number of submarginal
Section 1.1.3.5 references, p. 210
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Sys~ematics tubercles on adult females and on second-instar nymphs. Thus, females from the Palaearctic have from 0 to 8 or 9 pairs (,~ulc, 1932; Borchsenius, 1957; Dziedzicka and Sermak, 1967). These tubercles on specimens from the Palaearctic are usually deformed, although ,~ulc recorded adult females with 9 pairs of well-developed tubercles in Czechoslovakia. In the Far East, on the other hand (i.e. in Korea, China and Japan), up to 12 pairs of well-developed tubercles have been recorded on adult females off several different host plants and, on the basis of this character, the Far Eastern form was treated as a separate subspecies P. corni orientalis by Borchsenius (1957). However, among the numerous specimens collected from the adjacent Russian Far East, only one female (Vladivostok, on Spiraea) has been found with as few as 7 pairs of well-developed tubercles (Danzig, 1980, 1986). In recent publications from North America (Richards, 1958; Phillips, 1965a; Williams and Kosztarab, 1972; Hamon and Williams, 1984; Gill, 1988), a complex of species close to P. corni (the "corni-complex') has been recognised, in which the species mainly differ in the number of submarginal tubercles in the female. Apart from P. corni, the other species are P. quercifex (Fitch), P. pruinosum (Coquillett), P. cerasifex (Fitch) and P. putmani Phillips. However, so far it has proved impossible to distinguish these species with certainty on the basis of the morphological characters (Nakahara, 1981). The number of well-developed pairs of submarginal tubercles in 2nd-instar nymphs usually varies from 0 to 5, but many studies have shown that the number of tubercles depends on the geographic distribution of the population and on the host plant. Thus, most nymphal populations feeding on Prunus have tubercles. On the other hand, these tubercles are extremely rare or absent in nymphs which develop on Robinia and Gleditsia (Saakyan-Baranova et al., 1971). Nuzzaci (1969) described a new subspecies, P. corni apuliae off Vitis vinifera from Italy, which possessed tubercles the number varying between 10 and 13, but with 67 % of the insects having 12 tubercles in 6 pairs.
Variability of biological characters Heterogeneity in populations of P. corni is also shown in both the sex ratio and its phenology. A comprehensive study (Saakyan-Baranova et al., 1971) of this species was undertaken in The Laboratory of Experimental Entomology, The Zoological Institute, Russian Academy of Sciences, St. Petersburg. These observations are briefly considered below. Reproduction. As with many other coccids, P. corni reproduces primarily by parthenogenesis rather than by sexual reproduction. The sex ratio in populations of P. corni is extremely variable and apparently depends on the feeding conditions. Thus, for example, the proportion of males is, as a rule, much higher on Prunus species than on arboreal Fabaceae, although some authors (Thiem, 1933a; Canard, 1958) have related the fluctuations in sex ratio to climatic conditions and others to altitude (Thiem, 1933b). Thomsen (1929) described the type of parthenogenesis of P. corni in Europe as thelytoky, although, in America, Phillips (1965b) showed that the type of parthenogenesis differed between species of "corni-complex". For instance, P. cerasifex, was found to have deuterotoky and P. putmani diploid arrhenotoky. However, Nut (1972, 1980) showed that these two species had both types of parthenogenesis and that P. cerasifex also had thelytoky. Neither the cytogenetic data nor the morphological data, therefore, allows us to consider these species as being distinct. Thus, it appears as though there may be only a single species which shows considerable variation in the type of parthenogenesis, as noted below for Pulvinaria vitis. Seasonal development. Depending on geographic position and host plants, P. corni may develop one generation in the northern Palaearctic but up three generations in the south. Northern populations, which inhabit forest and forest-steppe ecosystems, are
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always monovoltine, but further south the number of generations observed varies depending on the host plants. In Romania (S~ivescu, 1943, 1944), Southern France (Canard, 1958), Moldova, the Caucasus and in the valleys of Central Asia (Saakyan-Baranova et al., 1971), only one generation normally develops on Prunus, Crataegus, Diospyros, Corylus and Acer negundo, whereas two generations develop on Caragana, Robinia, Gleditsia, Morus, Persica and Maclura. However, this pattern is broken in some localities, such as in southern France, where the second generation on Robinia is facultative (Canard, 1958), although three generations have been found on this host in the Caucasus (Dubrovskaya, 1959). In southern Moldavia and in Central Asia, a faeultative or even complete second generation can develop on Prunus (Saakyan-Baranova et al., 1971). In North America, where P. corni may have been introduced from Europe, only one generation has usually been observed (Baily, 1964; Williams and Kosztarab,1972; Hamon and Williams, 1984), although development of a second generation has been noted in Florida (Gill, 1988, without reference to the host plant) and in southern Pennsylvania on Persica vulgaris (Asquith, 1949). Laboratory studies of P. corni have shown that the development of populations from northern regions of Russia (St. Petersburg and Belgorad Province) are monocyclic with an obligatory diapause. The development depends on the photoperiodic regime and the host plant. This development of P. corni from Moldova depends on the host plant: the populations on Prunus have a northern type of development, i.e. monocyclic, whereas on Robinia they are polycyclic. In the populations of Central Asia the photoperiodic reaction does not depend on the host plan: development on both Prunus and Robinia was of the polycyclic type, since the retarding influence on Prunus was only slight. This dependence on the photoperiodic response of the host plant has also been noted with other insects, although the shifts in phenology are normally slight, where "such notable changes, as found in P. corni, have not been observed. Apparently (the changes in P. corni) are determined by the particularly close relationship of this species with its host plants. It is likely that this profound influence of the host plant will also be observed in other coccids. So far, it is difficult to judge the cause of such a strong influence, but it seems probable that it is associated with the periodicity of host plant growth. As in most trees, Prunus included, growth is determined by a photoperiodic reaction and so (in Prunus) is limited by a comparatively short spring, whereas the growth of Robinia and Caragana continues during most of the summer (Moshkov, 1961). Therefore, it is likely that one of the factors regulating the development of P. corni is the biochemical changes related to the cyclical growth of host plants, particularly those associated with the growth hormones. It should be emphasized that the photoperiodic responses that have been described (for P. corni) and which are typical of different populations, manifested themselves in most, but not in all, individuals in a population" (Saakyan-Baranova et al., 1971). Intraspecific differentiation The study of S~kyan-Baranova et al. (1971) on the morphology and life history of P. corni shows that populations can differ in a number of characters. Most populations can be placed in one of 3 main groups: The main characters of the first group are the following: (1) second-instar nymphs of both males and females possess submarginal tubercles, the number varying but generally averaging four or five pairs; (2)development of the monocyclic type; (3) males are present although the sex ratio varies depending on the geographic locality, host plant and meteorological conditions, and (4) the host plants belong to the genera Corylus, Ulmus, Fraxinus, Cotoneaster, Malus, Ribes, Rubus, Rosa and the species Prunus
Section 1.1.3.5 references, p. 210
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Systematics spinosa, P. domestica, Acer negundo, Diospyros kaki and Caragana arborescens but the latter only in the north of the Palaearctic. This population type is present throughout the Eurasian region, extending from Great Britain in the west to the Russian Far East and from the north-west of Russia in the north to southern Armenia in the south. Within this area, although the number of submarginal tubercles in second-instar nymphs from each geographic population may vary, it is typical of each particular population. This character is relatively stable in some populations but more variable in others. For instance, populations in the vicinity of St. Petersburg, Moscow and on the Sakhalin Island, and also those in Great Britain (Habib, 1957) and Switzerland (Suter, 1950) are characterized by four pairs of tubercles, whereas in Moldova, the Crimea, Armenia, in Kazakhstan near Alma-Atu and also in Far Eastern Russia, Poland (Kawecki, 1958; Bielenin, 1958; Dziedzicka and Sermak, 1967), Czechoslovakia (Blattny and Novieky, 1926) and in southern France (Canard, 1958), the average number of tubercles is generally five, although this can vary considerably. The second group of populations is very different from the first and has the following characters: (1) submarginal tubercles entirely absent in second-instar nymphs; (2) development is of the polyeyclic type; (3) males are either absent or extremely rare, i.e. reproduction is obligatory parthenogenetic, and (4) their host plants are primarily arboreal Fabaceae, Robinia pseudacacia, Gleditsia, Amorpha, Sophora, Caragana arborescens and also some Rosaceae (e.g., Persica) and Moraceae (e.g., Maclura and Morus). Populations of this second type have been found in the south of Russia, Transcaucasia, south-eastern Kazakhstan and in Central Asia. The third group of P. corni populations has a combination of the characters of the first two groups. Thus: (1) second-instar female nymphs usually lack submarginal tubercles although they are present in second-instar male nymphs; (2) at least a part of the population is polyeyclic but the other part apparently has monocyclic development; such populations have been found in Moldova, in northern Caucasus, in Armenia and in the vicinity of Alma-Am, Kazakhstan, and (3) their host plant is usually Prunus. From the above, it is clear that both the biological and morphological characteristics of P. corni populations vary geographically and also between host plants within the same geographic region. This creates a complex pattern of local populations with different combinations of characters. In the north, where the short summer season is only sufficiently long for the development of a single generation, natural selection has rejected all deviation from the monocyclic development (even when provided with more favorable conditions experimentally) although some polymorphism in this character has been noted. In the south, the growth period of the vegetation and the overall temperatures are sufficient for the development of two to three generations per year. Populations of P. corni which live on plants that suppress the growth of the scale insect nymphs (such as Prunus) are monocyclic, whereas all such restrictions are removed when the scales occur on such plants as Gleditsia and Robinia. Another effect of the host plant is the complete disappearance of males when P. corni develops on arboreal Fabaceae. The selection of genes for polycyclicity should occur each time that the host plant is favourable and when the vegetative growth period is long. However, it is likely that the number of different types of populations within P. corni is determined primarily by the presence of the main bisexual population and several different parthenogenetic clones (Danzig, 1995). Biological differentiation of populations has also been established in the diaspididLepidosaphes ulmi (L.)(Danzig, 1959b; Garret, 1973; Bouchra, 1978; Gerson, 1990).
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INTRASPECIFIC VARIABILITY IN POPULATIONS OF THE COTTONY VINE SCALE PU! VINARIA VITIS (LINNAEUS)
Pulvinaria vitis, like P. corni, is widespread and polyphagous and, as in the latter species, the sex ratio and phenology vary depending on the host plant. On species of Betula, Alnus, Populus, Salix and Sorbus, both in Europe (Green, 1920; Schmutterer, 1952; Danzig, 1959) and in the Far East of Russia (Danzig, 1980, 1986), adult females occur in small colonies or as single individuals; on the other hand, males form large colonies of up to 100 individuals, all of which are the progeny of one female. Males and females tend to develop on different plants, separated from each other by large distances. Some colonies on Crataegus and Sarothamnus consisted of only females whilst others had only single females and numerous males (Schmutterer, 1952). Colonies of the cottony vine scale on Ribes in Europe (Newstead, 1903; Danzig, 1959a) and Siberia (Konopleva, 1980), and on Spiraea in Saldaalin (Danzig, 1980, 1986) consisted of both males and females and reproduction was mostly sexual. However, Newste.ad (1903) reported an alternation of sexual and parthenogenetic generations on Ribes, from England but this was after only one years' observations. According to different authors, the main hibernating stage on Ribes is either the second-instar nymph (Drozdovsky, 1960; Konopleva, 1980) or the adult female (Newstead, 1903), whilst on other plant genera, it is both the adult females and second-instar nymphs (Schmutterer, 1952; Danzig, 1959, 1980, 1986; Drozdovsky, 1960). The biology of this species has not been studied in detail in North America; there is only data about parthenogenetic development and on the hibernation of young females on Prunus (Phillips, 1963). It has been suggested (Signoret, 1873; Borchsenius, 1957) that the cottony vine scale from currants is a separate species, P. ribesiae Signoret, or a variety, P. vitis ribesiae Signoret (Newstead, 1903). This was because adult females off Ribes and Spiraea were on average smaller than females off Betula, although they showed no significant morphological differences in microscopic characters. Recently, Malumphy (1992)has shown that the morphological characters of P. vitis depend on the nutritional conditions and that these can be changed by transferring the insects from one plant to another. Malumphy also found considerable variation in the type of parthenogenesis in P. vitis, i.e. that different populations could have thelytoky, deuterotoky or diploid arrhenotoky. Thus, P. vitis appears to vary in a manner very similar to that described above for P. corni.
INTRASPECIFIC VARIABILITY IN OTHER COCCID SPECIES. Variation of the shape, size and colour of the adult female body and the dependence of this variability (although not always very strictly) on the host plants has been observed for many other polyphagous and widespread species of soft scale. Thus, several complexes of species have been described which are now considered to be synonyms of the following: Eulecanium douglasi (~ulc), Parthenolecanium persicae (Fabricius) and Saissetia coffeae (Walker) (Newstead, 1903; Danzig, 1980, 1986). Hadzibeyli (1967, 1977, 1983) has described host plant forms of the following species from Transcaucasia: Eupulvinaria peregrina Borchsenius, Coccus hesperidum Linnaeus, Coccus pseudomagnoliarum Kuwana, Eulecanium tiliae (Linnaeus) and Chloropulvinaria floccifera (Westwood). In the case of C. floccifera, although the transfer of the insects from one plant to another was accompanied by high mortality, it also led to a transformation of the external appearance of the insects into the shape characteristic of
Section 1.1.3.5 references, p. 210
Systematics
208
the recipient plant. In Eulecanium franconicum (Lindinger), which is oligophagous on Ericales, different morphs (Fig. 1.1.3.5.1) were described simultaneously and independently as separate species (Kawecki, 1961) and as food forms (Danzig, 1961). Although individual and geographic variation of microscopic characters of Coccidae have been reported by several authors in adult females (Blair et al., 1964; Hodgson, 1967, 1968, 1969; Hanford, 1974; Koteja, 1974; Ben-Dov et al., 1975; Ben-Dov, 1978)and also in adult males (Giliomee, 1967), the dependence of this variability on host plants has not been recorded.
Fig. 1.1.3.5.1. Eulecanium franconicum (Lindinger), adult female. B - from CaUuna vulgaris. (From Danzig, 1961).
A - from Vaccinium uliginosum.
Differences in the sex ratio on different plants has been observed in the Chinese wax scale, Ericerus pela Chavannes, an oligophagous coccid found on Oleaceae. On Fraxinus, a few females grow in a mass of males, while on Ligustrum females predominate. The Chinese, therefore, when growing this scale for wax production (see Section 1.2.3.2), need to maximise the number of eggs and, therefore, they grow the insects first on Ligustrum and then transfer the eggs to Fraxinus. In China, even 500 years ago, there were distinct and separate regions for the production of the eggs and the wax; the former were produced along the boundaries of the Yunnan and Szechwan provinces where Ligustrum grows well, whereas the wax was grown in the northeast where Fraxinus abounds. In order to achieve this, females with eggs were transported over distances exceeding 500 km (Lo, 1955). In addition to the effect of the host plant on E. pela, the climatic conditions can also significantly influence the sex ratio in some regions. Thus, in the Russian Far East, at the northern boundary of its range, males of E. pela are numerous whereas females only occur singly on a given plant (Danzig, 1980, 1986). Intraspecific variation similar to that in Parthenolecanium corni and Pulvinaria vitis (i.e. in the sex ratio and in the types of parthenogenesis) have been noted and examined in detail in Coccus hesperidum and Saissetia coffeae (Thomsen, 1927, 1929; Nur, 1979, 1980). Another reason for morphological variation in soft scales is parasitization by hymenopterous parasitoids (Danzig, 1980, 1986). For instance, parasitized females of Eulecanium paucispinosum Danzig differed from healthy ones in their larger size, darker colouration and lack of wrinkles on the body, which is smooth and glistening (Fig. 1.1.3.5.2). Adult female Pulvinaria crassispina Danzig from the Russian Far East infected with the parasitoid Encyrtus swederi (Dalman) (Hymenoptera, Chalcidoidea) differed from healthy ones in having markedly fewer tubular ducts and multilocular discpores and, more particularly, in the complete absence of a submarginal band of ventral tubular ducts (Fig. 1.1.3.5.3). In addition, there was a decline in the number of marginal setae and spiracular spines. These changes have a marked effect on the ability of the insect to reproduce. The function of the tubular ducts and multilocular disc-pores is to secrete wax for building the ovisac, while the wax from the multilocular disc-pores
209
Intraspecific variation of taxonomic characters
Fig. 1.1.3.5.2. Eulecanium (From Danzig, 1980).
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Fig. 1.1.3.5.3. P u l v i n a r i a c r a s s i s p i n a Danzig, adult female, taxonomic characters on venter. A - healthy. B - parasitised, showing the reduction in the frequency and distribution of most secretary organs. (From Danzig, 1980).
210
Systematics
also p r e v e n t s the eggs f r o m sticking together. T h u s , the overall effect o f p a r a s i t i z a t i o n is to p r e v e n t the secretion o f an ovisac, causing these individuals to b e c o m e sterile. It s h o u l d be n o t e d that n o t all adult females o f the g e n u s P u l v i n a r i a s h o w this r e d u c t i o n in g l a n d structures w h e n parasitised.
REFERENCES Asquith, D., 1949. Two generations of European fruit lecanium in Southern Pennsylvania. Journal of Economic Entomology, 42: 853. Bailey, S.F., 1964. A study of the European fruit lecanium scale, Lecanium corni, on prune. Journal of Economic Entomology, 57: 934--938. Ben-Dov, Y., 1978. Taxonomy of the nigra scale, Parasaissetia nigra (Nietner) (Homoptera: Coccidae), with observations on mass rearing and parasites of an Israeli strain. Phytoparasitica, 6(3): 115-127. Ben-Dov, Y., 1993. A Systematic Catalogue of the Soft Scale Insects of the World (Homoptera: Coccoidea: Coccidae) with Data on Geographical Distribution, Host Plants, Biology and Economic Importance. Flora and Fauna Handbook No. 9, Sandhill Crane Press, Gainesville, Florida; Leiden, Netherlands. 536 pp. Ben-Dov, Y., Williams, M.L. and Ray, C.H., 1975. Taxonomy of the mango shield scale, Protopulvinaria mangiferae (Green) (Homoptera: Coccidae). Israel Journal of Entomology, 10: 1-17. Bielenin, I., 1958. Budowa i wystepwania gruczlow grzbietowobrzezuych u larw II stadium Lecanium corni Bouchr, Marchal (? necd') (l-lomoptera, Coccoidea, Lecaniidae). Polskie Pismo Entomologiczne, 27(1): 97-104. Blair, C.A., Blackith, R.E. and Boratyfiski, K., 1964. Variation in Coccus hesperidum L. (Homoptera: Coccidae). Proceedings of the Royal Entomological Society of London (A), 39(7-9): 129-134. Blattny, C. and Novicky, S., 1926. Studie o puldici svetkove (Lecanium corni Bouchr). Sbornic vyzkumnych ustavu zemedelskych, 17:1-91. 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). Bouchra, G., 1978. Sur deux races biologiques distinctes chez Lepidosaphes ulmi L. (Homoptera, Coccoidea, Diaspididae). Comptes Rendus des Srances de l'Academie des Sciences, Paris, Srrie D, 286(18): 1313-1314. Canard, M., 1958. Recherches sur la morphologie et la biologic de la cochenille Eulecaniwn corni Bouch6 0-lomopt~res - Coccoidea). Annales de l'Ecole Nationale Suprricure Agronomique de Toulouse, 6(2): 185-271. Danzig, E.M., 1959a. On the scale insect fauna (l-lomoptera, Coccoidea) of the Leningrad region. Entomologicheskoe Obozrenie, 38(2): 443-455. (In Russian, with English abstract). Danzig, E.M., 1959b. On the biological forms of the oyster-shell scale, Lepidosaphes ulmi (L.) (Homoptera, Coccoidea). Zoologicheskii Zhurnal, 38(6): 879-886. Danzig, E.M., 1961. Food forms of Euleeanium franconicum (Lndgr.) (Homoptera, Cocooidea). Entomologicheskoe Obozrenie, 40(3): 571-576. (In Russian). Entomological Revue, 40(3): 310-313. Danzig, E.M., 1966. The reduction of wax-secreting dermal structures of the females of Pulvinaria Targ. (Homoptera, Coccoidea) infested by parasites. Zoologicheskii Zhurnal, 45:1488-1492. (In Russian, with English abstract). Danzig, E.M., 1980. Scale insects of the Far East of the USSR (Homoptera, Coccinea) with phylogenetic analysis of scale insect fauna of the world. Nauka Publishers, Leningrad, 363 pp. (In Russian). Danzig, E.M., 1986. Coccids of the Far-Eastern USSR (Homoptera, Coccinea). Phylogenetic analysis of Coccids in the world fauna. Oxonian press, New Dehli, Calcutta, 450 pp. Danzig, E.M., 1995. Intraspecific variation in the scale insects (Homoptera: Coccinea). Israel Journal of Entomology, 29: 19-24. Drozdovsky, E.M., 1960. Scale insects (Homoptera, Coccoidea) on fruit trees and berry shrubs in Moscow region. Izvestiya Timiryazevskoy sel'skokhozyayswennoy Akademii, 1(32): 193-208. On Russian). Dubrowskaya, N.A., 1959. On the number of generations in Parthenolecanium corni Bouch6 (Homoptera, Coccoidea, Coccidae). Zoologichesky Zhurnal, 38(9): 1366-1374. On Russian, with English abstract). Dziedzicka, A. and Sermak, W., 1967. The variability of the dorso-marginal glands in larvae H and females in Lecanium corni Bouch6 of Taxus baccata. 1. Rosznik Nauk-Dydactyczny WSP w Krakowie, 29:25-31. Ebeling, W., 1938. Host-determined morphological variations in Lecanium corni. Hilgardia, 11: 613-631. Garrett, W.T., 1973. Biosystematics of the oystershell scale, Lepidosaphes ulmi (L.) (Homoptera: Diaspididae) in Maryland. Dissertation Abstracts, International. Section B. 33(10): 4843-4844. Gerson, U., 1990. Biosystematics. In: D. Rosen (F,ditor). Armored Scale Insects, their Biology, Natural Enemies and Control. World Crop Pests, Elsevier, Amsterdam, Vol. 4A, pp. 129-134. Gill, R.J., 1988. The Scale Insects of California. Part 1. The Soft Scales (Homoptera" Coccoidea: Coccidae). California Department of Food and Agriculture - Technical Series in Agricultural Biosystematics and Plant Pathology, Number 1, 132 pp.
lntraspecific variation of taxonomic characters
211
Green, E.E., 1920. Observations on British Coccidae. No. V. The Entomologist's Monthly Magazine, 56:114-130. Giliomee, J., 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. Habib, A., 1957. The morphology and biometry of the Eulecanium corni-group, and its relation to host-plants (Hemiptera, Homoptera: Coccoidea). Bulletin de la Socirt6 Entomologique d'Egypte, 50(41): 381-410. Hadzibeyli, Z.K., 1967. Ecological peculiarities on the species genus Eulecanium Ckll. in the Georgian fauna. Trudy Instituta Zashchity Rasteniy Akademii Nauk Gruzinskoi SSR, 19: 59-63. (In Russian). Hadzibeyli, Z.K., 1977. Biology, morphology and trophical forms of some species of the tribe Pulvinariini (Homoptera, Coccoidea) in Georgia. Entomologicheskoe Obozrenie, 56(3): 546-550. (In Russian). Entomological Revue, 56(3): 39-41. Hadzibeyli, Z.K., 1983. The coccids (Homoptera, Coccoidea) of the subtropical zone of the Georgian SSR. Metsniereba, Tbilisi, 294 pp. (In Russian, English summary). Hamon, A.B. and Williams, M.L., 1984. The Soft Scale Insects of Florida (Homoptera" Coccoidea: Coccidae). Arthropods of Florida and Neighbouring Land Areas. Florida Department of Agriculture and Consumer Services, Division of Plant Industry, 11, 194 pp. Hanford, L., 1974. The African scale insect genus Udinia De Lotto (Coccidae). Transactions of the Royal Entomological Society of London, 126(1): 1-40. Hodgson, C.J., 1967. A revision of the species of Inglisia Maskell (Homoptera: Coccoidea) recorded from the Ethiopian Region. Arnoldia (Rhodesia), 3(23): 1-11. Hodgson, C.J., 1968. Further notes on the genus Pulvinaria Targ. (Homoptera: Coccoidea) from the Ethiopian Region. The Journal of the Entomological Society of South Africa, 31 (1): 141-174. Hodgson, C.J., 1969. The status of Hemilecanium imbricans (Green) (Homoptera: Coccoidea) in Africa south of the Sahara. Journal Natural History, 3: 321-327. Kawecki, Z., 1958. Studia nad rodzajem Lecanium Burm. 4. Materialy do monographii misecnica sliwowego, Lecanium corni Bouchr, Marchal (9 nee d') (Homoptera, Coccoidea, Lecaniidae). Annales Zoologici Warszawa, 17(9): 135-246. Kawecki, Z., 1961. A revision of the species of the genus Lecanium Burm. occurring in Poland and the description ofLecanium slavum sp. n. Verhandlungen XI International Kongress fiir Entomologie, Wien, 1960, 1: 65 -67. Konopleva, V.F., 1980. The cottony black-current scale. Zashchita Rasteniy, 11: 64. (In Russian). Koteja, J., 1979. Revision of the genus Luzulaspis Cockerell (Homoptera, Coccidae). Polskie Pismo Entomologiczne, 49: 585-638. Lo, Shen-siang., 1955. A test in transporting the female adults of the wax insect from Sikang to Szechwan. Acts Entomologies Sinica, 5(4): 445-461. Malumphy, C.P.J., 1992. A Morphological and Experimental Investigation of the Pulvinaria vitis Complex in Europe. Ph.D. thesis, Imperial College, University of London, 270 pp. Marchal, P., 1908. Notes sur les cochenilles de l'Europe et du Nord de l'Afrique. Annales de la Socirt6 Entomologique de France, 77: 221-309. Moshkov, B.S., 1961. Photoperiodism of plants. Moscow-Leningrad, 318 pp. (In Russian). Nakahara, S., 1981. The proper placements of the Nearctic soft scale species assigned to the genus Lecanium Burmeister (Homoptera: Coccidae). Proceedings of the Entomological Society of Washington, 83(2): 283-286. Newstead, R., 1903. Monograph of the Coccidae of the British Isles. Vol. 2. Ray Society, London, 270 pp. Nur, U., 1972. Diploid arrhenotoky and automictic thelytoky in soft scale insects (Lecaniidae: Coccoidea: Homoptera). Chromosoma (Berlin), 39: 381-401. Nur, U., 1979. Gonoid thelytoky in soft scale insects (Coccidae: Homoptera). Chromosoma (Berlin), 72: 89-104. Nur, U., 1980. Evolution of unusual chromosome systems in scale insects (Coccoidea: Homoptera). In: R.L. Blackman and M. Ashburner (Editors), Royal Entomological Society of London, 10th Symposium, Insect Cytogenetics, London, 24-25 September 1979. Blackwell, Oxford, pp. 97-117. Nuzzaci, G., 1969. Nots morfo-biologica sull Eulecanium corni (Bouch6) ssp. apuliae nov. Entomologica, 5: 9-36. 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(4): 372-407. Phillips, J.H.H., 1965a. Notes on species of Lecanium Burmeister (Homoptera: Coccoidea) in the Niagara Peninsula, Ontario, with a description of a new species. The Canadian Entomologist, 97(3): 231-238. Phillips, J.H.H., 1965b. Biological and behavioral differences between Lecanium cerasifex Fitch and Lecanium putmani Phillips (Homoptera: Coccoidea). The Canadian Entomologist, 97(3): 303-309. Richards, W.R., 1958. Identities of species ofLecanium Burmeister in Canada (Homoptera: Coccoidea). The Canadian Entomologist, 90(4): 305-313. Sanders, J.G., 1909. The identity and synonymy of our soft scale insects. Journal of Economic Entomology, 2: 428-448. Saakyan-Baranova, A.A., Sugonyaev, E.S. and Sheldeshova, G.G., 1 9 7 1 . Brown fruit scale (Parthenolecanium corni Bouch6) and its parasites (Chalcidoidea). The essay of the complex investigation of host-parasite relations. Nauka Publishers, Leningrad, 166 pp. On Russian).
212
Systematics
S/ivescu, A.D., 1943. Oecoarten bei Lecanium. Bulletin de la Section Scientifique de l'Academic Roumaine, 25 (1942-43): 212-223. S/ivescu, A.D., 1944. Formes dcologiques des ldcanides de la faune Roumaine. Bulletin de la Section Scientifique de l'Acadrmie Roumaine, 27 (4): 230-246. Signoret, V., 1873. Essai sur les cochenilles ou gallinsectes (Homoptera-Coccides). 10 pattie. Annales de la Socirtd Entomologique de France, Series 5, 3: 27-48. Schmutterer, H., 1952. Die Okologie der Cocciden (Homoptera, Coccidae) Frankens. 2 Abschnitt. ZeitschriR fiir Angewandte Entomologie, 34: 65-100. Suit, K., 1932. (~skoslovensk6 druny rodu puclice (gn. Lecanium, Coccidae, Homoptera). Acta Societatis Scientiarum Naturalium Moravicae, 7(5): 134. Suter, P., 1950. Zur biologie von Lecanium corni Bouch6 (Homopt., Coccid.). Bulletin de la Socirtd Entomologique Suisse, 23(2): 95-103. Thiem, H., 1933a. Beitrag zur Parthenogenese und Ph~nologie der Geschlechter yon Eulecanium corni Bouchd (Coecidae). Zeitschrift fiir Morphologie und ()kologie der Tiere, 27: 294-324. Thiem, H., 1933b. Sexual biologische Studien an der Zwetschen Schildlause (Eulecanium cornO. Forchungen und Forschritte, 9(34): 492-493. Thomsen, M., 1927. Studien fiber die Parthenogenese bei einigen Cocciden und Aleurodiden. Zeitschrift fiir Zellforsehung und Microscopische Anatomie, 5: 1-116. Thomsen, M., 1929. Sex-determination in Lecanium. Proceedings of the 4th International Congress of Entomology, Ithaca, 1928, 1: 18-24. Voukassovitch, P., 1930. Sur la polyphagie de la cochenille Lecanium corni L. Compte Rendu des Seances de la Socirt6 de Biologie, Paris, 104: 1065-1067. 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 Bulletin, 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.
213
1.1.3.6 Zoogeographical Considerations and Status of Knowledge of the Family FERENC KOZ~,R and YAIR BEN-DOV
INTRODUCTION The family Coccidae is the third richest in the Coccoidea in terms of species but, as with the other scale insect families, our taxonomic knowledge is far from complete. According to two detailed analyses of the scale insects of the Palaearctic region (Koz~r and Walter, 1985; Ko~r and Drozdj~, 1987), 17 % of all Coccoidea from this region were described as new between 1960-1980 (Fig. 1.1.3.6.1), 13 % of which were species of Coccidae. Considering that it is estimated that there are 12,000 species of scale insect (Miller and Kosztarab, 1979; Ko~r, 1990) and that 20% of these are thought to be Coccidae, it seems likely that this family could have 2,400 species, more than twice the number currently recognized. 221
20
239
3 2 3.....
I
I
I
I I
i I
I I 1569
5
! 1
Lepidoptera Papilionidea Danainae
Coleoptera
Cur culionidae
Homoptera Aleyrod~dea
Thysa nopte ra Coccoldea and Coccidae
Fig. 1.1.3.6.1. Bar-chart showing the percentage of known species described as new between 1960-1980 in five insect groups. Numbers above each bar refer to the actual number of species described in the group during this period; hatched bar refers to the family Coccidae only. Data for Coleoptera, Lepidoptera and Thysanoptera from Strong et al., 1984.
Section 1.1.3.6 references, p. 227
214
Systematics
The frequency of new genera described in the Coccidae since 1758 is shown in Fig. 1.1.3.6.2 and it is clear that there has been a steady increase, particularly in the cumulative total, with 11-24 new genera every 10 years since 1940. It is likely that this trend will continue in the future. Not only is our present knowledge of the taxonomy of the Coccidae very incomplete but there is little agreement amongst taxonomists with regard to the classification of the Coccidae; in addition, the distribution of the known species and genera is inadequately known. Any zoogeographical analysis is therefore difficult and must be regarded as preliminary. 150
=" r 100 r" (1)
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E z
5O
25
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e
1758-61,-71. 81- 911801-11- 21- 31- 41- 51- 61- 71- 81- 91-901-11- 21- 31- 41- 51- 61- 71- 81607080901800102030 4050607080901900102030405080 7 0 8 0 gO
Years
Fig. 1.1.3.6.2. Frequency of new genera described in the family Coccidae during the period 1758-1990. Where is the number of new genera for each 10 years period and 9 .... Q is the cumulative total (data taken from generic list of Hodgson, 1994).
The differing views on the phylogeny of the Coccoidea also affect our interpretation of the zoogeography of the Coccidae. Thus, the particular species richness of the Coccidae in the tropics (Borchsenius, 1957; Williams, 1984; Ben-Dov, 1993) suggests that the main evolution of this family occurred there and only subsequently spread to the more temperate regions. However, Miller and Gonzales (1975) suggested that the Coccidae had a common origin with the Eriococcidae, which Hey (1962) believed originated in the temperate areas of the Gondwana continent.
Zoogeographical considerations and status of knowledge of the family
215
A better understanding of the host-plant relationships of soft scales would also be very helpful. It is generally accepted that the gymnosperms and cryptogams have been colonised from the angiosperms by several polyphagous soft scale genera as well as by others that have specialized in particular taxa, such as Physokermes on Piceae and Pinus in the Holarctic, Stotzia on Ephedra in the southern Palaearctic and Toumeyella on Pinus and Magnoliaceae in the Nearctic. The Cyperaceae and Poaceae are hosts to about 40 % of both genera and species of soft scale in Central Europe (where the fauna is fairly well known) (Kosztarab and Koz~r, 1988). However, within the Palaearctic region as a whole, only about 20 % of the Coccidae species are found on these two plant families, approximately equally divided between the temperate and Mediterranean areas. In the Nearctic, however, only about 7% of species have been recorded from grasses and sedges (Gill, 1988) and these two plant families have been equally poorly studied in other zoogeographic regions. None-the-less, recent descriptions of new taxa of soft scales from the Australian and Nearctic regions (Brookes and Koteja, 1982; Koteja and Brookes, 1981; Koteja and Howell, 1979) suggest that the species richness on these plant groups could be much higher - perhaps equal to that in Central Europe. Another niche much favored by many soft scales in the Palaearctic is on roots of plants belonging to genera such as Artemisia, Dianthus and Erica, especially in dry environments. These plant genera are also hosts to other coccoid families in other zoogeographic regions and it is likely that further soft scales will be found on the roots of these and similar plants outside the Palaearctic. There is, therefore, a great need for further extensive collecting throughout the world. There are few useful published data concerning the zoogeography of this family. One of the most important contributions was that of Borchsenius (1957), who analyzed the data for the Palaearctic and compared it with data from elsewhere in the world. Some information is also given in Williams (1984). Regional and country data are to be found as follows: Palaearctic: Kosztarab and Koz~r (1988), Ko~r and Drozdj~ (1987), Koz~r and Walter (1985). Pacific: Williams and Watson (1990). China and Oriental region: Tang (1991), Varshney (1985, 1992). Far East USSR: Danzig (1980). Within the Holarctic - California: Gill (1988); Florida: Hamon and Williams (1984); Virginia: Williams and Kosztarab (1972). Central Europe: Kosztarab and Ko~r (1988). There are no monographs for the Ethiopian and Australian regions, although there is a fairly extensive literature for the former. The following section attempts to analyse these data to see if there are any world-wide patterns in the zoogeography of this family.
ZOOGEOGRAPHY OF THE COCCIDAE OF THE WORLD According to Ben-Dov (1993), the family Coccidae contained about 1088 species in 144 genera, while Hodgson (1994) divided them among 160 genera. Earlier estimates include those of Eastop (1978), who had suggested 1162 species based on data in the Natural History Museum, London, Borchsenius (1957) with about 900 species and 100 genera, Kosztarab and Ko~r (1988) with about 1000 species and 100 genera and Tang (1991) with 928 and 139 species and genera respectively. The species and genetic richness for each region are shown in Fig. 1.1.3.6.3 and Table 1.1.3.6.1, based on Ben-Dov's (1993) Systematic Catalogue of the Coccidae of the World. These show that the richest regions are the Palaearctic and Neotropical, containing about 50% of known Coccidae, many of them endemic to these regions.
Section 1.1.3.6 references, p. 227
I
I
,
Fig. 1.1.3.6.3. Number of genera and species of Coccidae known from each zoogeographic region in 1990 (data from Ben-Dov, 1993).
I
217
Zoogeographical considerationsand status of knowledge of thefamily
Some genera, such as Lecanopsis, Exaeretopus, Eriopeltis and Luzulaspis, are considered to be phylogenetically old. On the other hand, the Ethiopian region harbours only about 20% of known species, followed by the Oriental region with only 8.1%. However, the ratio of genera to species differs between regions (Table 1.1.3.6.1), with the highest ratios (most species per genus) being found in the Neotropical, Palaearctic and Ethiopian regions. Table 1.1.3.6.1 also shows that the highest percentage (31%) of endemic genera is found in the Palaearctic, where the number of endemic species is higher than 80%. However, these high percentages could be the result of the more intensive exploration of the Palaeractic; further intensive study of other regions, such as the supposedly richer Ethiopian and Neotropics, might change these figures considerably. In the superfamily Coccoidea, comprising some 6000 species in 800 genera (Kosztarab and K o ~ r , 1988), the ratio of species to genera is 7.5:1, almost identical to the mean of 7.6:1 for the Coccidae. Comparing zoogeographic regions individually, the highest species:genus ratios are in the Neotropical, Palaearctic and Ethiopian regions, suggesting a high rate of speciation in these areas, especially on widely distributed woody plants. Species-rich soft scale genera include Ceroplastes, Coccus, Eulecanium, Pulvinaria and Saissetia. On the other hand, the Neotropical and Ethiopian regions have few soft scale genera which have evolved on either grasses or on relatively rare, non-apparent, perennial herbaceous plants. These genera are all highly specialize~, monotypic or containing few species which generally infest subterranean parts of plants. Perhaps conditions in the humid tropics are less favourable than in the drier ecosystems of the Palaearctic, such as in the deserts, semideserts, dry subtropical and Mediterranean forests, which are so species rich.
TABLE 1.1.3.6.1 The frequency of Coccidae in 9 zoogeographicalregions, where 'Total endemic species' includes species not found in endemic genera. Geographic regions
Palaearctic Nearctic Neotropical Ethiopian Oriental Australian News Zealand and Pacific Austro-Oriental Madagasian Total (World)
Number of Genera Species
Ratio of genera to species
Number of genera endemic to region Number of Genera Species in these genera
Total endemic species
58 27 51 48 44 23
299 105 298 251 126 73
1:5.2 1:3.9 1:5.8 1:5.2 1:2.9 1:3.2
28 1 20 18 6 5
78 1 26 47 6 18
244 48 247 211 80 54
18 28 20 144
60 99 43 1088
1:3.3 1:3.5 1:2.2 1:7.6
1 5 2 86
2 7 3 188
23 61 17 985
The rate at which new genera have been described can also be instructive (Fig. 1.1.3.6.4). It is clear that extensive taxonomic work has been done in the Palaearctic, Ethiopian and Oriental regions in the last 4-5 decades. On the other hand, very few new genera have been described in the 20th century from such regions as the Nearctic. As this area has been well explored, it may have a poor soft scale fauna. Other regions, such as the Neotropical and Australian, have a rich soft scale fauna, and the few descriptions of new genera reflects the low level of taxonomic activity during
Section 1.1.3.6 references, p. 227
Systematics
218
the 20th century. Recent observations from the Pacific region (Williams and Watson, 1990) support this view.
CHARACTERIZATION OF THE ZOOGEOGRAPHICAL REGIONS a. Palaearctie. While K o ~ r and Walter (1985) reported only 55 genera and 274 species in this region, Ben-Dov (1993) recorded 58 genera with 299 species. This region, therefore, has the richest fauna but this may be because it is the best explored. However, even within this area, a number of new species have been described in recent decades (Fig. 1.1.3.6.5), indicating that the fauna remains incompletely known. In a further analysis of the diverse environmental conditions prevailing in the Mediterranean subregion (Fig. 1.1.3.6.6), Koz~r and Drozdja'k (1987)concluded that this area was rich in Coccoidea but poor in soft scales. The Palaearctic region is characterized by several monotypic genera, such as Acantholecanium, Bodenheimera, Cajalecanium, Chlamydolecanium, Ericerus, Filippia, Hadzibejliaspis , Lecaniococcus , Leptopulvinaria , Mitrococcus , Phyllostroma , Psilococcus, Pulvinarisca, Sphaerolecanium and Takahashia. Also very characteristic are species of Parafairmairia, Psilococcus and Vittacoccus which live on sedges, Exaeretopus, Lecanopsis and Scythia on grasses, Stotzia on Ephedra sp., Rhodococcus on Rosaceae, Rhizopulvinaria on Caryophillaceae and Nemolecanium on Pinaceae. Some of these genera are considered to be phylogenetically primitive (Borchsenius, 1957). These data suggest that soft scales have evolved in a wide range of different environments. In the colder, more humid habitats, there are genera with few species, such as Psilococcus and Vittacoccus and others which are species rich (e. g. Luzulaspis). Still other genera, such as Scythia, live on grasses in the open steppes and others on bushes and the roots of perennial herbs in the Mediterranean region (e.g. Lecanopsis, Rhizopulvinaria and Stotzia). On the other hand, species in genera that live on trees and woody plants are less specialized and tend to be widely distributed, such
as Eulecanium and Parthenolecanium. The total species richness of this region, including cosmopolitan species, is shown by a number of genera - 35 spp. of Eulecanium on woody plants, 14 of Lecanopsis on grasses, 12 of Luzulaspis on sedges, 63 of Pulvinaria on trees and shrubs and 32 of Rhizopulvinaria on the roots of herbs.
b. Nearctic. The soft scale fauna of this region appears to be poor. Hamon and Williams (1984) listed only 25 genera with 85 species and Ben-Dov (1993) 27 genera with 105 species. However, the poorness of the fauna could be due to incomplete data, as suggested by the discovery of three new species of Luzulaspis (Koteja and Howell, 1979), indicating that genera typical of boreal and steppe environments in the Palaearctic might also be present in the Nearctic. The majority of species of Nearctic soft scales are typically found on trees and shrubs. Particularly characteristic genera are ToumeyeUa and Neolecanium, living on pine and magnolias respectively, while the only monotypic genus appears to be Pseudophilippia. The fauna also includes some widely distributed genera with numerous species, such as Ceroplastes with 11 spp., Coccus with 7 spp. and Pulvinaria with 23 spp., all typical of woodland and shrubs (Gill, 1988).
219
Zoogeographical considerations and status of knowledge of the family
PALAEARCTIC
10"
"
,~
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IL~
NEARCTIC 5
,
O
,
,
-
.
.
.
.
.
.
.
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ETHIOPIAN
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ORIENTAL
;.=-,- , , -, , 2, 3 , - , , 5, ~, 7 , - .J, ..1750~1-71" 01-91-1~1-11-;1- ;1-11- ~,"" o, '" 7, o~- ~, , ~ , , O0 70 Bogo'lSO0 1 0 2 0 3 0 4 0 ~ 0 a'O 70 BO l~O'lgO0 102:0 3 0 4 0 5~) ~ ) 70 8 0 0 0
g.l
Years
Fig. 1.1.3.6.4. Number of new genera described in the Coccidae in five geographic regions for each 10 year period from 1830 to 1990 (data from Hodgson, 1994).
220
Systematics
25 T
150
(n (9 u
.....
Q. u) ,<.,,.
0 Is,.
t-~ lOO
0
E z
50
25
1758-61- 71- 81- 91-1801-11- 21- 31-41- 51-61- 71- 81-91-1901-11-21-31- 41- 51- 61- 71- 816070 80 901800 1 0 2 0 3 0 4 0 5 0 60708090190010203040 5060708090
Years
Fig. 1.1.3.6.5. Frequency of new soft scale species described in the Palaearctic region, 1758-1980 , where is the number per 10 year period and 9 9 is the cumulative total (data from Kozair and Walter, 1985).
e. Neotropics. Fifty-one genera comprising 298 species are known from this region (Ben-Dov, 1993). The scale insect fauna tends to be specialized and rich, with a number of monotypic, apparently endemic genera, such as Alecanochiton, Anopulvinaria,
Cyclolecanium, Edwallia, Eutaxia, Megalecanium, Millericoccus, Neolecanochiton, Parapulvinaria, Platinglisia, Pseudalichtensia, Pulvinella and Stictolecanium (Ben-Dov, 1993; Borchsenius, 1957). The Neotropics are also species rich, particularly in some of the more cosmopolitan genera, e.g., Ceroplastes (73 spp.), Coccus (12 spp.), Eucalymnatus (13 spp.)and Saissetia (17 spp.), most of which are typical of woody plants. Few species are known from grassland and semidesert environments and these niches clearly need to be further explored - indeed the whole continent neexls more attention as almost all records are from a relatively small area of Brazil.
Zoogeographical considerations and status of knowledge of the family
221
EURO-SIBERIAN
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IRANO-TURANIAN
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1758"61- 71" 81-91-1801-11- 2'1- 31- 4'1- 5'1- 61" 7'1- I/1- 91-1901-11- 21- 31-41- t~- (~1- 1~1- Years oo 7o eo 9 o ~ o
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Fig. 1.1.3.6.6. Number of soR scale species from four subregions of the Palaearctic described during each 10 year period, 1758-1980 (data from Koz~r and Drozdj~ik, 1987).
Section 1.1.3.6 references, p. 227
222
Systematics
d. Ethiopian. Forty-eight genera containing 251 species have been recorded from this region (Ben-Dov, 1993). Several genera are monotypic and probably endemic, such as Allopulvinaria, Cissococcus, Conofilippia, Couturierina, Cryptinglisia, Cyphococcus, Idiosaissetia, Kozaricoccus , Membranaria, Mesembryna and RichardieUa (Ben-Dov, 1993; Borchsenius, 1957). However, many widespread genera are species rich in this region, such as Ceroplastes (40 spp.), Coccus (33 spp.), Etiennea (20 spp. but only in Africa), Pulvinaria (22 spp.) and Saissetia (22 spp.) (Ben-Dov, 1986, 1993; De Lotto, 1959, 1965, 1978; Hodgson, 1968, 1969a, b, 1991). In general, whilst some genera and some geographic areas within this region are well explored, others are not and considerable further study is still required. e. Oriental. Forty-four genera and 126 species (Ben-Dov, 1993; Varshney, 1985, 1992) have been reported from this region, although Tang (1991) recently recorded 39 genera and 83 species from China and nearby territories. This region also has many monotypic genera, e.g., Ericeroides , Metaceronema, Paracardiococcus , Paractenochiton, Podoparalecanium and Taiwansaissetia, some of which are considered to be endemic (Borchsenius, 1957). In addition, the Oriental region has several species-rich genera - Ceroplastes (8 spp.), Coccus (23 spp.), Paralecanium (13 spp.), Pulvinaria (16 spp.) and Saissetia (5 spp.) (Ben-Dov, 1993). However, only China, India and Sri Lanka have been more or less explored (Varshney, 1985, 1992; Tang, 1991). Varshney (1985, 1992)suggested that there might have been two centres of genetic evolution, one in the humid north-east of India, where Chinese, Indian and Malaysian elements meet, and the other in the dry lowland forest, plains and ephemeral habitats of southern India. The other areas within this region all need further exploration. L Australian. There is no comprehensive work on the Coccidae for this region, although Borchsenius (1957) considered that only 80 species in 20 genera had been recorded at that time. More recently, Ben-Dov (1993) listed 73 species in 23 genera, including several endemic genera, such as Alecanopsis (8 spp.), Austrolichtensia (1 sp.), Cryptes (2 spp.), Symonicoccus (6 spp.) and Waricoccus (1 spp.). This region needs further study and will surely be found to contain many more genera and species, particularly on grasses and herbs, as indicated by the discovery of Symonicoccus and Waricoccus (Brooke,s and Koteja, 1982; Koteja and Brookes, 1981). g. Pacific. According to Williams and Watson (1990), this region has 46 species belonging to 19 genera, most of which are probably of tropical origin, but also including one genus, Anthococcus, known only from this area. The most species rich genera are Ceroplastes (9 spp.), Coccus (7 spp.), Milviscutulus (4 spp.), Pulvinaria (5 spp.) and Saissetia (5 spp.) (Williams and Watson, 1990). h. New Zealand. Based on present knowledge, the soft scale fauna of this region appears to be poor, with only 5 genera and 22 species (Eastop, 1978). However, the Coccidae of this area are currently being revised (C.J. Hodgson and R. Henderson, personal communication) and it is clear that it is rather richer (with perhaps 50 species), although most of them are endemic; at least half the genera are introduced and cosmopolitan. Only Oenochiton, with perhaps as many as 20 species, is well represented (Hodgson, C.J., personal communication). However, the Eriococcidae and Pseudococcidae are abundant. i. Madagasian. Few data are available for Madagascar. Ben-Dov (1993) records only 43 species in 20 genera in this family, including the genus Antandroya, which resembles the Eriococcidae and which was considered by Williams (1984) to perhaps
Zoogeographical considerationsand status of knowledge of thefamily
223
represent the most primitive species of Coccidae (Williams, 1984). Only one genus, Suareziella, is monotypic (Ben-Dov, 1993). However, the poor data do not allow a discussion of the place of this region in Coccidae zoogeography. j. Austro-Oriental. This zoogeographic region was included by Ben-Dov (1993) in his Systematic Catalogue of Soft Scales and appears to be characterized by several monotypic genera, such as Alecanium, Anthococcus, Halococcus and Myzolecanium. This region contains large numbers of species in following genera: Ceroplastes (12 spp.), Coccus (21 spp.) and Paralecanium (15 spp., of which 14 appear to be restricted to this region).
CONNECTIONS BETWEEN REGIONS Based on the data in Ben-Dov (1993), 84 genera appear to be restricted to a single region, 42 to two or three regions and 19 have a world-wide distribution - i.e. are known from more than 3 regions. This data is used below to try and identify connections between the different centres of genetic diversification of soft scales (Fig. 1.1.3.6.7). The Palaearctic region shows some connection with the Nearctic region, sharing the genera Eriopeltis, Exaeretopus, Neopulvinaria and Physokermes (Fig. 1.1.3.6.7), whilst such widely distributed genera as Eulecanium, Parthenolecanium and Pulvinaria have the largest number of endemic species here (Table 1.1.3.6.2). Indeexl, even a few species are shared between these two regions, such as Eulecanium tiliae (L.), Parthenolecanium corni (Bouchr), Physokermes piceae (Schrank) and Pulvinaria vitis (L.). On the other hand, the connection between the Palaearctic and Oriental is less obvious, with only Dicyphococcus and the monotypic genera Metaceronema and Pseudopulvinaria occuring in both. There is also a strong connection between the Mediterranean sub-region of the Palaearctic and the Ethiopian region. These share such genera as Cryptinglisia, Messinea and Stotzia. The Ethiopian and Madagasian regions have the genera Mametia and Trijuba. The Madagasian region also shows some connection with both the Ethiopian and Palaearctic regions through the genera Parafairmairia and Waxiella. In addition, the genera Hemilecanium, Marsipococcus and Neoplatylecanium are shared between the Ethiopian and Oriental regions. Connections can also be seen with regard to species richness in the most cosmopolitan genera. Thus, the largest number of endemic species in Ceroplastes, Lichtensia and Saissetia are found in the Neotropical and Ethiopian regions, while large numbers of Coccus species occur in the Ethiopian, Neotropical, Oriental and Austro-Oriental regions. The Nearctic and Neotropical regions share such genera as Mesolecanium, Metapulvinaria, Philephedra and Pseudokermes, while the Oriental and Austro-Oriental regions have Neosaissetia and Xenolecanium (Fig. 1.1.3.6.7) and a number of species of cosmopolitan genera. Connection between the Australian region and New Zealand are obscure but may be through the genus Ctenochiton when this is better known. Inglisia, which has an apparently wide distribution, is actually a monotypic genus restricted to New Zealand (C.J. Hodgson and R. Henderson, personal communication). The fauna of New Zealand appears to be remarkably isolated.
Section 1.1.3.6 references, p. 227
TABLE 1.1.3.6.2 A list of 19 cosmopolitan genera, i.e. which include one or more species known from at least 3 zoogeographical regions. Number of species apparently restricted to respective region
Genera Akennes Ceroplastes Ceroplasiodes coccus
Ctenochiton Eucalymnaiur Eulecanium Inglisia Kilifia Lichtensia Milviscutulur Paralecanium Parasaissetia Panhenolecanium Platylecanium Proiopulvinaria Puivinaria Saissetia Vimonia
Total
Palaearctic
0 4 0 3 0 0 32 0 2 1 0 1 0 7 I 1 53 4 0 109
Nearctic
Neotropic
0
8 73 4 12 1 13 6
Ethiopian
Oriental
Australian
0 2 0 0 13 0 0
1 2 1 13 3 0 0 1 0 0 0 11 0 0 2 0 12 1 0
2 1 1 3
0 3 0 1 0 0 0 0 19 18 0
1 34 2 25 0 0 2 6 0 7 0 0 3 0 0 0 15 18 0
21
159
113
47
0
1 0 0 0 5 0 0 0
0 0
1
New Zealand and S. Pacific
Number of species Total number known from more of species one region in genus AustroOriental
Madagasian
0 0 0 3 0 0 1 0 5 1 0
0 0 11 0 0 5 0 0 0 1 0 1 0 0 1 1 0
0 5 0 13 3 0 0 1 1 0 1 14 0 0 5 0 2 1 1
0 2 0 1 0 0 0 0 0 1 0 0 1 0 0 0 3 1 0
27
20
47
9
7 0 2 1
0 0
0 17 1 14 0 1 3 2 3 0 2 2 1 3 1 2 15 5 1
12 138 10 84 25 14 50 17 6 12 3 33 5 13 10 3 138 50 2 625
Zoogeographical considerations and status of knowledge of the family
225
CENTRES OF DIVERSIFICATION OF LARGE COSMOPOLITAN GENERA There are 19 genera of soft scales which are distributed in more than three regions and these are treated here as cosmopolitan (Table 1.1.3.6.2). This small group of genera contains more than half (625 spp.) of all known Coccidae. However, of these species, only 73 are distributed in more than one region and most are endemic to one of the regions (Table 1.1.3.6.2). Of the species in these cosmopolitan genera, most belong to five genera and these are treated separately below. i. Pulvinaria and related genera. According to Malumphy (1991), the tribe Pulvinariini consists of 24 genera and 205 species, but Ben-Dov (1993) included 138 species in the genus Pulvinaria. There is no agreement between coccidologists on the classification of this tribe, and some workers put almost all species into Pulvinaria itself, while others accept the classification of Borchsenius (1957) who split Pulvinaria into some eight to ten genera (Ben-Dov, 1993; Malumphy, 1990; Qin and Gullan, 1992; Williams and Watson, 1990; Hodgson, 1994). The largest number of species of Pulvinaria (sensu lato) (about 53) is found in the Palaearctic (Ben-Dov, 1993), especially the eastern part, which may be the centre of speciation of this group, with the species living on the foliage perhaps evolving in the humid areas and the species found in other microhabitats evolving in the drier environments. In the Mediterranean subregion and in Central Asia, the root-infesting genus Rhizopulvinaria is richly represented by about 32 species (Ben-Dov, 1993). The Neotropical, Ethiopian and Oriental regions each have 12-19 species of Pulvinaria but many of these are probably not congeneric with Pulvinaria (sensu stricto). Perhaps the cotton-like ovisacs typical of species of the Pulvinariini, which cover only the eggs and not the female, are most advantageuos in more temperate areas, while ovisacs which cover the whole body of the female, such as in most Filippiinae, could have an evolutionary advantage in both dry and humid environments.
ii. Ceroplastes and related genera. The Ceroplastinae contains about 138 species (Ben-Dov, 1993), of which 73 appear to be endemic to the Neotropics, 34 to the Ethiopian region and only very few (4-5) in other regions. Those recorded from the Mediterranean part of the Palaearctic and from the Nearctic are mostly introduced, cosmopolitan species. The dense wax cover and the fact that most species are monovoltine suggests that this group originally evolved in a very dry climate. iii. Coccus. This genus contains about 84 species (Ben-Dov, 1993). The richest fauna is found in the Ethiopian (25 spp.), Oriental (13) and Austro-Oriental regions (13) (Ben-Dov, 1993). The Neotropics currently has only 12 local Coccus species but it is likely that many more species will be discovered. The lack of protection to the rather elastic body of the adult females of this genus and their continuous, multivoltine development without a diapause, suggests that Coccus probably evolved in the very humid tropics. iv. Saissetia. This world-wide genus contains 49 species (Ben-Dov, 1993), with the largest number in the Ethiopian and Neotropical regions (18 and 17 respectively). The hard sclerotised dorsum of the females gives good protection in dry tropical and subtropical conditions and these areas could have served as centres for evolution. V. Eulecanium. Most of the 50 species of Eulecanium are known from the Palaearctic (32 spp.), which seems to have been the center of evolution for this genus. Other species are known from the Nearctic (5 spp.) and from the Neotropics (6 spp.).
Section 1.1.3.6 references, p. 227
I
~
I
____
I
I
~~
Fig. 1.1.3.6.7. Number of genera and species of Coccidae shared by two geographic regions. The data for Australia and New Zealand are too few for useful comparison.
Zoogeographical considerations and status of knowledge of the family
227
Several other cosmopolitan genera have a large number of species in one region but also have a few elsewhere (Table 1.1.3.6.2). Examples are Akermes and Eucalymnatus in Neotropics, Parthenolecanium in the Palaearctic and Platylecanium in the Austro-Oriental region.
REFERENCES Ben-Dov, Y., 1986. Taxonomy of two described and one new species of Waxiella De Lotto (Homoptera: Coccoidea" Coccidae). Systematic Entomology, 11" 165-174. Ben-Dov, Y., 1993. A Systematic Catalogue of the SoR Scale Insects of the World (Homoptera: Coccoidea: Coccidae) with Data on Geographical Distribution, Host Plants, Biology and Economic Importance. Sandhill Crane Press, Inc., Gainesville, Florida ~nd Leiden, The Netherlands. 536 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). Brookes, H.M. and Koteja, J., 1982. Waricoccus parvisetosus gen. et sp. n. (Homoptera, Coccidae) from Australia. Polskie Pismo Entomologiczne, 52: 183-187. Danzig, E.M., 1980. Coccoids of the Far East USSR. With a Phylogenetic Analysis of the Coccoid Fauna of the World. Nauka, Leningrad. 367 pp (in Russian). De Lotto, G., 1959. Further notes on Ethiopian species of the genus Coccus (Homoptera: Coccoidea: Coccidae). Journal of the Entomological Society of Southern Africa, 22: 150-173. De Lotto, G., 1965. On some Coccidae (Homoptera), chiefly from Africa. Bulletin of the British Museum (Natural History) Entomology, 16: 177-239. De Lotto, G., 1978. The soft scales (Homoptera: Coccidae) of South Africa, HI. Journal of the Entomological Society of Southern Africa, 41: 135-147. Eastop, V.F., 1978. Diversity of the Sternorrhyncha within major climatic zones. Symposia of the Royal Entomological Society of London, 9: 71-88. Gill, R.J., 1988. The Scale Insects of California, Part 1. The Soft Scales (Homoptera: Coccoidea: Coccidae). California Department of Food and Agriculture, Sacramento, California, 132 pp. Hamon, A.B. and Williams, M.L., 1984. Arthropods of Florida and Neighboring Land Areas, vol. 11. The soft scales of Florida (Homoptera: Coccoidea: Coccidae). Florida Department of Agriculture & Consumers Services. Contribution no 600. Florida Department of Agriculture, Gainesville, 194 pp. Hodgson, C.J., 1968. Further notes on the genus Pulvinaria Targ. (Homoptera : Coccoidea) from the Ethiopian region. Journal of the Entomological Society of Southern Africa, 31: 141-174. Hodgson, C.J., 1969a. Notes on Rhodesian Coccidae (Homoptera: Coccoidea), II. Arnoldia (Rhodesia) 40): 1-43. Hodgson, C.J., 1969b. Notes on Rhodesian Coccidae (Homoptera. Coccoidea), HI. Arnoldia (Rhodesia) 4(4): 1-42. Hodgson, C.J., 1991. A revision of the scale insect genera Etiennea and Platysaissetia (Homoptera: Coccidae) with particular reference to Africa. Systematic Entomology, 16: 173-221. Hodgson, C.J., 1994. The Scale Insect Family Coccidae: an Identification Manual to Genera. CAB International, Wallingford, 639 pp. Hoy, J.M., 1962. Eriococcidae (Homoptera: Coccoidea) of New Zealand. New Zealand Department of Scientific and Industrial Research Bulletin, 146: 1-219. Kosztarab, M. and Koz~r, F., 1988. Scale Insects of Central Europe. Akad6miai Kiad6, Budapest, 456 pp. Koteja, J. and Brooks, H.M., 1981. Symonicoccus gen. n., with five new Australian species (Homoptera, Coccidae). Polskie Pismo Entomologiczne, 51: 377-392. Koteja, J. and Howell, J.O., 1979. Luzulaspis Cockerell (Homoptera: Coccidae) in North America. Annals of the Entomological Society of America, 72: 334-342. Koz~ir, F., 1990. Why are there so few scale insects (Homoptera: Coccoidea). Proceedings of the 6th International Symposium of Scale Insect Studies, Cracow, August 6-12, 1994, Part II: 13-17. KozAr, F. and Drozdj~k, J., 1987. Some questions concerning the knowledge of Palaearctic Coccoidea (Homoptera). Bolletino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', 43 (Suppl.): 97-105. Koz~r, F. and Walter, J., 1985. Check-list of the Palaearctic Coccoidea (Homoptera). Folia Entomologica Hungarica, 46: 63-110. Malumphy, C.P., 1991. A morphological and experimental investigation of the Pulvinaria vitis complex in Europe. Ph.D. Thesis, University of London. 270 pp. Miller, D.R. and Gonzales, R.H., 1975. A taxonomic analysis of the Eriococcidae of Chile. Revista Chilena de Entomologia, Santiago, 9: 131-163. Miller, D.R. and Kosztarab, M., 1979. Recent advances in the study of scale insects. Annual Review of Entomology, 24: 1-27. Qin, T.K. and Gullan, P.J., 1992. A revision of the Australian Pulvinariini soft scales (lnsecta: Hemiptera: Coccidae). Journal of Natural History, 26: 103-164.
228
Systematics Strong, D.R., Lawton, J.H. and Southwood, T.R.E., 1984. Insects on Plants. Community Patterns and Mechanisms. Blackwell Scientific Publications, Oxford-London. 313 pp. Tang, Fang-tch, 1991. The Coccidae of China. Shanxi United Universities Press, Shanxi. 377 pp. Varshney, R.K., 1985. A review of Indian coccids (Homoptera: Coccoidea). Oriental Insects, 19: 1-101. Varshney, R.K., 1992. A check-list of the scale insects and mealybugs of South Asia. Part I. Records of the Zoological Survey of India, Occasional Paper No. 139: 1-152. Williams, D.J., 1984. Some aspects of the zoogeography of scale insects (Homoptera: Coccoidea). In: Z. Kaszab (Editor), Verhandlungen des Zehntcn Internationalen Symposiums iiber Entomofaunistik Mitteleuropas (SIEEC), 15-20 August 1983, Mtizrdk K6zm~vel6ddsi Kiad6, Budapest, pp 331-333. Williams, D.J. and Watson, G.W., 1990. The Scale Insects of the Topical South Pacific Region. Part 3, The Soft Scales (Coccidae) and other Families. CAB International, Wallingford, 267 pp. Williams, M.L. and Kosztarab, M., 1972. Morphology and systematics of the Coccidae of Virginia with notes on their biology (l-lomoptera: Coccoidea). Virginia Polytechnic Institute and State University, Research Division Bulletin, 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.
229
1.1.3.7 Phylogeny DOUGLASS R. MILLER and CHRIS J. HODGSON
INTRODUCTION The use of cladistic analyses to determine possible relationships within the Coccoidea have been few (Miller, 1984 (major portions of the Coccoidea); Miller and Miller, 1993a, 1993b (Eriokermes and Puto); Foldi, 1995 (Limacoccus); Miller and Williams, 1995 (Micrococcidae); Miller and Williams, 1995 (adult males of the ToumeyeUa group); Qin and Gullan, 1995 (Ceroplastinae); Hodgson and Henderson, 1996 (Eriochiton)), although several non-cladistic phylogenies have been suggested (Borchsenius, 1958 (based mainly on adult female characters); Boratyfiski & Davies, 1971 (based on adult male characters); Koteja, 1974 (based on the structure of the adult female mouthparts); Miller & Kosztarab, 1979 (a version of Boratyriski & Davies (1971) modified on the basis of more recent descriptions of males); Danzig, 1986 (using the morphology of the adult female, adult male and crawler and also life history characters) and Koteja (in Kosztarab & KozAr, 1988). Few classifications have been suggested for the family Coccidae and none have been based on phylogenetic analyses. The most recent classifications are those of Tang et al. (1990), Tang (1991) and Hodgson, 1994a. The first two papers by Tang proposed a rather complex classification based entirely on female characters. Most of the genetic groupings suggested are very different from those given in the studies of males (Giliomee, 1967), (Miller and Williams, 1995a). Hodgson (1994a) introduced a classification based on the adult morphology of both males and females. He divided the Coccidae into 10 subfamilies, with the Coccinae divided into four tribes; he suggested that the status of these groupings needed further study. This classification is summarised in Table 1.1.3.4.4 and is the basis of the cladistic study outlined below; the following analysis also studied the sister-group relationships of families within the Coccoidea thought to be closest to the soft scales. The only previous phylogenetic analyses which included a range of taxa within the Coccidae is that of Qin (1993) which remains unpublished (see the discussion below) and Miller and Williams (1995a). For a detailed outline of earlier classifications, see Section 1.1.3.4.
METHODOLOGY Exemplar taxa were chosen for each of the higher-level taxa in the Coccidae classification provided by Hodgson (1994a). Particular families were chosen as outgroups from those suggested by previous studies to be closely related to the Coccidae. The family Pseudococcidae was also chosen as an outgroup since there is general agreement that it is outside of the Coccidae. In many instances it was necessary to score characters for an exemplar taxon using the adult males, adult females and first instars of two or more different species. We recognize that this is a serious problem because
Section 1.1.3.7 references, p.
242
230
Systematics
the mosaic of characters given for a conglomerate of species do not exist in nature. Unfortunately, we were forced to use this strategy because data on exemplar species that included all three instars generally do not exist. Data were gathered either from published information or from direct examination of specimens (Appendix 1.1.3.7.1,A). The characters and character-states used are presented in Appendix 1.1.3.7.1,B and the matrix of character-states for each taxon is shown in Appendix 1.1.3.7.1,C. Unknown and ambiguous characters (e.g., thoracic characters in wingless males) are scored as a dash. Phylogenetic analyses were performed using PAUP 3.1.1 (Swofford, 1993). MacClade 3.01 (Maddison and Maddison, 1992) was used to examine the trees and study character distribution. The various analyses were produced using the PAUP Heuristic search, with 500 random-addition sequence replicates. The selected successive-weighting protocol was weights of 0 to 1,000. The original data matrix contained about 250 characters but these were reduced to 105 characters by eliminating characters that were either autapomorphic or did not apply to the taxa finally included in the analyses. Outgroup comparison was used to determine the polarity of characters and all multistate characters were treated as unordered. Determination of convergences and reversals when the state of an hypothesised lineage was given in MacClade as equivocal was done by assuming that the equivocal character-state was the same as the adjacent unequivocal state lower on the tree, i.e. DELTRAN (see Maddison and Maddison, 1992).
RESULTS AND DISCUSSION Analysis of the complete data set produced 14 equally parsimonious trees (Length [number of steps or changes] = 479, CI [consistency index] = 33, RI [retention index] = 52)when the Aclerdidae, Asterolecaniidae, Cerococcidae, Eriochiton, Eriococcidae, Kermesidae, Lecanodiaspididae, Micrococcidae, Pseudococcidae, Stictococcidae and Tachardiidae were used as the outgroup. A single tree was produced using successive weighting (Fig. 1.1.3.7.1) (CI=46, RI=68) and this was used as the hypothesis of relationships for the Coccidae. The 50% consensus tree is identical except Cissococcinae is a lineage independent ofEulecaniinae + Filippiinae. One of the fourteen trees was identical with the successively-weighted tree. The same results were obtained when the Pseudococcidae was used as the only outgroup. The 14 trees primarily differed in the relative positions of the outgroups but, within the group traditionally called the Coccidae, the primary difference was in the position of the Cissococcinae. It was always in a basal position, either as the most basal clade in the Coccidae, or as the most basal part of a group comprised of the Eulecaniinae, Filippiinae and Cissococcinae, or even as more basal than the Aclerdidae. Although the Aclerdidae is the sister-group of the Coccidae in 9 of the 14 most parsimonious trees, in 3 trees the Tachardiidae was the sister-group to the Coccidae plus the Aclerdidae, with the Cissococcinae positioned more basally than the Aclerdidae, while in 2 trees the Tachardiidae was the sister group of the Coccidae, with the Aclerdidae more basally than the Cissococcinae. These results led us to examine how different outgroups impact on the relationships of the taxa traditionally included within the Coccidae. When an analysis was run using the Cissococcinae as the outgroup and with only the other groups generally considered to be Coccidae included, there were two equally parsimonious trees (Length = 211, CI = 0.51, RI = 0.50); the single successively-weighted tree (Fig. 1.1.3.7.2) is basically the same as Fig. 1.1.3.7.1 except that the Cissococcinae is a lineage independent of the Filippiinae + Eulecaniinae. When a similar analysis was run using the Aclerdidae as the outgroup, a single most parsimonious tree was found (Length = 229, CI = 0.47, RI = 0.51) (Fig. 1.1.3.7.3) that was basically the same as Fig. 1.1.3.7.1 except that Cyphococcinae was basal to the Pseudopulvinariinae and the Filippiinae, Eulecaniinae and Cissococcinae were independent lineages. When another
Phylogeny
231
Pseudococcidae Eriococcidae
L. l!
l
Eriochiton
45
461
Kermesidae Stictococcidae Tachardiidae Asterolecaniidae
I
Lecanodiaspididae
i
41
26
i
Cerococcidae
25
Micrococcidae Aclerdidae
i 3g
Cissoco~inae !
i
Eulecaniinae
i
38
37
i
Filippiinae
36
Cyphococcinae
'1 3',l
35
.
'i
Pseudopulvinariinae Eriopeltinae
33
Myzolecaniinae
i 32
Cardiococcinae
T
i 27
L
L
Paralecaniini Ceroplastinae
i 31
i
I
3O
Saissetiini Pulvinariini
2g Coccini
Fig. 1.1.3.7.1. Cladogram produced from 14 equally parsimonious trees by successive weighting, using 105 characters from the adult female, adult male and 1st instar-nymphs, character-states unordered and with the Aclerdidae, Asterolecaniidae, Cerococcidae, Eriococcidae, Eriochiton, Kermesidae, Lecanodiaspididae, Micrococcidae, Pseudococcidae, Stictococcidae and Tachardiidae as outgroups and the higher taxa within the Coccidae (bracketed with an *) as the ingroup (Length = 479; CI = 0.33; RI = 0.52). Note that one of the 14 trees was identical to the successively-weighted tree.
Section 1.1.3.7 references, p. 242
Systematics
232
Cissococcinae Eulecaniinae Filippiinae Pseudopulvinariinae Eriopeltinae Cyphococcinae Myzolecaniinae
L
Cardiococx~inae Paralecaniini Ceroplastinae Saissetiini Pulvinariini Coccini
Fig. 1.1.3.7.2. As for Fig. 1.1.3.7.1 but cladogramproduced from 2 equallyparsimonious trees by successive weighting, using the Cissocoecinae alone as the outgroup (Length = 211; CI = 0.51" RI = 0.50). Note that the Cissococcinae now forms a separate lineage from the Eulecaniinae and Filippiinae.
similar analysis was run using the Tachardiidae as the outgroup and including the Aclerdidae and Micrococcidae, 4 most parsimonious trees were found (Length = 279, CI = 0.46, RI = 0.51) with a single successively-weighted tree (Fig. 1.1.3.7.4). Although this tree has the same relative infrastructure as the tree in Fig. 1.1.3.7.1, the positions of the Cissococcinae and Aclerdidae have changed, so that the Cissococcinae is now more basal and the Aclerdidae is part of what is traditionally included in the Coccidae. To be certain that a taxon outside of the Coccidae is used as an outgroup, an additional analysis was run using the asterolecanoid lineage (Asterolecaniidae, Cerococcidae and Le~anodiaspididae) as the outgroup and including the Aclerdidae, Micrococcidae, Tachardiidae and Coccidae. Three most parsimonious trees were found (Length = 347, CI = 0.40, RI = 0.53). The single successively-weighted tree (Fig. 1.1.3.7.5) is identical with Fig. 1.1.3.7.4, except that the Aclerdidae is outside of the group traditionally included in the Coccidae; it is also identical to Fig. 1.1.3.7.1 except that the Cissococcinae is a lineage separate from the Eulecaniinae + Filippiinae lineage. The same results were obtained when each of the asterolecanoid families were separately treated as the only outgroup. Regardless of the problems surrounding the choice of an outgroup, the internal structure of the group traditionally included within the Coccidae was relatively constant. In all iterations examined, the relationships of the Cardiococcinae, Paralecaniini, Ceroplastinae, Pulvinariini, Coccini, Saissetiini and Myzolecaniinae were the same. In only one tree of the 14 produced with the full complement of outgroups (Fig. 1.1.3.7.1) was the relationships of the Eriopeltinae, Pseudopulvinariinae and Cyphococcinae altered; in this case the Cyphococcinae was placed adjacent and basal to the
Phylogeny
233
Aclerdidae Cissococcinae Eulecaniinae Filippiinae
l
Cyphococcinae Pseudopulvinariinae Eriopeltinae Myzolecaniinae Cardiococcinae
I
Paralecaniini Ceroplastinae Saissetiini Pulvinariini Coccini
Fig. 1.1.3.7.3. As for Fig. 1.1.3.7.1 except that only a single tree was produced when the Aclerdidae alone was used as the outgroup (Length = 229; CI =0.47; RI = 0.51). Note that this is similar to Fig. 1.1.3.7.1 except that the Cyphococcinae is more basal than the Pseudopulvinariinae and that the Cissococcinae, Eulecaniinae and Filippiinae are independent lineages.
Myzolecaaiinae. The position of the Cissococcinae varied from forming a group with the Eulecaniinae and Filippiinae, to being a separate lineage l o o t e d in the most basal portion of the Coccidae. The Eulecaniinae and Filippiinae either formed a group or were separate lineages adjacent to the more basal Cissococcinae. The relationships of the outgroups are quite variable, accounting for a significant portion of the homoplasy in the analysis. The placement of the Stictococcidae was especially troublesome since it was located adjacent to the Pseudococcidae in some trees and near the Micrococcidae and Tachardiidae in others. One tree even had the Stictococcidae as the basal part of the asterolecanoid lineage. This instability was not unexpected, since the purpose of our analysis was to determine the relationships of the groups within the Coccidae and with the families that have been hypothesized to be close relatives. Therefore, the characters that were selected for this analysis were those most pertinent for determining the relationships among the soft scale groups and are probably less appropriate for studying the relationships of the groups that are more distantly related. Because of the large number of characters used in this analysis, it has not been possible to show the character changes on a tree. This information can be obtained in Appendix 1.1.3.7,D.
Section 1.1.3.7 references, p. 242
Systematics
234
Tachardiidae Micrococcidae Cissococcinae Aclerdidae
r-
Eulecaniinae Filippiinae Cyphococcinae Pseudopulvinariinae Eriopeltinae Myzolecaniinae Cardiococcinae
I
Paralecaniini Ceroplastinae Saissetiini
l
Pulvinariini Coccini
Fig. 1.1.3.7.4. As for Fig. 1.1.3.7.1 except that the cladogram was produced from 4 equally parsimonious trees by successive weighting, with the Tachardiidae as the outgroup plus the Aclerdidae and Micrococcidae
(Length = 279; CI = 0.46" RI = 0.51). Note that the Aclerdidae now fall within the taxa traditionally included in the Coecidae, i.e. between the Cissococcinae and Eulecaniinae + Filippiinae.
Characters that justify the monophyly of the clades are as follows (see Fig. 1.1.3.7.1 for internode numbers): Internode 46. 2.1 (independently derived in the Saissetiini and Paralecaniini); 10.3 (independently derived in the Pseudopulvinariinae); 15.1 (independently derived in the Cissococcinae); 20.1 (independently derived in the Saissetiini and Cerococcidae); 21.1 (independently derived in the Cerococcidae and Saissetiini); 35.2 (independently derived in the Aclerdidae); 38.1; 39.2 (reversal within clade defined by intemode 46 in the Cissococcinae and Myzolecaniinae); 53.1 (independently derived in the Saissetiini; reversal within clade defined by internode 46 at lineage 27 and in the Aclerdidae and Eulecaniinae); 54.2 (reversal within clade defined by internode 46 at lineage 25 and in the Stictococcidae); 60.1 (independently derived in the Eriopeltinae); 62.1 (independently derived in the Eriopeltinae; reversal within clade defined by intemode 46 at lineage 34); 63.1 (reversal within clade defined by intemode 46 at lineage 32 and in the Pseudopulvinariinae and Stictococcidae); 68.1 (reversal within clade def'med by intemode 46 at lineage 28 and in the Stictococcidae); 69.1 (reversal within clade defined by intemode 46 at lineage 33 and in the Cissococcinae and Stictococcidae); 73.1 (reversal
Phylogeny
235
Cerococcidae Lecanodiaspididae Asterolecaniidae Micrococcidae
l I
Aclerdidae Tachardiidae Cissococcinae Eulecaniinae Filippiinae Cyphococcinae Pseudopulvinariinae Eriopeltinae Myzolecaniinae Cardioccx~inae Paralecaniini Ceroplastinae Saissetiini Pulvinariini Cax~ini
Fig. 1.1.3.7.5. As for Fig. 1.1.3.7.1 exceptthat the cladogramwas produced fromthree equally parsimonious trees by successive weighting (Length = 347; CI = 0.40; RI = 0.53) using the Asterolecaniidae, Cerococcidae and Lecanodiaspididae as the outgroup and including the Aclerdidae, Micrococcidae and Tachardiidae. Note that this tree is identical to Fig. 1.1.3.7.4 except that the Aclerdidae is now outside the clade traditionally included in the Coccidae.
within clade defined by intemode 46 in the Paralecaniini and Tachardiidae); 79.2 (reversal within clade defined by intemode 46 at lineage 32 and in the Filippiinae, Le.canodiaspididae and Stictococcidae); 91.2; 100.1 (reversal within clade defined by intemode 46 at lineage 35). lnternode 45. 9.2 (independently derived in the Kermesidae and Micrococcidae); 17.1; 19.1 (independently derived in the Kermesidae, Tachardiidae and Asterolecaniidae); 22.1 (independently derived in lineages 43 and 30); 26.1 (independently derived in the Aclerdidae, Cyphococcinae and Stictococcidae); 28.1 (independently derived in lineage
Section 1.1.3.7 references, p. 242
236
Systematics
39 and the Cerococcidae); 32.1 (independently derived in lineage 26); 33.1 (independently derived in lineage 39 and the Stictococcidae and Cerococcidae); 36.2 (independently derived in lineages 26 and 39); 66.1 (independently derived in lineage 26 and the Kermesidae and Myzolecaniinae); 74.1 (independently derived in lineage 43 and the Cerococcidae and Saissetiini); 87.2 (independently derived in the Asterolecaniidae and Kermesidae); 102.1 (independently derived inAclerdidae, Cerococcidae, Kermesidae and Paralecaniini). Internode 44. 1.1 (independently derived in the Eriococcidae); 23.4 (reversal within clade defined by intemode 44 in the Eriopeltinae, Filippiinae and Pseudopulvinariinae); 24.1 (independently derived in lineage 32 and the Eulecaniinae and Pseudopulvinariinae; reversal within clade defined by internode 44 at lineage 41); 27.4 (reversal within clade defined by internode 44 at lineage 29 and in the Cardiococcinae and Eulecaniinae); 36.1; 43.2 (reversal within clade defined by intemode 44 at lineage 30 and in the Eriopeltinae and Paralecaniini); 45.2 (reversal within clade def'med by internode 44 at lineage 25 and in the Micrococcidae); 46.1; 71.1; 85.1 (reversal within clade defined by intemode 44 in the Eulecaniinae and Tachardiidae); 89.1 (reversal within clade defined by intemode 44 at lineage 3 8). Internode 43. 4.1 (independently derived in Eriochiton); 18.1 (reversal within clade defined by intemode 43 in the Saissetiini); 20.2 (reversal within clade defined by intemode 43 in the Cerococcidae and Saissetiini); 22.1 (independently derived in lineages 30 and 45; reversal within clade defined by intemode 43 at lineage 40); 35.1 (independently derived in the Cardiococcinae and Pseudopulvinariinae); 67.1 (independently derived in the Eriococcidae; reversal within clade defined by intemode 43 at lineage 33 and in the Asterolecaniidae, Cissococcinae and Filippiinae); 74.1 (independently derived in lineage 45 and the Cerococcidae and Saissetiini; reversal within clade defined by intemode 43 at lineage 32 and in the Asterolecaniidae and Lecanodiaspididae); 86.1 (reversal within clade defined by intemode 43 at lineage 37 and in the Le~anodiaspididae and Pseudopulvinariinae); 103.2 (independently derived in the Ceroplastinae, Eulecaniinae, Le~anodiaspididae, Saissetiini, Stictococcidae and Tachardiidae). lnternode 42. 9.1; 15.2 (reversal within clade def'med by intemode 42 in the Cissococcinae); 21.2 (reversal within clade defined by intemode 42 in the Cerococcidae); 30.4 (independently derived in Eriochiton; reversal within clade defined by internode 42 at lineage 26); 40.1 (reversal within clade defined by internode 42 at lineages 31 and 36 and in the Micrococcidae and Pseudopulvinariinae); 44.1 (reversal within clade defined by intemode 42 at lineage 38); 58.1 (reversal within clade defined by intemode 42 at lineage 25 and in the Cyphococcinae and Eulecaniinae); 64.1 (independently derived in Eriochiton and the Kermesidae; reversal within clade def'med by mtemode 42 at lineage 34); 78.1 (reversal within clade defined by mtemode 42 in the Aclerdidae, Cerococcidae and Cissococcinae). Internode 41. 4.2; 24.0 (reversal); 81.1 (independently derived in the Stictococcidae; reversal within clade defined by internode 41 at lineage 37); 87.1. Internode 40. 7.1; 8.1 (independently derived in lineages 27 and 28 and with the Stictococcidae; reversal within clade defined by intemode 40 at lineage 35); 11.2 (independently derived in Eriochiton; reversal within clade def'med by intemode 40 in the Aclerdidae, Filippiinae and Eriopeltinae); 22.0 (reversal); 29.2 (independently derived in Eriochiton; reversal within clade defined by internode 40 in the Aclerdidae). Internode 39. 3.1 (independently derived in the Kermesidae and Stictococcidae; reversal within clade defmed by intemode 39 at lineage 28 and in the Eriopeltinae, Eulecaniinae and Paralecaniini); 28.1 (independently derived in lineage 45 and the Cerococcidae; reversal within clade defined by internode 39 in the Cissococcinae); 33.1 (independently derived in lineage 45 and the Cerococcidae and Stictococcidae); 36.2 (independently derived in lineages 26 and 45; reversal within clade defined by internode 39 in the Myzolecaniinae and Pseudopulvinariinae); 38.2 (independently derived in the
Phylogeny
237 Tachardiidae); 45.1 (independently derived in the Asterolecaniidae and Eriochiton); 50.1 (independently derived in the Asterolecaniidae and Eriochiton); 77.1 (independently derived in the Cerococcidae, Eriococcidae and Tachardiidae; reversal within clade defined by intemode 39 in the Cardiococcinae and Cissococcinae); 105.1 (independently derived in the Le,canodiaspididae). lnternode 38. 6.1 (independently derived in lineage 25, Eriochiton and the Kermesidae, Saissetiini and Tachardiidae; reversal within clade defined by intemode 38 at lineage 32); 9.3 (independently derived in lineage 25; reversal within clade defined by internode 38 in the Pseudopulvinariinae); 10.4 (independently derived in Eriochiton; reversal within clade defined by intemode 38 in the Filippiinae and Pseudopulvinariinae); 35.3 (independently derived in lineage 26; reversal within clade def'med by internode 38 in the Cardiococcinae and Pseudopulvinariinae); 44.0 (reversal; reversal also in the Lecanodiaspididae); 48.1; 51.1 (convergent in the Cerococcidae and Tachardiidae; reversal within clade defined by internode 38 in the Filippiinae and Pseudopulvinariinae); 88.1 (independently derived in lineage 25, Eriochiton and the Kermesidae and Tachardiidae; reversal within clade defined by intemode 38 in the Paralecaniini); 89.0 (reversal); 99.1 (independently derived in the Kermesidae and Tachardiidae). Internode 37. 81.0 (reversal); 86.0 (reversal; reversal also in the Lecanodiaspididae and Pseudopulvinariinae). Internode 36. 25.1 (independently derived in lineage 28 and the Aclerdidae, Eriococcidae, Eriopeltinae and Lecanodiaspididae); 34.1 (independently derived in lineage 32 and the Cyphococcinae); 40.0 (reversal; reversal also in lineage 31 and in the Lecanodiaspididae, Micrococcidae and Pseudopulvinariinae); 59.1 (independently derived in lineage 32 and the Tachardiidae); 76.1 (independently derived in the Cerococcidae, Pseudopulvinariinae and Tachardiidae); 94.2 (independently derived in lineage 33 and the Aclerdidae, Asterolecaniidae and Cerococcidae); 95.3 (independently derived in the Saissetiini and Pseudopulvinariinae); 97.1 (independently derived in lineage 29 and the Myzolecaniinae); 98.1 (independently derived in lineage 30). lnternode 35. 8.0 (reversal; reversal also in the Filippiinae); 55.1 (independently derived in the Kermesidae and Tachardiidae; reversal within clade def'med by intemode 35 at lineage 32); 62.0 (reversal); 65.1 (independently derived in the Cerococcidae, Filippiinae and Tachardiidae); 80.1 (independently derived in lineage 25 and the Stictococcidae); 100.0 (reversal); 103.2 (independently derived in the Lecanodiaspididae, Stictococcidae and Tachardiidae; reversal within clade def'med by internode 35 in the Myzolecaniinae). Internode 34. 20.3 (independently derived in Asterolecaniidae, Filippiinae and Tachardiidae; reversal within clade def'med by intemode 34 in the Saissetiini); 60.0 (reversal); 61.1 (reversal within clade defined by intemode 34 in the Myzolecaniinae and Paralecaniini); 64.0 (reversal); 73.2 (independently derived in the Filippiinae and Stictococcidae); 84.1 (independently derived in the Cissococcinae, Kermesidae, Le~anodiaspididae and Stictococcidae). Internode 33. 2.2 (independently derived in Eriochiton and the Cyphococcinae, Filippiinae and Kermesidae; reversal within clade defined by intemode 33 in the Saissetiini and Paralecaniini); 37.2 (independently derived in the Filippiinae and Asterolecaniidae; reversal within clade def'med by intemode 33 in the Pulvinariini and Saissetiini); 53.2 (independently derived in the Tachardiidae); 67.0 (reversal; reversal also in the Asterolecaniidae, Cissococcinae and Filippiinae), 69.0 (reversal; reversal also in the Cissococcinae and Stictococcidae); 94.2 (independently derived in lineage 36 and the Aclerdidae, Asterolecaniidae and Cerococcidae); 104.1 (reversal within clade in the Cardiococcinae). Internode 32. 5.1 (independently derived in the Cyphococcinae, Eulecaniinae and Stictococcidae; reversal within clade defined by intemode 32 in the Saissetiini); 6.0; 14.1
Section 1.1.3.7 references, p. 242
238
Systematics
(independently derived in the Cyphococcinae, Eulecaniinae and Le~anodiaspididae); 24.1 (independently derived in the Pseudopulvinariinae and lineage 44); 34.1 (independently derived in lineage 36 and the Cyphococcinae); 55.0 (reversal); 59.1 (independently derived in lineage 36 and the Tachardiidae; 63.0 (reversal; reversal also in the Pseudopulvinariinae and Stictococcidae); 74.0 (reversal; reversal also in the Aclerdidae and Lecanodiaspididae); 79.0 (reversal; reversal also in the Filippiinae, Stictococcidae and Lecanodiaspididae). Internode 31. 40.0 (reversal; reversal also in the ~ o d i a s p i d i d a e , Micrococcidae and Pseudopulvinariinae); 42.2 (independently derived in the Filippiinae and Pseudopulvinariinae). Internode 30. 22.1 (independently derived in lineages 43 and 45); 41.2 (independently derived in the Filippiinae); 43.0 (reversal; reversal also in the Filippiinae, Lecanodiaspididae and Pseudopulvinariinae); 66.2 (independently derived in the Paralecaniini and Stictococcidae); 70.1 (independently derived in the Cyphococcinae, Filippiinae, Myzolecaniinae, Stictococcidae and Tachardiidae); 75.1; 76.1 (independently derived in the Cerococcidae, Pseudopulvinariinae and Tachardiidae); 82.1 (independently derived in the Cardiococcinae, Lecanodiaspididae, Pseudopulvinariinae and Stictococcidae); 83.1 (independently derived in the Cardiococcinae, Eriopeltinae and Filippiinae); 90.2; 92.1; 93.1; 96.1 (independently derived in the Eriopeltinae); 98.1 (independently derived in lineage 36). Internode 29. 27.2 (independently derived in the Cardiococcinae, Eulecaniinae and Micrococcidae); 49.1; 72.1 (independently derived in the Filippimae, Pseudopulvinariinae and Tachardiidae); 97.1 (independently derived in lineage 36 and the Myzolecaniinae). Internode 28. 3.0 (reversal; reversal also in the Eulecaniinae, Eriopeltinae and Paralecaniini); 8.1 (independently derived in lineages 27 and 40 and with the Stictococcidae); 25.1 (independently derived in lineage 36 and the Aclerdidae, Eriococcidae, Eriopeltinae and Le~anodiaspididae); 58.2 (independently derived in the Aclerdidae and Myzolecaniinae); 68.0 (reversal; reversal also in the Stictococcidae); 101.1 (independently derived in the Asterolecaniidae and Paralecaniini); 103.1 (independently derived in the Cardiococcinae and Eriopeltinae). Internode 27. 8.1 (independently derived in lineages 28 and 40 and the Stictococcidae); 53.0 (reversal; reversal also in the Aclerdidae and Eulecaniinae); 54.1 (independently derived in the Eriopeltinae and Tachardiidae); 65.0 (reversal). Internode 26. 16.1 (independently derived in the Filippiinae); 30.0 (reversal); 32.1 (independently derived in lineage 45); 35.3 (independently derived in lineage 38); 36.2 (independently derived in lineages 39 and 45); 43.3 (independently derived in the Aclerdidae and Cissococcinae); 57.1; 66.1 (independently derived in lineage 45 and the Myzolecaniinae); 89.2 (independently derived in the Myzolecanimae and Pseudopulvinariinae); 95.1 (independently derived in the Aclerdidae and Myzolecaniinae). lnternode 25. 6.1 (independently derived in lineage 38, Eriochiton and the Kermesidae, Saissetiini and Tachardiidae); 9.3 (independently derived in lineage 38); 12.1 (independently derived in the Aclerdidae, Eriococcidae and Kermesidae); 37.1 (independently derived in the Eriococcidae, Pseudopulvmariinae and Saissetiini); 54.0 (reversal; reversal also in the Stictococcidae); 58.0 (reversal; reversal also in the Cyphococcinae and Eulecaniinae); 80.1 (independently derived in lineage 35 and the Stictococcidae); 88.1 (independently derived in lineage 38, Eriochiton and the Kermesidae and Tachardiidae).
CONCLUSIONS The primary thrust of this analysis was to study the monophyly of the family Coccidae, to understand the relationships of the higher-level taxa within the Coccidae and to examine the relationships of families that have been hypothesized as being closely related
Phylogeny
239 to the Coccidae. The monophyly of the Coccidae is well supported by this analysis. This analysis also supports the transfer of Eriochiton to the Eriococcidae (Hodgson, 1994b). The single unambiguous character defining the Coccidae is the dorso-ventrally elongated head on the adult male (48.1 and 48.2). Other characters that exhibit low amounts of homoplasy and support the monophyly of the family are features in the first instar: spiracular disc-pore rows that are distinct and complete (9.3, independently derived in the Cerococcidae and Lecanodiaspididae but absent in the Pseudopulvinarimae) and anal lobes that are withdrawn as anal plates (10.4, a character that is independently derived in Eriochiton but not shared by the Filippiinae or Pseudopulvinariinae); and in the adult male: abdominal ventral setae more numerous than abdominal dorsal setae (99.1 independently derived in the Kermesidae and Tachardiidae). It is of interest that the clade comprising the Coccidae plus the Aclerdidae is strongly supported as well, suggesting the possibility that aclerdids are simply basal coccids that have specialised on monocotyledonous plants, especially grasses. Since both groups are easily diagnosed as separate entities, and since there is some question about whether the tachardiids are more closely related to the coccids than are the aclerdids and because the current literature consistently treats the Coccidae, Aclerdidae and Tachardiidae as distinct families, we here accept them as separate but closely related. The relationships of the higher-level groups within the family Coccidae are fairly consistent. One of the most strongly defined groups is comprised of the Ceroplastinae, Saissetiini, Pulvinariini and Coccini. There are four unambiguous characters that def'me this group, all in the adult male, namely the basalare not joining the pleural wing process to the metepistemum (75.1); pleurites present on segment VII only (90.2); the caudal extension of segment VIII is prominent and pointed (92.1) and a cicatrix is present on segment VIII (93.1). The placement of the Paralecaniini as most closely related to the Cardiococcinae suggests that it is not part of the Coccinae as previously suggested (Hodgson, 1994a). This hypothesis needs to be tested more fully, since the lineage containing the Cardiococcinae and Paralecaniini is weakly defined. It also is clear that the Cissococcinae is basal within the Coccidae and might even be more basal than the Aclerdidae. Relationships within the Coccidae suggest that the Eulecaniinae and Filippiinae are basal and the Myzolecaniinae, Eriopeltinae, Pseudopulvmariinae and Cyphococcinae are intermediate in their position. The only phylogenetic analysis of the Coccidae undertaken previous to our study was that of Qin (1993). Unfortunately, the phylogenetic portion of this work has not been published. In order to understand the relationships of the genus Ceroplastes with other soft scale genera, he sampled representatives of most of the major groups within the Coccoidea including Aclerda (Aclerdidae), Eriococcus (Eriococcidae), Eriochiton (Eriococcidae) and Lecanodiaspis (Lecanodiaspididae) as outgroups, and with Bodenheimera (Filippiinae), Coccus (Coccini), Cryptes (Eulecaniinae), Eulecanium (Eulecaniinae), Filippia (Filippiinae), Cardiococcus (Cardiococcinae), Cryptostigma (Myzolecaniinae), Eriopeltis (Eriopeltinae), Inglisia (Cardiococcinae), Mallococcus (Filippiinae), Myzolecanium (Myzolecaniinae), Phyllostroma (Filippimae), Pseudopulvinaria (Pseudopulvinariinae), Pulvinaria (Pulvinariini), Saissetia(Saissetiini), Toumeyella (Myzolecaniinae) and five taxa that belong to the Ceroplastinae. His analysis included 126 morphological characters from the adult female and the first-instar nymphs plus one character from chromosome number. He did not include representatives of the Cissococcinae, Cyphococcinae or the Paralecaniini. His results are qualitatively similar to ours although he obtained slightly different trees depending on his choice of outgroup.
Section 1.1.3.7 references, p. 242
240
Systematics
-L
Eriococcidae Eriochiton
Aclerdidae Lecanodiaspididae Filippiinae 2 Eulecaniinae Filippiinae 1 Cardi~inae Eriopeltinae Myzolecaniinae Pseudopulvinariinae Ceroplastinae Coccini Pulvinariini Saissetiini Fig. 1.1.3.7.6. Modified version of the consensus tree produced from six equally parsimonious trees produced by Qin (1993) from an heuristic search, using 126 characters taken from the adult females and first-instar nymphs plus one character from chromosome number, using the Eriococcidae, Eriochiton, Lecanodiaspididae and Aclerdidae as outgroups and twenty-six taxa within the Coccidae as the ingroup (Length = 430; CI = 0.38). Within the Coccidae, the following genera were included from each higher taxon: Cardiococcinae: Inglisia and Cardiococcus; Ceroplastinae: Ceroplastes, Ceroplastidia, Gascardia, Paracerostegia, Waxiella and Vinsonia; Coccini: Coccus; Eriopeltinae: Eriopeltis; Eulecaniinae: Eulecanium and Cryptes; Filippiinae 1: Filippia, Bodenheimera and Mallococcus, and Filippiinae 2: Phyllostroma; Myzoleeaniinae: Cryptostigma, Myzolecanium and Toumeyella; Pseudopulvinariinae: Pseudopulvinaria; Pulvinariini: Pulvinaria and Saissetiini: Saissetia. Note that the Coccini, Pulvinariini and Saissetiini form a distinct clade which is sister to the Ceroplastinae, as in the present analyses.
We have provided one version of the consensus tree that he obtained (Fig. 1.1.3.7.6) by using all four outgroups. His results included 6 equally parsimonious trees (Length = 430, CI= 0.38). Although the relationships of the Cardiococcinae, Eriopeltinae, Myzolecaniinae and Pseudopulvinariinae were unresolved, the trees were otherwise consistent with the results of our analysis, i.e. that the Coccini, Pulvinariini and Saissetiini formed a distinctive group that was the sister of the Ceroplastinae, with the Cardiococcinae, Eriopeltinae, Myzolecaniinae and Pseudopulvinariinae intermediate in the tree and with the Eulecaniinae and Filippiinae basal. Use of the Aclerdidae as the sole outgroup produced a single tree (Length = 366, CI = 0.42) (Fig. 1.1.3.7.7) that was better resolved than the tree shown in Fig. 1.1.3.7.6. Although this tree shared many similarities with our results, the basal position of the Myzolecaniinae is quite different from the results of any of our analyses.
Phylogeny
241
Aclerdidae Myzolecaniinae Filippiinae 1
t I iii II
Eulecaniinae Filippiinae 2 Eriopeltinae
l
Pseudopulvinariinae
/
Cardiococcinae Ceroplastinae Pulvinariini Saissetiini Coccini
Fig. 1.1.3.7.7. Modified version of the single tree produced by Qin (1989); data as for Fig. 1.1.3.7.6 but with the Aclerdidae alone as the outgroup (Length = 366; CI = 0.42). Note that the position of the Myzoleeaniinae is much more basal than in present analyses.
The relationships of the families outside of the Coccidae remain controversial. In a paper published by Miller and Williams (1995), evidence is provided that the Micrococcidae and Aclerdidae are more closely related to one another than to the Coccidae. They also suggested that the Tachardiidae was the sister to the Micrococcidae + Aclerdidae + Coccidae and described it as a well-defined group. A second discrete group called theasterolecanoids (Asterolecaniidae + Cerococcidae + I.ex~anodiaspididae) was the sister of the Tachardiidae + Micrococcidae + Aclerdidae + Coccidae group. This arrangement is slightly different from the hypothesis presented here in which the Micrococcidae is closely related to the Aclerdidae but does not form a monophyletic group. The position of the Tachardiidae is variable. It is apparent that it is related to the aclerdids, coccids and micrococcids but its exact position remains to be resolved. The "asterolecanoid" group is well def'med but is placed much closer to the Coccidae + Aclerdidae group than in Miller and Williams (1995). There may be several explanations for these differences, probably the most important of which is that neither analysis was designed to examine these relationships in detail. In the current study considerable emphasis was placed on the males but, as winged males in the Micrococcidae are unknown, these missing data may have influenced its placement. It is evident that more work is needed in this area, but these hypotheses provide the framework for further phylogenetic exploration.
Section 1.1.3.7 references, p. 242
242
Systematics
ACKNOWLEDGEMENTS We are especially grateful to Dr. Robert Minckley (Department of Entomology, Auburn University, Auburn, Alabama, USA) for his extensive comments and helpful suggestions. We are also grateful for the helpful comments from James Pakaluk and Michael Schauff, both of the Systematic Entomology Laboratory, US Department of Agriculture, Beltsville, Maryland, USA.
REFERENCES Afifi, S.A., 1968. Morphology and taxonomy of the adult males of the families Pseudococcidae and Eriococcidae (Homoptera: Coccoidea). Bulletin of the British Museum (Natural History), London, Entomology Supplement 13: 1-210. Baer, R.G. and Kosztarab, M., 1985. A morphological and systematic study of the first and second instars of the Family Kermesidae in the Nearctic region (Homoptera: Coccoidea). Bulletin of the Virginia Agricultural Experiment Station, Virginia Polytechnic Institute and State University, Blacksburg, 85 (11): 119-261. Boratyfiski, K. and Davies, R.G., 1971. The taxonomic value of male Coccoidea (Homoptera) with an evaluation of some numerical techniques. Biological Journal of the Linnean Society, 3: 57-102. Borchsenius, N.S., 1958. On the evolution and phylogenetic interrelations of the Coccoidea. Zoologicheskii Zhurnal, 37: 765-780. Bullington, S.W. and Kosztarab, M., 1985. Revision of the Family Kermesidae (Homoptera)in the Nearctic Region based on adult and third instar females. Bulletin of the Virginia Agricultural Experiment Station, Virginia Polytechnic Institute and State University, Blacksburg, 85(11): vi+ 1-119. Danzig, E.M., 1986. Coccids of the Far-Eastern USSR (Homoptera, Coccinea). Phylogenetic Analysis of Coccids in the World Fauna. Nauka Publishers, Leningrad, 1980. Translated from the Russian and published by the United States Department of Agriculture and the National Science Foundation, Washington, DC. xxv+450 pp. Foldi, I., 1995. A taxonomic revision of Limacoccus Bondar with a cladistic analysis of its relationships with other scale insects (Hemiptera: Coccoidea). Systematic Entomology, 20: 265-288. 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. Giliomee, J.H. and Munting, J., 1968. A new species of Asterolecanium Tar. (Homoptera: Coccoidea: Asterolecaniidae) from South Africa. The Journal of the Entomological Society of Southern Africa, 31 : 221229. Hamon, A.B. and Kosztarab, M., 1979. Morphology and systematics of the first instars of the genus Cerococcus (Homoptera: Coccoidea: Cerococcidae). Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 146: vi+ 121. Henderson, R.C. and Hodgson, C.J., 1995. The taxonomic relationships of the eriococcid genus Eriochiton Maskell, with observations on the biology of some species. Proceedings of the VII International Symposium of Scale Insect Studies, The Volcani Center, Agricultural Research Organisation, Bet Dagan, Israel. Israel Journal of Entomology, 29: 75-83. Hodgson, C.J., 1991. A rede scription of Pseudopulvinaria sikla'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., 1994a. The Scale Insect Family Coccidae: An Identification Manual to Genera. CAB International, Wallingford. vi + 639 pp. Hodgson, C.J., 1994b. Eriochiton and a new genus of the scale insect family Eriococcidae (Homoptera: Coccoidea). Journal of the Royal Society of New Zealand, 24: 171-208. Hodgson, C.J. and Henderson, R.C., 1996. A review of the Eriochiton spinosus (Maskell) species-complex (Eriococcidae: Coccoidea), including a phylogenetic analysis of its relationships. Journal of the Royal Society of New Zealand, 26: 143-204. Howell, J.O., 1973. The immature stages ofAclerda tiUandsiae (Homoptera: Coccoidea: Aclerdidae). Annals of the Entomological Society of America, 66: 1335-1342. Kosztarab, M. and Ko~r, F., 1988. Scale Insects of Central Europe. Series Entomologica, Vol. 41. W. Junk, Dordrecht, 456 pp. Koteja, J., 1974. Comparative studies on the labium in the Coccinea 0tomoptera). Zeszyty Naukowe Akademii Rolniczej w Krakowie, 27: 1-162. Koteja, J. and Zak-Ogaza, B., 1972. Morphology and taxonomy of the male Kermes quercus (L.) (Homoptera: Coccoidea). Acta Zoologica Cracoviensia, 17: 195-215. Lambdin, P.L. and Kosztarab, M., 1977. Morphology and systematics of the adult females of the genus Cerococcus (Homoptera: Coccoidea: Cerococcidae). Bulletin of the Virginia Polytechnic Institute and State University, Blacksburg, Research Division, 128: 1-252. Maddison, W.P. and Maddison, D.R., 1992. MacClade, version 3. Sinauer Associates Inc., Massachusetts, USA.
Phylogeny
243 Miller, D.R., 1984. Phylogeny and classification of the Margarodidae and related groups (Homoptera: Coccoidea). Verhandlungen des Zehnten lnternationalen Symposiums fiber Entomofaunistik Mitteleuropas (SIEEC X), 15-20 Aug. 1983, Budapest, pp. 321-324. Miller, D.R. and Denno, R.F., 1977. A new genus and species of mealybug with a consideration of morphological convergence in three arboreal species (l-lomoptera: Pseudococcidae). Systematic Entomology, 2:11-157. Miller, D.R. and Kosztarab, M., 1979. Recent advances in the study of scale insects. Annual Review of Entomology, 24: 1-27. Miller, D.R. and Miller, G.L., 1993a. Description of a new genus of scale insect with a discussion of relationships among families related to the Kermesidae (Homoptera: Coccoidea). Systematic Entomology, 18: 237-251. Miller, D.R. and Miller, G.L., 1993b. A new species of Puto and a preliminary analysis of the phylogenetic position of the Puto group within the Coccoidea (Homoptera: Pseudococcidae). Jeffersoniana, 4: 1-35. Miller, D.R., Tong-Xian Liu and Howell, J.O., 1992. A new species of Acanthococcus (Homoptera: Coccoidea: Eriococcidae) from Sundew (Drosera~ with a key to the instars of Acanthococcus. Proceedings of the Entomological Society of Washington, 94: 512-523. Miller, D.R. and Williams, D.J., 1995. Systematic revision of the family Micrococcidae (Homoptera: Coccoidea), with a discussion of its relationships, and a description of a gynandromorph. Bollettino del Laboratorio de Entomologia Agraria 'Filippo Silvestri', Portici, 50 (1993): 199-247. Miller, G.L. and Williams, M.L., 1995a. Systematic analysis of the adult males of Toumeyella group, including Mesolecanium nigrofasciatum, Neolecanium cornuparvum, Pseudophilippia quaintancii, and Toumeyella spp. (Homoptera: Coccidae) from America north of Mexico. Contributions of the American Entomological Institute 28: 1-68. Munting, J., 1966. Lac insects (Homoptera: Lacciferidae) from South Africa - II. Revue de Zoologic et Botanic Africaine, 74: 121-134. Munting, J. and Giliomee, J.H., 1967. A new species of Lecaniodiaspis Targ. (Homoptera: Asteroh~caniidae) from South Africa. Journal of the Entomological Society of Southern Africa, 29: 102-108. Qin, T.K., 1993. Phylogeny and Biogeography of the Wax Scales (Hemiptera, Coccoidea: Coccidae) with Special Reference to Ceroplastes sinensis Del Guercio. Ph.D. thesis, Australian National University, Canberra, Australia. Qin, T.K. and Gullan, P.J., 1995. A cladistic analysis of wax scales (Hemiptera: Coccoidea: Coccidae: Ceroplastinae). Systematic Entomology, 20: 289-308. 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., 1981. Redescription and lectotype designation of the tessellated scale, Eucalynmatus tessellatus (Signoret) (Homoptera: Coccidae). Proceedings of the Entomological Society of Washington, 83: 230-244. Ray, C.H. and Williams, M.L., 1982. Descriptions of the immature stages of Protopulvinaria pyriformis (Cockerell) (Homoptera: Coccidae). The Florida Entomologist, 65: 169-176. 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. Richard, C., 1971. Contribution a l'rtude morphologique et biologique des Stictococcinae (Horn., Coccoidea). Annales de la Socirt6 Entomologique de France (N.S.), 7: 571-609. Richard, C., 1976. Rrvision du groupe Stictococcus, et crration de taxa nouveaux (Homoptera, Coccoidea). Annales de la Socirt6 Entomologique de France (N.S.), 12: 653-669. Russell, L.M., 1941. A classification of the scale insect genus Asterolecanium. United States Department of Agriculture, Miscellaneous Publication No. 424, 322 pp. Swofford, D.L., 1993. PAUP - Phylogenetic analysis using parsimony, version 3.1.1. Illinois Natural History Survey, Champaign, Illinois, 257 pp. Tang, Fang-teh., 1991. The Coccidae of China. Shanxi United Universities Press, P.R. China. 377 pp. + 84 figs. 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, Aug. 6-12th, 1990, Part H: 75-77. Williams, D.J., 1985. The British and some other European Eriococcidae (Homoptera: Coccoidea). Bulletin of the British Museum (Natural History), Entomology Series 51 (4): 347-393. Williams, D.J. and Granara de Willink, M.C., 1992. Mealybugs of Central and South America. CAB International, Wallingford, 635 pp. Williams, M.L. and Kosztarab, M., 1970. A morphological and systematic study on the first instar nymphs of the genus Lecanodiaspis (Homoptera: Coccoidea: Lacanodiaspididae). Virginia Polytechnic Institute, Blacksburg, Virginia, Research Division Bulletin No. 52, 96 pp.
244
Systematics
APPENDIX
1.1.3.7,A
Sources of the characters and character-states, where i. 1st instar nymph, ii. adult female and iii. adult male. 1. Aclerdidae: i. Aclerda tiUandsiae Howell (Howell, 1973). ii. Aclerda tillandsiae Howell (Howell, 1973). iii Aclerda arundinariae McConnell, near Narrows Marina, Seashore State Park, Virginia, USA, on Arundinaria sp., 9.v.1971. USNM, 2 specimens. 2. Asterolecaniidae: i. Asterolecanium zanthenes Russell (Russell, 1941). ii. Aswrolecanium proteae Giliomee & Munting (Giliomee and Munting, 1968). iii. Asterolecanium proteae Giliomee & Munting (Giliomee and Munting, 1968). 3. Cardiococcinae: i. Lecanochiton metrosideri Maskell. Sewell Park, New Zealand, ex Metrosideros lucida, 22.xi.1984, C.F. Butcher. NZAC, 3 specimens. ii. Cardiococcus umbonatus Cockerell (Hodgson, 1994a). iii. Inglisia theobromae (Newstead) (Giliomee, 1967). 4. Cerococcidae: i. Cerococcus quercus Comstock (Hamon and Kosztarab, 1979). ii. Cerococcus quercus Comstock (Lambdin and Kosztarab, 1977). iii. Cerococcus andinus Leonardi, Cacheuta, Argentina, on Tricyela cacheuti, 15.ii.1909. USNM, 3 specimens. 5. Ceroplastinae: i. Ceroplastes sinensis del Guercio (Quin, 1993). ii. Ceroplastes janeirensis (Gray) (Hodgson, 1994a). iii. Ceroplastes berliniae Hall (Giliomee, 1967). 6. Cissococcinae: i. C~'ssococcusfulleri Cockerell, Durban Botanical Gardens, Natal, South Africa, Jan. 1920, C.K. Brain. USNM, 3 specimens. ii. Cissococcusfulleri Cockerell (Hodgson, 1994a). iii. Ci'ssococcusfulleri Cockerell, Durban Botanical Gardens, Natal, S. Africa, Jan. 1920, C.K. Brain. USNM, 2 pharate adults. 7. Cocclni: i. Eucalymnatus tessellatus (Signoret) (Ray and Williams, 1981). ii. Coccus hesperidum Linnaeus (Hodgson, 1994a). iii. Coccus hesperidum Linnaeus (Giliomee, 1967). 8. Cyphococcinae: i. Messinea conica De Lotto, Asmara, Eritrea, 29.vii.1947, on Acacia abyssinica, De Lotto. BMNH, 3 specimens. ii. Cyphococcus caesalpiniae Laing (Hodgson, 1994a). iii. Messinea conica De Lotto, Asmara, Eritrea, 29.vii. 1947, on Acacia abyssinica, De Lotto. BMNH, 1 specimen. 9. Eriochitonini: i. Eriochiton spinosus (Maskell) (Hodgson, 1994b). ii. Eriochiton spinosus (Maskell) (Hodgson, 1994b). iii. Eriochiton hoheriae Hodgson (Henderson and Hodgson, 1994). 10. Eriococcidae: i. Acanthococcus eriogoni (Ehrhorn) (Miller et al., 1992). ii. Eriococcus buxi (Fonscolombe) (Williams 1985). iii. Eriococcus buxi (Fonscolombe) (Afifi, 1968). 11. Eriopeltinae: i. Paralecanopsis turcica Bodenheimer (Hodgson, 1994a). ii. Eriopeltisfestucae (Fonscolombe) (Hodgson, 1994a). iii. Eriopeltis ?festucae (Fonscolombe) (Giliomee, 1967). 12. Eulecaniinae: i. Eulecanium tiliae (Linnaeus), Chester, England, no date or host, R. Newstead. BMNH, 7 specimens. ii. Eulecanium tiliae (Linnaeus) (Hodgson, 1994a). iii. Eulecanium tiliae (Linnaeus) (Giliomee, 1967). 13. F'flippiinae: i. Bodenheimera rachelae (Bodenheimer) (Hodgson, 1994a). ii. Filippia follicularis (Targioni Tozzetti) (Hodgson, 1994a). iii. Filippia follicularis (Targioni Tozzetti) (Giliomee, 1967). 14. Kermesidae: i. Kermes cockerelli Ehrhorn (Baer and Kosztarab, 1985) ii. Kermes sylvestris (Cockerell & King) (Bullington and Kosztarab, 1985). iii. Kermes quercus Linnaeus (Koteja & Zak-Ogaza, 1972). 15. Lecanodiaspidldae: i. Lecanodiaspis sardoa Targioni Tozzetti (Williams and Kosztarab, 1970). ii. Lecanodiaspis sardoa Targioni Tozzetti (Kosztarab and Ko~r, 1988). iii. Lecanodiaspis elytropappi Munting & Giliomee (Giliomee, 1967). 16. Micrococcidae: i. Micrococcus bodenheimeri Bytinski-Salz (Miller and Williams, 1995). ii. Micrococcus bodenheimeri Bytinski-Salz (Miller and Williams, 1995). iii. No alate males known. 17. Myzolecaniinae: i. Neolecanium cornuparvum (Thro) (Ray and Williams, 1983). ii. Myzolecanium kibarae Beccari (Hodgson, 1994a). iii. Pseudophilippia quaintancii Cockerell (Ray and Williams, 1980).
Phylogeny
245
APPENDIX 1.1.3.7,A (continued) 18. Paralecaniini: i. Paralecanium macrozamiae (Fuller), Swan River, Western Australia, on Macrozamia frazeri, 1897. USNM, 6 specimens. ii. Paralecanium frenchii (MaskeU) (Hodgson, 1994a). iii. Paralecanium maritimum Green, Bentota, Ceylon, ex Carissa sp. BMNH, 1 specimen. 19. Pseudococcidae: i. Leptococcus metroxyli Reyne (Miller and Denno, 1977). ii. Pseudococcus longispinus (Targioni Tozzetti) (Williams and Granara de Willink, 1992). iii. Pseudococcus viburni (Signoret) (=P. affinis (Maskell)) (Afifi, 1968). 20. Pseudopulvinariinae: i. Pseudopulvinaria sikkimensis Atldnson (Hodgson, 1991). ii. Pseudopulvinaria sikkimensis Atkinson (Hodgson, 1991). iii. Pseudopulvinaria sikMmensis Atldnson (Hodgson, 1991). 21. Pulvinariini: i. Protopulvinaria pyriformis (Cockerell) (Ray and Williams, 1982). ii. Pulvinaria vitis (Linnaeus) (Hodgson, 1904a). iii. Pulvinaria acericola (Walsh & Riley) (Giliomee, 1967). 22. Saiss~ilni: i. Etiennea petasus Hodgson (Hodgson, 1993). ii. Saissetia coffeae (walker) (Hodgson, 1994a). iii. Parthenolecanium corni (Bouch~) (Giliomee, 1967). 23. Stictococcidae: i. Stictococcus sjostedti (Cockerell), Nigeria, on Cola acuminata, 19.ii.1984, USNM; 6 specimens. ii. Stictococcus pujoli Richard (Richard, 1976). iii. Stictococcus intermedius Newstead (Richard, 1971). 24. Tachardiidae: i. Tachardiafici Green, India. G. Wyatt #14916. BMNH, 9 specimens. ii. Tachardia karoo Brain (Munting, 1966). iii. Tachardia aurantiaca Cockerell, Bangkok, Thailand, on Acacia and Aizyphus mauritiana, 1 .v. 1973 and 24.iv.1973. USNM, 2 specimens.
Systematics
246
APPENDIX 1.1.3.7,B List o f c h a r a c t e r s a n d c h a r a c t e r states F'wst I a s t a r s : 1. Eyespots: far from antennae on venter = 0; far from antennae on margin = 1 2. Antennal scape: on anterior margin = 0; about l x width of scape away from margin = 1; 2x width o f scape or more away from margin = 2 3. Antennae: 1-2x width of scape apart = 0; greater than 2x width of scape apart = 1 4. Labial segments: 3 = 0; 2 = 1; 1 = 2 5. Tarsal digitules: similar = 0; dissimilar = 1 6. Claws: denticle: absent = 0; present = 1 7. Tarsal c a m p a n i f o r m pore: present = 0; absent = 1 8. Claw digitules: similar = 0; dissimilar = 1 9. Spiracular disc-pore rows: absent = 0; in or closely associated with peritreme = 1; distinct but incomplete = 2; distinct and complete = 3 10. Anal lobes: small m e m b r a n o u s = 0; absent = 1; distinct membranous = 2; distinct sclerotised = 3; withdrawn as anal plates = 4 11. Anal plates: n u m b e r formed from anal lobes: absent = 0; 1 = 1; 2 = 2 12. Anal cleR: inner margin sclerotisation: absent = 0; present = 1 13. Anal lobe seta" long apical seta" present = 0; absent = 1 14. Stigmatic spines: absent = 0; present = 1 15. Setae dorsally: 3 or more pairs o f longitudinal lines = 0; 2 pairs of lines = 1; 1 pair o f lines or no dorsal setae = 2 1 6 . 8 - s h a p e d pores: absent = 0; present = 1 17. Microtubular ducts: absent = 0; present = 1 18. Tibial seta: outer distal: present = 0; absent = 1 19. Tibial seta: outer medial: present = 0; absent = 1 20. Tibial setae: number: > 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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Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved.
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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
259
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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Y. Ben-Dov and C.J. Hodgson (Editors) 9 1997 Elsevier Science B.V. All rights reserved
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,
Section 1.2.1.3 references, p. 266
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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
Section 1.2.2.1 references, p. 274
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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
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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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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
Morphology and anatomy of honeydew eliminating organs
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
Sooty moulds
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).
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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
Section 1.2.3.2 references, p. 319
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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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305
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.
Section 1.2.3.2 references, p. 319
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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
Section 1.2.3.2 references, p. 319
Soft scales as beneficial insects
308
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
330
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
Ecology
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.
Solt 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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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
Section 1.3.2 references, p. 138
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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
Section 1.3.3 references, p. 342
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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
Section 1.3.3 references, p. 342
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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
346
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
Seasonal history; diapause
347
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; 2, >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
<1
O. smaragdina
(L.) Corr. Serr.
Milviscutulus mangiferae (Green)
Eucalyptus deglupta
3
O.smaragdina
Blume
Psidium guajava L.
Coccus celatus
Coffea canephora
De Lotto
Pierre ex Froehn (robusta coffee)
C. canephora
O.smaragdina
c. 50
< 5
120
< 2
3
O.smaragdina
1O0
0
4
Solenopsis geminata (Fabricius) (Formicinae)
Relationships with ants
363
reviewed by Hrlldobler and Wilson (1990). The ant species predominating in an area is referred to as "dominant" and usually excludes other dominants, although certain dominants are able to co-exist and then are referred to as "co-dominants" (Majer, 1972; Leston, 1973; Adenuga and Adeboyeku, 1987). Both Oecophylla longinoda and O. smaragdina, for example, are abundant and dominant ants over much of their respective ranges (Hrlldobler and Wilson, 1990). The distribution pattern of the dominant species is thought to form a three-dimensional mosaic resulting from aggressiveness and competition for food and nesting sites (Majer, 1972; Leston, 1973). A characteristically different arthropod community (including coccoids) may be associated with each dominant (or co-dominant) ant species, with composition depending on the predatory and tending habits and the feeding specialisation of the ants (Majer, 1976). Obviously, the food habits and competitive abilities of the dominant or co-dominant ant species in any locality may affect the composition and size of resident coccid populations, both directly and also indirectly, as a consequence of which species of non-dominant ants can co-exist with the dominants. Other than anecdotal observations in the coccid-ant literature, there seems to have been little attempt to determine how interspecies differences in ant aggression or behaviour correlate with success of the ants in deterring natural enemies of scale insects (Buckley and Gullan, 1991). This is surprising given that the manipulation of ant community structure by selective removal of certain species (Leston, 1973; Majer, 1976; Samways et al., 1982) or simply killing or excluding all ants (Young, 1982; Moreno et al., 1987; Njeru, 1990) have frequently been suggested as means of controlling coccoid pests.
BENEFITS OF COCCIDS TO ANTS Much of the earlier ant and coccid literature refers to coccids as "cows" that are "milked" for their honeydew by the ants (e.g., Wheeler, 1910; Bailey 1922b; Bequaert, 1922; Tho, 1978). This is an apt analogy that, at least for some coccid-ant associations, can be extended to the ants "farming" the coccids as a source of proteins and lipids in addition to the carbohydrate obtained from the honeydew (Bailey, 1923; Carroll and Janzen, 1973) (Fig. 1.3.5.3). Indeed, Way (1963) and Carroll and Janzen (1973) suggest that the more dependent an ant colony appears to be on homopterans, the more likely that the ants are harvesting them for protein and lipid as well as honeydew. The culling and eating of coccoids appears prevalent among ants involved in certain obligate ant-plant mutualisms (see section on Coccids, Ants and Ant-plants), but with less intimate associations, like those between introduced or cosmopolitan ants (e.g., Linepithema humile) and pest soft scales, there is no indication of predation (e.g., Steyn, 1954; Bartlett, 1961; Way, 1963; Haines and Haines, 1978). Nevertheless, in some studies, there are observations of ants killing and/or removing some of the coccids that they tend (Way, 1954b; Das, 1959; Maschwitz et al., 1985, 1991b), perhaps because the coccids are surplus to honeydew requirements (Way, 1954b, 1963), but evidence that the coccids are actually eaten is more scanty. Consumption of scale insects and other homopterans can be demonstrated most easily and conclusively by examining the gut contents or larval food pellets of the ants. By this means and by direct observation of ant behaviour, Bailey (1922b, 1923) showed that members of certain plant-ant groups, such as Pseudomyrmex and Tetraponera species, are more likely to eat their associated coccoids than other plant-ants, such as Azteca and Crematogaster species. Such differences in ant use of coccoids probably depend on the dietary requirements of the ants, including the availability of alternative protein and lipid food sources, both now and during the past history of the associated taxa. Lipids and proteins play a vital part in ant nutrition (Beattie, 1985), but the importance of coccids as food items for ants is small in comparison to the use of their honeydew as
Section 1.3.5 references, p. 371
364
Ecology
a carbohydrate or energy source (Way, 1963; Carroll and Janzen, 1973; Buckley 1987b; H611dobler and Wilson, 1990). Although the honeydews of only a few Coccidae have been analysed chemically (Hackman and Trikojus, 1952; Ewart and Metcalf, 1956), it is clear that the main components of coccid honeydews are water-soluble carbohydrates, mostly sugars, plus water and much smaller proportions of nitrogen-containing compounds and traces of other substances. A noteworthy feature of honeydew production is the copious quantity produced in relation to the small size of the coccids (Ewart and Metcalf, 1956). A single large citrus tree infested with Coccus hesperidum, for example, has been estimated to yield only 14 lbs of sucrose per year from the harvested oranges compared with 600 lbs of sucrose collected per year by the ant Anoplolepis custodiens from the same tree (Steyn, 1954). It is not surprising that such an abundant and readily-harvested sugar source is a major component of the diet of many ants.
For the ants, however, not all honeydews are alike. The constituents of phloem and hence coccid honeydew may differ among plant species (Hackman and Trikojus, 1952; Molyneux et al., 1990), or vary seasonally, or vary on different parts of the same plant, or with plant age (reviewed by Way, 1963). In addition, the coccid digestive process may alter the composition of ingested sap and add synthetic components (Ewart and Metcalf, 1956) and it is possible that some honeydews contain specific ant-attractants, as suggested by Andrews (1930) and Buckley (1987a). All of the above factors may affect the suitability or palatability of the honeydew to tending ants. Not all coccid honeydews are equally attractive to the worker ants of L. humile, which prefer the honeydew of C. hesperidum to that of other coccids, especially to that of Coccus pseudomagnoliarum (Kuwana) which is relatively unattractive to the ants (Flanders, 1951; Ewart and Metcalf, 1956). The differential attractiveness of the honeydew of these two citrus-feeding Coccus species is not due to qualitative differences in sugars or amino acids (Ewart and Metcalf, 1956) but may reflect either differences in the quantities of honeydew produced by the two species or differences in the plant defensive compounds present in the phloem of the different plant parts upon which the coccids generally feed. The adults of C. hesperidum are commonly found on the leaves, whereas adults of C. pseudomagnoliarum primarily occur on the twigs of citrus (Gill, 1988). lntra-plant differences in phloem quality may determine whether ants attend homopterans or not. For example, aphids feeding on oleander have been shown to be more attractive to tending ants when feeding on floral tips than on leaf tips, although the factor responsible is not known (Bristow, 1991). Recent analyses of the honeydew of various sap-sucking insects have indicated the presence of certain plant secondary compounds, such as alkaloids, in the phloem of their host plants (Dreyer et al., 1985; Molyneux et al., 1990) and it is possible that the preferences exhibited by ants for certain coccid honeydews may be due to the absence of such compounds. Bristow (1991) emphasises the need to consider ant-homopteran associations in relation to the relative importance to ants of nutrients, plant defensive chemistry and quantities of honeydew produced. Thus, not all soft scales may be equally attractive to ants and the benefit to a given ant species of a particular plant-coccid association may depend on a number of factors.
COCCIDS, ANTS AND ANT-PLANTS A special kind of coccid-ant association occurs in species of a number of coccid genera that have been collected from inside the hollow chambers of myrmecophytes or ant-plants. These plants have specialised structures, such as leaf pouches or swollen hollow stems, petioles, roots or pseudobulbs, that are known as domatia and that serve
R F
$
s 2
f.
TABLE 1.3.5.3 Coccidae associate with ants in antplants (myrmecophytes). Unidentified plants are exclude Obligate plant-ants are indicated with an asterisk ~
*.
Doubtful mymecophytes are indict d with a question mark (?).
3 n
G
~~
Distribution
Coceids
Ants
Afmtmpical
Hcmilrcanium recuwarum Newstead
Forel (cited as
Cremalogasrer luurenn'
Ant-plant g a w
Plant f d y
Form of domatia
Reference
Psydrax
Rubiaceae
Hollow branches
Newstead, 1910; Bequaert, 1922
(= Plecrronia)
C. aficana hUrCnh)
Australasian (including New Guinea)
Neotropical
Udinia newsreadi Hanford
Cremarogastcr aficana schumanni Mayr
Barterin
Passifloraceae
Hollow stems
Mann, 1922; Bailey, 19228; Hanford, 1974
Myzolecanium kibarae Beccari Myzolecanium spp .
Anonychomywna (formerly Iridomynnu) scruraror (F. Smith) & other A . spp. Terraponera sp. *
Kibara Sreganrhcra Aphanomixis? Myristica Cupaniopsis
Monimiaceae Meliaceae Myristicaceae Sapindaceae
Hollow branches, stems or internodes, often swollen
Beccari, 1877; Bequaert, 1922; Huxley, 1986; Ward, 1991; Gullan et al., 1993; Hodgson, 1994
Torarchus cndocanrhiwn Gullan and Stewart
Podomynna ap.
Canrhium
Rubiaceae
Hollow stems and branches
Monteith, 1990; Gullan and Stewart(l966)
Akcnnes cordiae Morrison
Zacryprocem sp.
Cordia
Ehretiaceae
Hollow, swollen stems
Momson, 1929
Cryprostigma biorbiculus Momson
Aaeca pim'cri complex Cordia (cited as A. longiceps Emery); Pseudomywncx ira (Forel); P . sericeus group
Ehretiaceae
Hollow, swollen stems
Momson, 1929; Wheeler, 1942; Qin and Gullan, 1989
Cryprostigma inquilina (Newstead)
Azcca pim'eri complex (cited as A. longiccps) & Pseudomymur sp .
Ehretiaceae Polygonaceae
Hollow stems, swollen in Cordia
Morrison, 1922, 1929; Wheeler, 1942; Benson, 1985; Qin and Gullan, 1989; Hodgson, 1994
(or Boraginaceae)
Cordia Triplaris
J
n 7!
TABLE 1.3.5.3 (continued)
Distribution
Cdds
Ants
Ant-plant genus
Plant f d y
Form of domatia
Reference
Neotropical (continued)
Cryprostigma quinqucpori (Newstead)
Azrcca alfari spp group+ & Azvca sp.
Cecropia
Cecropiaceae (or Moraceae)
Hollow stems
Morrison 1922, 1929; Bailey 1922b;
Cryprostigma reticukdaminac Morrison
Amca pim'eri complex (cited as A. longiceps)
Coda
Ehretiaceae
Hollow, swollen stems
Morrison, 1929; Wheeler, 1942; Qin and Gullan, 1989
Cryprostigma spp.
Azreca sp.
Albizia? Sapium? Sapium?
Leguminosae Euphorbiaceae Euphorbiaceae
Hollow branched stems
P.J. Gullan and P.S. Ward, unpublished
.
Pseudomynner viduus (F. Smith)
Oriental
Cyclolecanium hyperbarenun Morrison
A-ca pim'cri complex Cordia (cited as A. longiceps); Camponorus sp .; Cremarogaster sp.; Pseudomynner scnccus g p
Ehretiaceae
Hollow, swollen stems Morrison, 1929; Wheeler, 1942; Hodgson, 1994
Unidentified
Mynnclachista sp.
Duroia
Rubiacene
Hollow, swollen stems P.J. Gullan and P.S. Ward, unpublished
Coccus cavirm'colus Morrison C. circularis Momson C . macarangicolus Takahashi C. macarangar Morrison C. penangemis Momson C. sccretus Morrison C. tumulifm Momson
C. macarangicolus associated with Crematogasrcr sp.; others without ant data but probably associated mostly with Cremaiogasrer spp.+
Macaranga
Euphorbiaceae
Hollow stems or internodes
Morrison, 1921; Takahashi, 1952; Tho, 1978; Fiala and Maschwitz, 1990; Fiala, 1991
Unidentified
Cladomynna spp. A & B+ Saraca Crrmatogasrcr sp .
Leguminosae
Hollow internodes
Maschwitz et al., 1991a
Unidentified
Cladomynna sp. C+
Crypteroniaceae
Hollow internodes
Maschwitz et al., 1991a
Unidentified
Philidris cordatus Lecanoptcris (F. Smith) & Crematogaster ireubi Emerv
Polypodiaceae
Hollow or expanded rhiiomes
Gay and Hensen, 1992
Crypreronia
Relationships with ants
367
no obvious function other than the housing of ants (Beattie, 1985; H611dobler and Wilson, 1990). Ants gain shelter and often also food resources such as access to extrafloral nectaries (EFNs), food bodies (rich in lipids and proteins) or coccids, whereas the plants may derive protection from herbivores and/or competitors or obtain nutrients absorbed from the contents of the ant nests (Beattie, 1985; Benson, 1985; Huxley, 1986)(Fig. 1.3.5.6). Many domatia appear to have evolved from natural plant cavities which were utilised by ants and modified by selection (McKey, 1989). True domatia form independently of the presence of the ants, even in glasshouses from which ants are excluded. They may have become domiciles for homopterans only secondarily or else the homopterans may have been instrumental in the inception of some mutualisms by providing the food which drew the ants into a closer relationship with the plants (Benson, 1985; Ward, 1991). Specialised ant-coccid mutualisms involving domatia occur almost exclusively in tropical or subtropical areas (Table 1.3.5.3 and references therein). The likely explanation for this distribution is that most myrmecophytes are restricted to tropical vegetation because ants cannot survive cold conditions in thin-walled plant cavities
Fig. 1.3.5.6. Summarydiagram of possible interactions present in coccid-ant-myrmecophyteassociations. Direct positive (+), negative (-) and neutral (0) influences are shown. Various combinationsof these effects may operate in any given association, and the overall effect of the interactions on each participantwill depend on the relative magnitude of each individual effect.
Section 1.3.5 references, p. 371
368
Ecology (Benson, 1985). Coccids and sometimes also mealybugs (Pseudococcidae) have been recorded from the domatia of many of the classic myrmecophyte genera such as Cecropia, Cordia and Macaranga (references in Table 1.3.5.3; Longino, 1991; Ward, 1991). Notably, coccoids are absent from one well studied ant-myrmecophyte association, namely the Neotropical Pseudomyrmex ants in swollen-thorn Acacia (Ward, 1991), presumably because the plants supply the food requirements of the ants directly from EFNs and food bodies (Hblldobler and Wilson, 1990) rather than indirectly via coccoids. In other myrmecophyte genera, only some species may house ants that tend coccoids; for example, in the African ant-plant genus Leonardoxa, the ants associated with L. letouzeyi tend large numbers of coccoids in the hollow internodes, whereas the ants of L. africana do not tend any homopterans (McKey, 1991). An explanation for this differential behaviour of the ant species associated with L. letouzeyi and L. africana is that the latter host has large EFNs whereas those of the former are not very different in size and number from those of non-myrmecophytic species of Leonardoxa. Hence coccids can be functionally equivalent to the ant-attracting food resources that have evolved in many myrmecophytes. In the tropical plant genus Macaranga, myrmecophytic species, which house scale insects within their hollow stems, have reduced nectary production compared with non-myrmecophytes (Fiala and Maschwitz, 1992). This finding is interpreted as a means of saving plant assimilates and stabilising the association between Macaranga and its obligate ant partner, since access to scale insect honeydew is restricted to the domatia-living ants. Although coccids have been reported from at least some ant-plant genera in each of the major geographical regions where ant-plants occur (Table 1.3.5.3), their associations with ant-plants may be more prevalent than the literature indicates. Most recent researchers have concentrated on the interactions between the ants and the plants, with the coccoids frequently remaining unidentified and mentioned only in the context of potential ant food. This failure to include more detailed information on the coccoids of these systems is partly a consequence of the unavailability of expertise in coccoid identification. Most studies refer to both soft scale insects and mealybugs simply as "coccids" or "homopterans". Such records have been excluded from Table 1.3.5.3, which, therefore, underestimates the incidence of coccids in domatia. Certain genera of coccids, such as Cyclolecanium, Cryptostigma, Myzolecanium and the group of "Coccus" species associated with Macaranga, appear to be obligate inhabitants of ant nests, either in true domatia or, in the case of some species of Cryptostigma and Myzolecanium, sometimes inside live stems of non-myrmecophytes (Fig. 1.3.5.7). Conclusive data on the degree of specificity of coccid species to particular ant and plant species are generally lacking, although Myzolecanium species are known to associate with a number of different ant and plant genera (Gullan et al., 1993), in contrast to the Macaranga-inhabiting "Coccus" species which have been recorded
Fig. 1.3.5.7. Three coccids of a Myzolecanium sp. in the nest of Podomyrmalaevifrons F. Smith in the hollow stem of a sapling in Papua New Guinea, near Madang.
Relationships with ants
369
mostly from the nests of ants of Crematogaster species, especially of the subgenus Decacrema (unpublished data of B. Fiala, P.J. Gullan, H.-P. Heckroth and A. Moog, and see references in Table 1.3.5.3; Morrison (1921) acknowledges that these soft scale species were not true members of Coccus L.). Species of some other myrmecophilic coccid genera, such as Cribrolecanium (Green, 1921), Halococcus (Takahashi, 1951) and Houardia (Hodgson, 1990) are common inhabitants of ant nests in chambers in live stems of non-myrmecophytes. Ants may either construct the chambers by hollowing out the pithy stem or occupy hollow stems excavated by boring insects. The occurrence of coccids in live stems of non-myrmecophytes is poorly documented but probably widespread, so it is difficult to be certain of the specificity of coccid-ant and coccid-plant associations in true domatia. For example, in the Neotropics, where the specialised myrmecophytes have been relatively well studied, nesting by ants in live stems of other plants is a much more widespread phenomenon than is generally recognised and, almost universally, live stems occupied by ants contain coccoids (J.T. Longino, personal communication). Coccids obviously provide an important source of carbohydrates to plant-ants in the form of honeydew, although it is not known for most associations whether this supply is available continuously. For the coccids to qualify as ideal trophobionts they must fulfill Hrlldobler and Wilson's (1990, p. 524) criterion that their life cycles be Mnot tightly synchronised so that stages capable of producing honeydew are available throughout the year ~. Some Myzolecanium species from Papua New Guinea seem to satisfy this criterion (Gullan et al., 1993). However, ants also may consume the coccids that live in their nests, especially if the colony is heavily dependent on the coccids for food (Carroll and Janzen, 1973). Direct harvesting ofcoccoids (actually mealybugs and stictococcids) has been reported for certain plant-ants, such as Neotropical Pseudomyrmex species inhabiting Tachigali and Triplaris and African Tetraponera (formerly Pachysima) species inhabiting Barteria (Bailey, 1922b, 1923; Wheeler, 1942; Carroll and Janzen, 1973). However, it is unclear whether obligate Cecropia-inhabiting Azteca species utilise only the honeydew from the coccoids within their nests (Bailey, 1922b, 1923) or also directly harvest them for proteins and lipids (Carroll and Janzen, 1973). Probably both honeydew collection and eating of coccids occurs in most plant-ants, as suggested by Gullan et al. (1993) for the various ant associates of Myzolecanium species in Papua New Guinea. In some mealybug-ant mutualisms, the queen ant carries a mealybug in her mandibles during the nuptial flight, thus establishing a honeydew source for the newly-founded nest (reviewed by Hrlldobler and Wilson, 1990, p. 257, who incorrectly refer to mealybugs as coccids). Currently, there is no evidence that any queen ants carry coccid nymphs to new nests in this manner, possibly because the colony-founding queens of arboreal-nesting ants need unencumbered mandibles to chew into plant tissue. Ants of Crematogaster species which inhabit Macaranga (Euphorbiaceae) (Fiala and Maschwitz, 1990) and those of Cladomyrma species (Formicinae) associated with Saraca (Caesalpiniaceae) and Crypteronia (Crypteroniaceae) (Maschwitz et al., 1991 a), all from Malaysia, cultivate coccids and/or mealybugs within their myrmecophytes but the queens do not carry the coccoids on their nuptial flight. Worker ants, however, may later carry coccids into the newly-established nests. Alternatively, first-instar coccid nymphs may walk into ant nests via entrance holes made in stems by the ants. A study of the ontogeny of young ant colonies in myrmecophytes, including records of the first appearance of coccids (and mealybugs) in nests, for a variety of ant-plant associations would provide valuable data on the broader question of the role of trophobionts in the inception of ant-plant mutualisms. The available data on the establishment of coccoids within ant nests in myrmecophytes (Fiala and Maschwitz, 1990; Maschwitz et al., 1991a) suggest that the coccoids enter the nest chambers soon
Section 1.3.5 references, p. 371
Ecology
370
after colony initiation. Further studies may answer the question of whether the initial establishment of colonies in ant species that associate with coccoids is equally successful with and without the coccoids.
SUMMARY AND SUGGESTIONS FOR FUTURE RESEARCH Many ants attend coccids to collect honeydew but, in some ant-coccid associations, the ants also cull coccoids, perhaps as a source of protein and lipid or as a means of regulating their food resources. Ant attendance benefits coccids by deterring predators and parasitoids and, additionally, by removing the honeydew which can foul coccid aggregations and serve as a substrate for sooty moulds and perhaps other fungi. Ants may carry coccids in their mandibles to suitable feeding sites, even on different plants. l n d ~ , transport of coccids by ants may be a very widespread phenomenon, although it is not clear that all ants carry soft scales or that ants that do are indiscriminate in their selection of coccid species and instars. Frequently ants construct silk, carton or dirt shelters over the scales. Close association with ants, especially in shelters or nests, may reduce coccid disease because of antibiotic chemicals secreted by the ants. Such chemical protection may be most beneficial to coccids in tropical climates. Further applied research could focus usefully on the effects of ant metapleural gland secretions on the entomopathogenic fungi of the coccids, and on the ability of different ant species to disseminate the spores of such fungi. Experiments with cultivated plants have shown that ants foster coccids, often increasing their pest status. Nevertheless, some predatory ants that depend on honeydew, such as Oecophylla species, Dolichoderus thoracicus and Azteca species, may have uses in the biological control of a range of arthropod and even vertebrate pests (Way and Khoo, 1992). Thus, controlling soft scales by killing or excluding ants may increase populations of other plant pests that the ants either displace or prey upon. Floristically and structurally, more complex ecosystems may encourage beneficial ants that depend on honeydew. Studies of pest management in mixed plantings, in comparison to the more typical agricultural monocultures, neexl to consider coccid-ant relationships. In this regard, data on coccids and ants in natural ecosystems may have application to management of insect communities in our crops. Finally, the evolutionary ecology of ants and their mutualistic associations with many plants, especially myrmecophytes, is an expanding area of theoretical biology. The role of coccids in establishing and maintaining such associations may be a fruitful area for further studies. A major unknown factor is the specificity of coccids to both ant and myrmecophyte species.
ACKNOWLEDGEMENTS I am grateful to B. Bolton, J.T. Longino, S.O. Shattuck, R.W. Taylor and P.S. Ward for helping me to check the currently valid names of the ants mentioned here, but I take full responsibility for any remaining errors. G.W. Watson kindly obtained a few obscure references. D.J. Williams commented on the coccid records in one of the tables and has been my long-term mentor on all things coccidological. C.J. Hodgson has been immensely generous with his taxonomic data on coccid genera and has provided lively correspondence on all manner of coccid matters. Y. Ben-Dov, R.C. Buckley, P.S. Cranston, C.J. Hodgson, C.A.M. Reid and S.O. Shattuck made helpful comments on drafts of this Section. Karina Hansen Mclnnes is the biological artist who skillfully and patiently prepared the illustrations, in some cases from my less-than-perfect photographs and from pinned specimens of the ants.
Relationships with ants
371
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The scale insects of California. Part I: The soft scales (Homoptera: Coccoidea: Coccidae). Technical Series in Agricultural Biosystematics and Plant Pathology, California Department of Food and Agriculture, 1:132 pp. Grant, S. and Moran, V.C., 1986. The effects of foraging ants on arboreal insect herbivores in an undisturbed woodland savanna. Ecological Entomology, 11: 83-93. Green, E.E., 1921. On a new genus of Coccidae from the Indian region. Annals and Magazine of Natural History, (set. 9) 8: 639-644. Gullan, P.J., Buckley, R.C. and Ward, P.S., 1993. Ant-tended scale insects (Hemiptera: Coccidae: Myzolecanium) within lowland rain forest trees in Papua New Guinea. Journal of Tropical Ecology, 9: 81-91. Gullan, P.I. and Stewart, A.C., 1996. A new genus and new species of ant-associated coccid (Hemiptera: Coccidae: Myzolecaniinae) from Canthium I,am. (Rubiaceae). Memoirs of the Queensland Museum 39:307-314. Hackman, R.H. and Trikojus, V.M., 1952. The composition of honeydew excreted by Australian coccids of the genus Ceroplastes. The Biochemical Journal, 51: 653-656. Haines, I.H. and Haines, J.B., 1978. Pest status of the crazy ant, Anoplolepis longipes (Jerdon) (Hymenoptera: Formicidae), in the Seychelles. Bulletin of Entomological Research, 68: 627-638. Hanford, L., 1974. The African scale insect genus Udinia De Lotto (Coccidae). Transactions of the Royal Entomological Society of London, 126: 1-40. Hanks, L.M. and Sadof, C.S., 1990. The effect of ants on nymphal suvivorship of Coccus viridis (Homoptera: Coccidae). Biotropica, 22: 210-213. Hodgson, C.J., 1990. The scale insect genus Houardia Marchal (Homoptera: Coccidae). Systematic Entomology, 15: 219-226. Hodgson, C. J., 1994. The Scale Insect Family Coccidae: an Identification Manual to Genera. CAB International, Oxen, UK. 639 pp. Hrlldobler, B. and Engel-Siegel, H., 1984. On the metapleural glands of ants. Psyche, 91: 201-224. Hrlldobler, B. and Wilson, E.O., 1990. The Ants. The Belknap Press of Harvard University Press. Cambridge, Massachusetts, 732 pp. Huxley, C.R., 1986. Evolution of benevolent ant-plant relationships. In: B. Juniper and R. Southwood (Editors), Insects and the Plant Surface. Edward Arnold, London, pp. 257-282. Jutsum, A.R., Cherrett, J.M. and Fisher, M., 1981. Interactions between the fauna of citrus trees in Trinidad and the ants Atta cephalotes and Azteca sp. Journal of Applied Ecology, 18: 187-195. Leston, D., 1973. The ant mosaic - tropical tree crops and the limiting of pests and diseases. Pests Articles and News Summaries (Centre for Overseas Pest Research, London), 19: 311-341. Longino, J.T., 1991. Azteca Ants in Cecropia Trees: Taxonomy, Colony Structure, and Behaviour. In: C.R. Huxley and D.F. Cutler (Editors), Ant-Plant Interactions. Oxford University Press, Oxford, pp. 271-288. McKey, D., 1989. Interactions between ants and leguminous plants. In: C.H. Stirton and J.L. Zarucchi (Editors), Advances in Legume Biology. Monographs in Systematic Botany from the Missouri Botanical Garden Number 29: 673-718. McKey, D., 1991. Phylogenetic Analysis of the Evolution of a Mutualism: Leonardoxa (Caesalpiniaceae) and its associated Ants. In: C.R. Huxley and D.F. Cutler (Editors), Ant-Plant Interactions. Oxford University Press, Oxford, pp. 310-334. Majer, J.D., 1972. The ant mosaic in Ghana cocoa farms. Bulletin of Entomological Research, 62:151-160. Majer, J.D., 1976. The influence of ants and ant manipulation on the cocoa farm fauna. Journal of Applied Ecology, 13: 157- 175. Mann, W.M., 1922. Notes on a collection of West African myrmecophiles. Bulletin of the American Museum of Natural History, 45: 623-630. Maschwitz, U., Dumpert, K. and Schmidt, G., 1985. Silk pavilions of two Camponotus (Karavaievia) species from Malaysia: description of a new nesting type in ants (Formicidae: Formicinae). Zeitschrifl flit Tierpsychologie, 69(3): 237- 249. Maschwitz, U., Fiala, B., Moog, J. and Saw, L.G., 1991a. Two new myrmecophytic associations from the Malay Peninsula: ants of the genus Cladomyrma (Formicidae, Camponotinae) as partners of Saraca thaipingensis (Caesalpiniaceae) and Crypteronia griffithii (Crypteroniaceae). Insectes Sociaux, Paris, 38: 27-35.
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Maschwitz, U., Dumpert, K., Botz, T. and Rohe, W., 1991b. A silk-nest weaving Dolichoderine ant in a Malayan rain forest. Insectes Sociaux, Paris, 38: 307-316. Miller, N.C.E., 1931. Coccus (Lecanium) viridis Green. The "green scale" of coffee. Straits Settlements and Federated Malay States Department of Agriculture Scientific Series, No. 7:17-29. Molyneux, R.J., Campbell, B.C. and Dreyer, D.L., 1990. Honeydew analysis for detecting phloem transport of natural plant products. Implications for host-plant resistance to sap- sucking insects. Journal of Chemical Ecology, 16: 1899-1909. Monteith, G., 1990. The plant-ant connection. Wildlife Australia, 27: 6. Moreno, D.S., Haney, P.B. and Luck, R.F., 1987. Chlorpyrifos and diazinon as barriers to Argentine ant (Hymenoptera: Formicidae) foraging on citrus trees. Journal of Economic Entomology, 80: 208-214. Morrison, H., 1921. Some nondiaspine Coccidae from the Malay Peninsula, with descriptions of apparently new species. The Philippine Journal of Science, 18: 637-677. Morrison, H., 1922. On some trophobiotic Coccidae from British Guiana. Psyche, 29: 132-152. Morrison, H., 1929. Some neotropical scale insects associated with ants. (Hemiptera- Coccidae). Annals of the Entomological Society of America, 22: 33-00. Newstead, R., 1910. On two new species of African Coccidae. Journal of Economic Biology, 5" 18-22. Njeru, E.I., 1990. Control of coffee scale insect pests in Kenya -a review. Kenya Coffee, 55(641): 801-804. Nixon, G.E.J., 1951. The Association of Ants with Aphids and Coccids. Institute of Entomology, London, 36 pp. Qin, T.K. and Gullan, P.J., 1989. Cryptostigma Fen'is: a coccoid genus with a strikingly disjunct distribution (Homoptera: Coccidae). Systematic Entomology, 14: 221-232. Samways, M.J., Nel, M. and Prins, A.J., 1982. Ants (Hymenoptera: Formicidae) foraging in citrus trees and attending honeydew-producing Homoptera. Phytophylactica, 14: 155-157. Smith, M.R., 1942. The relationship of ants and other organisms to certain scale insects on coffee in Puerto Rico. The Journal of Agriculture of the University of Puerto Rico, 26: 21-27. Steyn, J.J., 1954. The pugnacious ant (Anoplolepis custodiens Smith) and its relation to the control of citrus scales at Letaba. Memoirs of the Entomological Society of Southern Africa, No. 3: 1-96. Strickland, A.H., 1950. The entomology of swollen shoot of cacao. I.- The insect species involved, with notes on their biology. Bulletin of Entomological Research, 41: 725-748. Sudd, J.H., 1987. Ant aphid mutualism. In: A.K. Minks and Harrewijn, P. (Editors), Aphids their Biology, Natural Enemies and Control. Volume 2A. Elsevier, Amsterdam, pp. 355-365. Sugonyayev, E.S., 1995. Ants nesting on living plants in the tropics as refuges for soft-scale insects (Homoptera, Coccidae, protecting them from attacks of chalcidoid parasites (Hymenoptera, Chalcidoidea). Zoologicheslfii Zhurnal, 74:80-87 (In Russian). [English translation in Entomological Review, 75: 120-127]. Takahashi, R., 1951. Three new myrmecophilous scale insects from the Malay Peninsula (Homoptera). Mushi, 22: 1-8. Takahashi, R., 1952. Some species of nondiaspine scale insects from the Malay Peninsula. Insecta Matsumurana, 18: 9-17. The, Y.P., 1978. Living in harmony. Nature Malaysiana, 3" 34-39. Van der Goot, P., 1916. Verdere onderzoekingen omtrent de oeconomische beteekenis der gramang-mier. Mededeelingen van het Proefstation Midden-Java, Salatiga, 22: 1-122. [summarised in English in Review of Applied Entomology, (A) 5: 273-276] Ward, P.S., 1991. phylogenetic analysis of pseudomyrmecine ants associated with domatia-bearing plants. In: C.R. Huxley and D.F. Cutler (Editors), Ant-Plant Interactions. Oxford University Press, Oxford, pp. 335-352. Way, M.J., 1954a. Studies on the life history and ecology ofthe ant OecophyUa longinoda Latreille. Bulletin of Entomological Research, 45: 93-112. Way, M.J., 1954b. 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. Way, M.J. and Khoo, K.C., 1992. Role of ants in pest management. Annual Review of Entomology, 37: 479-503. Wheeler, W.M., 1910. Ants. Their Structure, Development and Behavior. Columbia University Press, New York and London, 663 pp. Wheeler, W.M., 1942. Studies of Neotropical ant-plants and their ants. Bulletin of the Museum of Comparative Zoology, 90: 1- 262. Williams, D.J., 1982. The distribution and synonymy of Coccus celatus De Lotto (Hemiptera" Coccidae) and its importance on coffee in Papua New Guinea. Bulletin of Entomological Research, 72: 107-109. Williams, J. R. and Williams D.J., 1980. Excretory behaviour in soR scales (Hemiptera: Coccidae). Bulletin of Entomological Research, 70: 253-257. Young, G.R., 1982. Recent work on biological control in Papua New Guinea and some suggestions for the future. Tropical Pest Management, 28:107-114.
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Soft Scale Insects - Their Biology, Natural Enemies and Control
Y. Ben-Dov and C.J. Hodgson (Editors) 1997 Elsevier Science B.V.
375
1.3.6 Encapsulation of Parasitoids DANIEL BLUMBERG
INTRODUCTION Encapsulation is a common defense mechanism exerted by a host insect in response to invasion by a metazoan parasitoid or other foreign organisms. Encapsulation p e r se is a haemocytic reaction directed against parasitoids which are too large to be phagocytizeA by a single cell. It is also provoked by a variety of inert materials. The encapsulation ofparasitoids by host insects has been reviewed extensively by Salt (1963, 1968, 1970), Shapiro (1969), Nappi (1974, 1975), Whitcomb et al. (1974), Grtz (1975), Ratcliffe (1982), Ratner and Vinson (1983), Grtz and Boman (1985), Blumberg (1990), Vinson (1990, 1993) and others. In the process of cellular encapsulation, the host's blood cells (or haemocytes) surround and adhere to the surface of the invading object, forming a multicellular capsule-like envelope around it. Grtz (1986) described the sequence of events during cellular encapsulation and tentatively divided the process into ten consecutive steps, most of which are completed within 15 minutes, the entire reaction lasting between one and three days. A fully developed capsule is comprised of several types of haemocytes, the most recognize~ forms of which are prohaemocytes, plasmatocytes, oenocytoids, spherule cells, thrombocytoids and granular haemocytes. These cells differ in size, shape and function, as well as in their frequency among the total haemocyte population of a given insect species (Grtz and Bornan, 1985; Vinson, 1990). Since encapsulation is performed by the blood cells of the host, it is effective only against internal parasitoids, which insert their eggs and undergo their development within the host body. Very often, the innermost cells of the capsules formed around living organisms undergo melanization, with melanin being deposited on the surface of the encapsulated object. Melanization is less common when inert materials are encapsulated (Grtz and Boman, 1985). Melanin is formed principally during the oxidation and polymerization of phenols, such as tyrosine and dopa, by enzymes referred to collectively as phenoloxidases (Nappi, 1975). The importance of melanization in the encapsulation reactions of insects was demonstrated by using various phenoloxidase inhibitors, either by injection into the host body or by feeding. In this way melanin deposition was prevented and the amount of encapsulation was reduced (Brewer and Vinson, 1971; Nappi, 1973; Beresky and Hall, 1977). Another type of encapsulation is humoral, which entails the formation of a melanotic capsule around the parasitoid without direct participation ofhaemocytes. The occurrence of humoral encapsulation is correlated with low haemocyte counts, is formed rapidly in minutes and may be highly efficient against fungi, nematodes and bacteria, occurring in vivo as well as in vitro (Grtz and Boman, 1985). The capsule usually isolates parasitoid eggs or larvae in the insect host's haemocoel, causing their death by suffocation, starvation, or by the physical prevention of development. This explains why the capsule must be complete to be effective. Partially
Section 1.3.6 references, p. 384
376
Ecology
encapsulated parasitoids can survive and may continue to develop normally (Van den Bosch, 1964). Other effects of encapsulation may include inhibition of embryonic development (Muldrew, 1953; Bronskill, 1960), distortion of eggs and prevention of growth (Salt, 1955), prolongation of total parasitoid development, and reduction in the number of parasitoid progeny (Brewer, 1971; Blumberg, 1977). According to Salt (1970), any insect capable of encapsulation may encapsulate all internal parasitoids, except for a few species which are unmolested by the blood cells and, which, therefore successfully complete their parasitic development. These hostadapted species or strains have evolved specific adaptations and mechanisms which enable them to avoid encapsulation by their host. The various means by which insect parasitoids resist the internal defense reactions of their hosts were reviewed by Salt (1968) and Vinson (1990, 1993). Vinson (1990) divided the ways in which parasitoids may handle the insect immune system into five subcategories: avoidance, evasion, destruction, suppression and subversion. In this regard, it was found recently that females of many hymenopteran parasitoids in the families Braconidae and Ichneumonidae produce viruses (polydnaviruses) in their reproductive tracts (Edson et al., 1981; Stoltz et al., 1984; Vinson, 1990; Krell, 1991). The virus, which is injected into the host with the parasitoid egg, interferes with the production of immune factors by the host and thus protects the egg from encapsulation. The incidence of parasitoid egg encapsulation by a host insect is considered an important parameter of host suitability that can affect the fate and efficacy of an introduced parasitoid in new regions (Bess, 1939; Bartlett and Ball, 1966; Messenger and Van den Bosch, 1971; Dijkerman, 1990). High rates of encapsulation may account for outbreaks of insect pests, indirectly indicating the ineffectiveness of their parasitoids (Muldrew, 1953; Brewer, 1971). In the laboratory, this may hinder the mass rearing of a natural enemy (Reed et al., 1968; Hart, 1972; Blumberg, 1977). The intensity of the host's defensive reaction can change with time (Bouletreau, 1986). Through natural selection, a parasitoid can lose its effectiveness because of the development of immunological resistance by the host (Muldrew, 1953; Turnbull and Chant, 1961). On the other hand, by avoiding the host defense reaction, the parasitoid can gradually adapt itself to the host, with the result that parasitoid efficacy is enhanced (Messenger and Van den Bosch, 1971). Genetically based variations in encapsulation frequency are also known among Drosophila species (Carton and Bouletreau, 1985; Bouletreau, 1986). Different degrees of susceptibility to encapsulation in parasitoid species attacking the same host insect may confer upon the more resistant parasitoid an advantage, thereby enhancing its chances of survival. For example, the two encyrtid parasitoids, Metaphycus swirskii Annecke and Mynhardt and M. bartletti Annecke and Mynhardt were introduced into Israel in 1973 and 1976 respectively, to control the Mediterranean black scale, Saissetia oleae (Olivier) (Blumberg and Swirski, 1988). While M. swirskii is susceptible to encapsulation by mature scale insects, especially at 28" and 32~ M. bartletti is completely immune to encapsulation by all host stages, even at 32~ This, along with other biological differences between the two parasitoids, may explain why M. bartletti has displaced M. swirskii in the field and has very rapidly become the most abundant natural enemy of S. oleae (Blumberg and Swirski, 1982). The encapsulation of eggs of the parasitoid Comperiella bifasciata (Howard) (Hymenoptera: Encyrtidae) by the California red scale, Aonidiella aurantii (Maskell) (Homoptera: Diaspididae), in Australia (Brewer, 1971), as well as those of Metaphycus stanleyi (Compere) and M. swirskii by the pyriform scale, Protopulvinaria pyriformis Cockerell (Homoptera: Coccidae) in Israel (Blumberg, 1991, Blumberg et al., 1993), are examples of a reduced parasitoid efficacy in the field caused by a high prevalence of parasitoid encapsulation. The consistent effects of encapsulation in reducing effective parasitism in the field have also been demonstrated for the parasitoid, Bathyplectes curculionis (Thomson) (Hymenoptera: Ichneumonidae), in larvae of the alfalfa weevil, Hypera postica (Gyllenhall) (Coleoptera: Curculionidae) (Berberet et al., 1987).
Encapsulation of parasitoids
377
In superparasitized hosts, not all parasitoid eggs may be encapsulated, thus enabling one or more of them to avoid the reaction and to develop normally. This phenomenon, quite frequent in many associations of soft scale insects and their parasitoids, undoubtedly reduces the efficiency of the defense reaction and thereby favours the parasitoid and not the host. Two parameters can therefore be used for measuring encapsulation incidence in a superparasitize~ host: (i)the aggregate percentage of encapsulated eggs, and (ii) the percentage of parasitized hosts wherein encapsulation has completely prevented parasitoid development. This second parameter actually reflects the rate of efficient encapsulation (Blumberg, 1991). Encapsulation reactions by insect hosts depend greatly on the host and the parasitoid species, as well as on the environmental conditions under which the host and the parasitoid interact (Salt, 1963).
FACTORS AFFECTING ENCAPSULATION INCIDENCE BY SOFT SCALE INSECTS Most of the information on parasitoid encapsulation by soft scale insects (Table 1.3.6.1) relates to parasitoids which attack four species: the brown soft scale, Coccus hesperidum L.; the hemispherical scale, Saissetia coffeae (Walker); the Mediterranean black scale, S. oleae and the pyriform scale, P. pyriformis. Fig. 1.3.6.1 presents various types of encapsulation of parasitoid eggs and larvae in five species of soft scale insects. Among the important factors that may affect the frequency of parasitoid encapsulation in soft scale insects are (i) the host insect: its age, strain, physiological condition and whether or not it is superparasitized; (ii) the rearing temperature and (iii) the host plant.
THE HOST INSECT 1. Effect o f host age This has been demonstrated in nine parasitoid-host interactions (Table 1.3.6.1), in which parasitoid encapsulation became more frequent as the host matured. Encapsulation by scale insect nymphs was usually low, but the ovipositing female was often capable of encapsulating all parasitoid eggs and thus prevented any successful parasitism. Thus, the oviposition of Metaphycus helvolus and M. flavus in preovipositing females of S. coffeae and in the ovipositing females of C. hesperidum was greatly reduced because these host-stages encapsulated all the eggs of these parasitoids. This greatly reduces their effective parasitism and indicates that, whereas a certain host stage may be thought to be untouched by a parasitoid, it may nevertheless be parasitizexl and resist the parasitoid by encapsulation. Age-enhanced encapsulation is known to occur also in parasitoid-host interactions of other groups of insects (Schneider, 1950; Walker, 1959; Van den Bosch, 1964; Parker, 1971; Lynn and Vinson, 1977; Morris, 1976; Berberet, 1982; Van Driesche, 1988; Debolt, 1991). Salt (1963) suggested that the increased potency of the haemocytic reaction in larger individuals is to be attributed to the larger number of haemocytes available for reaction. Salt (1968) likewise concluded that "the real advantage of an early attack is that it allows the parasitoid progeny to become accepted by the blood cells of the host before vigorous defence reactions are possible." According to Lynn and Vinson (1977), the effect of increasing host age on increasing the incidence of parasitoid encapsulation could be due to an inadequate titer of (a) the enzymes necessary for degradation of the protective egg layer, or (b) recognition factor(s).
Section 1.3.6 references, p. 384
378
Ecology TABLE 1.3.6.1 Incidence of parasitoid encapsulation in 12 interactions of soft scale insects and their parasitoids, as affected by the physiological age of the host, rearing temperature and host plant. Abbreviations: N - Nymph; Y Young female; M - Fully grown female; L - laboratory; F - Field; G - Greenhouse; condit. - conditions; temp. - temperature; encap. - encapsulation; Citron - Citron melon fruit, C~trulus vulgaris; squash - squash fruit, Cucurbita moschata; potato - potato sprouts; unpub. - unpublished. Percent efficient encapsulation is the percentage of parasitized hosts wherein encapsulation has completely prevented parasitoid development.
Host insect
Parasitoid
Ceroplastes floridensis
Tetrastichus ceroplastae
Coccus hesperidum
Metaphycus flavus
Metaphycus helvolus
Host age
Rearing condit, and temp. ~
Host plant
L 20
Sweet lime 90
L 20
Hedera helix
27
Host plant
Ben-Dov, 1972
L 28 L 28 L 28
Squash Squash Squash
0 4 100
Host age
Blumberg, 1977
N + Y +M N + Y +M
L 28 L 28
Squash Oleander
10 46
Host plant
Blumberg, 1977
N Y M
L 28 L 28 L 28
Squash Squash Squash
45 50 100
Host age
Blumberg, 1977
N
L 20 L 27 L 33
Citron Citron Citron
87 93 100
Rearing temp.
Blumberg and DeBach, 1981
34 72
Host age
J.P. Kaas (unpub .) in Visser and van Alphen, 1987
Host age, rearing temp.
Blumberg and DeBach, 1981
Host age, host plant
Blumberg and DeBach, 1981
N Y M
L 27 L 27 L 27
Citron Citron Citron
5 10 41
N Y M
L 33 L 33 L 33
Citron Citron Citron
25 58 88
N Y M
F F F
Banana Banana Banana
8 39 68
N Y M
F F F
Citrus Citrus Citrus
15 64 88
lecaniorum
Y M M
L 28 L 28 L 32
Squash Squash Squash
18 84 99
Host age, rearing temp.
Blumberg and Goldenberg, 1992
Metaphycus stanleyi
Y
G 15-21 Hedera
6-17
Ambient temp.
Blumberg, 1991
Encyrtt~
Protopulvinaria pyriformis
References
N Y M
N M
Metaphycus stanleyi
% Factors efficient affecting encap, encap. incidence
Y
G 23-32
helix Schefllera 78-100 arboricola
Encapsulation of parasitoids
379
TABLE 1.3.6.1 (continued)
Host insect
Parasitoid
Host age
Rearing Host condit, plant and temp. *C
% Factors efficient affecting encap, encap.
Y
F 21-24
Avocado
0-11
Y
F 28-33
Avocado
54-75
Y
G 14-18 Sche2ffera 5-22 arboricola
Y
G 14-18
Avocado
Milviscutulus Metaphycus mangiferae swirskii
N Y
L 28 L 28
Mango Mango
Saissetia coffeae
Metaphycus helvolus
N Y M
L 28 L 28 L 28
Metaphycus flavus
N Y M
Metaphycus
Protopulvinaria
Metaphycus stanleyi
pyriformis
swirskii
Encyrms
infe~
Saissetia oleae
Metaphycus swirskii
References
incidence Rearing temp.
Blumberg, 1991
Host plant
Blumberg, 1991
0 9
Host age
Blumberg and Swirski, 1984
Potato Potato Potato
55 64 100
Host age
Blumberg, 1977
L 28 L 28 L 28
Potato Potato Potato
0 75 100
Host age
Blumberg, 1977
N N Y Y Y M
L L L L L L
Potato Potato Potato Potato Potato Potato
5-13 100 34 62-65 100 96-100
Host age, rearing temp.
Blumberg, 1988
Y Y
L 28 L 32
Potato Potato
2 21
Rearing temp.
Blumberg and Goldenberg, 1992
Y Y Y
L 24 L 28 L 32
Potato Potato Potato
3 0 43
Host age, Rearing temp.
Blumberg, 1982
M M M
L 24 L 28 L 32
Potato Potato Potato
21 41 97
16-28 32 16 20-28 32 16-32
0-2
2. Effect of host strain Different geographic races of the same insect host may react differently to the same parasitoid (Muldrew, 1953; Puttler, 1967), just as different strains of the same parasitoid species may react differently to a single host species (Salt and Van den Bosch, 1967; Blumberg and Luck, 1990). The different incidences of encapsulation of M. helvolus eggs by C. hesperidum in Israel, California and The Netherlands, as well as of M. swirskii eggs by the same host species in Israel and Greece (Table 1.3.6.2), may stem from the existence of biological strains of the host, to which the parasitoid is differently adapted. Bartlett and Ball (1966) reported that Encyrtus lecaniorum (Mayr)
380
Ecology
Fig. 1.3.6.1. A - Encapsulated egg ofMetaphycus helvoluswithin Coccus hesperidum. B - Encapsulated eggs of Metaphycus swirskii within Coccus hesperidum. C - Encapsulated larva of Metaphycus swirskiiwithin Coccus hesperidum. D - Encapsulated eggs ofMetaphycus swirskiiwithin Saissetiacoffeae. E - Young larva of Encyrtus infelixattached to a capsule which was formed by Saissetia coffeae. F - Young female of Protopulvinariapyriformis,parasitized by Metaphycus sp., which contains five encapsulated eggs together with a parasitoid pupa. G - Encapsulated eggs of Encyrtus infelixwithin a young female of Protopulvinaria pyrifonnis. H - Young female of Protopulvinariapyriformis, containing a pupa of Metaphycus sp. together with encapsulated eggs of Encyrtus in[el&. I - Encapsulated eggs of Tetrastichusceroplastae within the fig wax scale, Ceroplastes rusci. J- Parasitoid egg encapsulation within a young female of Coccus pseudomagnoliarum, collected on citrus in Porterville, California, in 1978.
Encapsulation of parasitoids
381
(Hymenoptera: Encyrtidae), originally taken from C. hesperidum in the Mediterranean area, produced progeny in 98 % of these scales in Texas but in only 2 % of the same species in California. In Texas, encapsulation of eggs of Microterys flavus (Howard) (Hymenoptera: Encyrtidae) by the California strain of C. hesperidum was less frequent than by the local strain of the host (Hart, 1972). Maund and Hsiao (1991) recorded significant differences in the incidence of encapsulation of Bathyplectes curculionis in three strains of its host, Hypera postica, and stresseA the importance of investigating the compatibility between host strains and their parasitoids in developing a sound biological control strategy.
TABLE 1.3.6.2 Incidence of parasitoid encapsulation in different strains of Coccus hesperidum.
Parasitoid
Metaphycus helvolus
Metaphycus swirskii
Origin of
Percent Fawatpsulation
Reference
C. hesperidum Israel
71-74
Blumberg, 1977
California
93-100
Blumberg and DeBach, 1981
The Netherlands
40
J.P. Kaas, (unpublished) in Visser and van Alphen, 1987
Israel
100
Blumberg, 1976, 1977
Greece
Not reported
Viggiani and Mazzone, 1977; Paraskakis et al. 1980
3. Effect of the host's physiological condition The health and vigor of the host are among several factors which affect the occurrence of an encapsulation response by an insect host (Salt, 1963; Van den Bosch, 1964; Messenger and Van den Bosch, 1971). Different procedures based on intentional weakening of soft scale insects, such as exposure of the host to extreme temperatures prior to parasitization, can bring about a significant reduction in the host's encapsulation ability by a yet unknown mechanism. Consequently, the mass rearing of parasitoids may be improved greatly. This was demonstrated by Blumberg (1976) for eggs of M. swirskii deposited in C. hesperidum and S. coffeae, as well as by Blumberg and Goldenberg (1992) for eggs of Encyrtus infelix (Embleton) deposited in P. pyriformis (Table 1.3.6.3). The extreme temperature of 40~ to which C. hesperidum and S. coffeae were subjected for 24 h before exposure to oviposition by M. swirsla'i, had the greatest effect on the reduction of encapsulation by the above two host species. The degree of reduction was affected by the physiological age of the host, being highest (100 %) in the nymphal stage and lowest (69 %) in reproducing female scales (Blumberg, 1982). Prevention of encapsulation of M. swirskii eggs was detected also in C. hesperidum which had been weakened by the prior parasitization of a Coccophagus species (Hymenoptera: Aphelinidae): none of the parasitoid eggs deposited in Coccophagus-parasitized scales became encapsulated. Likewise, a significant reduction in the ability of C. hesperidum to encapsulate M. swirskii eggs was recorded in these insects which, prior to their exposure to the parasitoid, had been weakened by removal from their host plant (oleander leaves) to a glass slide, or by detachment of infested oleander leaves from the plant itself (Blumberg, 1982). Information is also available on reducing the haemocytic reaction of an aphid (EI-Shazly, 1972), of noctuid caterpillars
Section 1.3.6 references, p. 384
Ecology
382
(Brewer and Vinson, 1971) and of beetle larvae (Van den Bosch, 1964), by changing diet composition, selected chemicals or starvation, respectively. 4. Effect of superparasitism As the number of parasitoids per host increases, the encapsulation reaction appears to decrease both in intensity (Van den Bosch and Dietrick, 1959; Salt, 1959) and incidence (Schneider, 1950; Puttler and Van den Bosch, 1959; Puttler, 1967). This has been attributed to a weakening of the host by excessive parasitism, thereby lessening its ability to produce a complete reaction (Salt, 1963; van Alphen and Visser, 1990). Superparasitism may, therefore, be considered as a mechanism by which the parasitoid circumvents the host defense system (Salt, 1968; Vinson, 1990). In the association of E. lecaniorum with C. hesperidum, where 84 % superparasitism was evident, the percent parasitized hosts with a developing parasitoid was much higher (95.1%) in superparasitized hosts, than in solitary parasitized ones (4.2%). This explains the significant difference between the aggregate percent of encapsulated eggs (64.8 %) and percent efficient encapsulation (18.4 %) (Blumberg and Goldenberg, 1992). Similarly, it was found (Blumberg and Luck, 1990) that multiple eggs of a California strain of Comperiella bifasciata were less likely to be encapsulated by Aonidiella aurantii than solitary eggs of the parasitoid. Superparasitism in the latter two parasitoid-host interactions may be an adaptation to the higher rates of encapsulation encountered by the solitary eggs of the parasitoids. The occurrence of superparasitism is, therefore, advantageous to the parasitoid, since it leads to more surviving progeny than solitary parasitism (Puttler, 1967; Streams, 1971; Giordanengo and Nenon, 1990).
TABLE 1.3.6.3 Effect of extreme high temperature (40"C), to which Coccidae species were subjected for 24 h prior to parasitization by two encyrtid parasitoids, on parasitoid egg encapsulation. + : Host insect exposed, - : Not exposed. Parasitoid
Host insect
Host plant
High temperature exposure
Metaphycus swirskii
Encyrtus infelix
Coccus hesperidum
Squash fruit
Saissetia coffeae
Potato sprouts
Protopulvinaria Hedera helix pyriformis
Fatsia japonica
-
% parasitoid
Reference
development
prevented by encapsulation 100
Blumberg, 1976
+
12.8
+
83.6 6
+
90-100 34
Blumberg and Goldenberg, 1992
+
90-100 50
Blumberg and Goldenberg, 1992
Blumberg, 1976
EFFECT OF THE REARING TEMPERATURE This has been demonstrated in seven host-parasitoid interactions (Table 1.3.6.1), in which the incidence of encapsulation increased with a rise in the rearing temperature. Within each physiological age range, the incidence of encapsulation of M. swirskii eggs
Encapsulation of parasitoids
383
in S. coffeae under laboratory conditions was not materially affected by temperatures ranging from 20 to 28~ but increased considerably from 27-28~ to 32-33~ This increase in encapsulation frequency was greater in mature than in young female scales. A positive correlation between the ambient temperature and encapsulation incidence was demonstrated for eggs of M. stanleyi in P. pyriformis, under both greenhouse and field conditions. The high rates of encapsulation which were recorded in Israel during the summer may account for the inability of M. stanleyi to exert efficient biological control of P. pyriformis in the field (Blumberg, 1991). Regarding seasonal variations in the host's defensive ability, encapsulation is sometimes more frequent in cooler than in warmer seasons (Hu, 1939; Flanders and Bartlett, 1964). Salt (1963) relates this occurrence to the slow development and inactivity of the host during the cold season. Lynn and Vinson (1977) reported temperature-dependent in vivo encapsulation of eggs of the parasitoid Cardiochiles nigriceps Viereck (Hymenoptera: Braconidae) by Heliothis spp. (Lepidoptera: Noctuidae). Van Driesche et al. (1986), however, noted that encapsulation rates of eggs of the parasitoid Apoanagyrus diversicornis (Howard) (Hymenoptera: Encyrtidae) by Phenacoccus herreni Cox and Williams (Homoptera: Pseudococcidae) were higher at 25 ~ than at 30~ in both nymphs and adults. Encapsulation of eggs of the parasitoid Habrolepis rouxi (Compere) (Hymenoptera: Encyrtidae) in A. aurantii was unaffected by the rearing temperature (Blumberg and DeBach, 1979). Likewise, Ben-Dov (1972) found that encapsulation of the parasitoid Tetrastichus ceroplastae (Hymenoptera: Eulophidae) by its host, Ceroplastesfloridensis Comstock (Homoptera: Coccidae), was as frequent at 20 ~ as at 28~ Berberet (1986) found no significant temperature-induced differences in percentage larvae of the curculionid Hypera postica that encapsulated the parasitoid B. curculionis. Walker (1959) found that efficient encapsulation of the cynipid parasitoid Pseudeucoila bochei Weld (Hymenoptera: Cynipidae) in Drosophila melanogaster Meigen was most frequent at temperatures between 18~ and 20~
THE HOST PLANT
The interaction among three trophic levels: the host plant, the insect herbivore and the natural enemy, may affect the immunity of insect pests to natural enemies (Price, 1986). Such an interaction, as regard parasitoid encapsulation, may explain the unique effect of the host plant on parasitoid-host relationships. Hence, parasitoid efficacy can sometimes be determined by the degree of immunity induced by the host plant to the host insect. One major reason for the failure of parasitoids of A. aurantii imported from the Orient to colonize in California in this century was the immunity conferred to the host scale by the host plant, which was manifested by encapsulation of parasitoid eggs, at least in part (Flanders, 1942; Smith, 1957; Compere, 1961). The effect of the host plant on the incidence of parasitoid encapsulation by soft scale insects in four parasitoid-host interactions is shown in Table 1.3.6.1. The influence of the host plant, for example, on the encapsulation of eggs of M. stanleyi by P. pyriformis suggests that a better control of the pest is likely to be achieved in scales growing on avocado than on Hedera helix or Schefflera arboricola. Table 1.3.6.4 demonstrates 12 parasitoid-host interactions in which six species of soft scale insects were found to be unsuitable for parasitic development due to high incidence of parasitoid encapsulation. In five of the interactions, complete encapsulation was recorded regardless of the rearing conditions of the host and parasitoid. In the other interactions, the hosts' unsuitability (due to high incidence of encapsulation) was caused either by the host age (mature females), the rearing temperature (32~ the host plant or by a combination of these factors.
Section 1.3.6 references, p. 384
384
Ecology TABLE 1.3.6.4 Host-parasitoid interactions in which soft scale insects were unsuitable for parasitic development due to high incidence of parasitoid encapsulation.
Host insect
Parasitoid
Percent encapsulation under the indicated conditions
Reference
Ceroplastes floridensis
Tetrastichus ceroplastae
90
In scales reared on rooted leaves of sweet lime, at 20* and 28~
Ben-Dov, 1972
Coccus hesperidum
Metaphycus swirskii
100
Regardless of host age, rearing temperature or host plant
Blumberg, 1976, 1977
Metaphycus
100
In fully grown females at 2 8 0 C
Blumberg, 1977
Metaphycus helvolus
100
In fully grown females at 2 8 0 C
Blumberg, 1977
Metaphycus stanleyi
88
In fully grown females at 330C
Blumberg and DeBach, 1981
Ency rtus infelix
1O0
Regardless of host age, rearing temperature or host plant
Blumberg and Goldenberg, 1992
Encyrt/~
84-99
In fully grown females at 28-32"C
Blumberg and Goldenberg, 1992
100
At 32.2~
Reed et al., 1968
Encyrtus infelix
100
Regardless of host age, rearing temperature or host plant
Blumberg and Goldenberg, 1992
Protopulvinaria Encyrtus pyriformis infelix
100
Regardless of host age, rearing temperature or host plant
Blumberg and Goldenberg; 1992
Pulvinaria urbicola
Encyrtus
1O0
Regardless of host age, rearing temperature or host plant
Blumberg and Goldenberg, 1992
Saissetia coffeae
Metaphycus swirskii
100
In nymphs and young females at 32~ in fully grown females at 16, 20, 24, 28 and 320C
Blumberg, 1988
Saissetia oleae
Metaphycus swirskii
97
In fully grown females at 32~
Blumberg, 1982
~vus
lecaniorum Encyrtus
lecaniorum Parasaissetia nigra
infelix
REFERENCES Bartlett, B.R. and Ball, J.C., 1966. The evolution of host suitability in a polyphagous parasite with special reference to the role of parasite egg encapsulation. Annals of the Entomological Society of America, 59: 42-45. Ben-Dov, Y., 1972. Life history of 7etrastichus ceroplastae (Girault) (Hymenoptera: Eulophidae), a parasite of the Florida wax scale, Ceroplastesfloridensis Comstock (Homoptera: Coccidae) in Israel. Journal of the Entomological Society of Southern Africa, 35: 17-34. Berberet, R.C., 1982. Effects of host age on embryogenesis and encapsulation of the parasite Bathyplectes curculionis in the alfalfa weevil. Journal of Insect Pathology, 40: 359-366. Berberet, R.C., 1986. Relationship of temperature to embryogenesis and encapsulation of eggs of Bathyplectes curculionis (Hymenoptera: lchneumonidae) in larvae ofHyperapostica (Coleoptera: Curculionidae). Annals of the Entomological Society of America, 79: 985-988.
Encapsulation of parasitoids
385
Berberet, R.C., Wilson, L.J. and Odear, M., 1987. Probability for encapsulation of eggs of Bathyplectes curculionis (Hymenoptera: lchneumonidae) by larvae of Hypera postica (Coleoptera: Curculionidae) and resulting reduction in effective parasitism. Annals of the Entomological Society of America, 80: 483-485. Beresky, M.A. and Hall, D.W., 1977. The influence of phenylthiourea on encapsulation, melanization, and survival in larvae of the mosquito Aedes aegypti parasitized by the nematode Neoaplectana carpocapsae. Journal of Invertebrate Pathology, 29: 74-80. Bess, H.A., 1939. Investigations on the resistance of mealybugs (Homoptera) to parasitization by internal hymenopterous parasites, with special reference to phagocytosis. Annals of the Entomological Society of America, 32: 189-226. Blumberg, D., 1976. Extreme temperatures reduce encapsulation of insect parasitoids by their insect hosts. Experientia, 32: 1396-1397. Blumberg, D., 1977. Encapsulation of parasitoid eggs in soft scales (Homoptera: Coccidae). Ecological Entomology, 2: 185-192. Blumberg, D., 1982. Further studies of the encapsulation ofMetaphycus swirsla'iby soR scales. Entomologia Experimentalis et Applicata, 31: 245-248. Blumberg, D., 1988. Encapsulation of eggs of the encyrtid wasp, Metaphycus swirskii, by the hemispherical scale, Saissetia cofl'eae: effects of host age and rearing temperature. Entomologia Experimentalis et Applicata, 47: 95-99. Blumberg, D., 1990. Host resistance: encapsulation of parasites. In: D. Rosen (Editor), The Armored Scale Insects, Their Biology, Natural Enemies and Control. Elsevier Science Publishers B.V., Amsterdam, The Netherlands, Vol. B, pp. 221-228. Blumberg, D., 1991. Seasonal variations in the encapsulation of eggs of the encyrtid parasitoid Metaphycus stanleyi by the pyriform scale, Protopulvinaria pyriformis. Entomologia Experimentalis et Applicata, 58:231-237. Blumberg, D. and DeBach, P., 1979. Development ofHabrolepis rouxi Compere (Hymenoptera: Encyrtidae) in two armoured scale hosts (Homoptera: Diaspididae) and parasite egg encapsulation by California red scale. Ecological Entomology, 4: 299-306. Blumberg, D. and DeBach, P., 1981. Effects of temperature and host age upon the encapsulation of Metaphycus stanleyi and Metaphycus helvolus eggs by brown soR scale Coccus hesperidum. Journal of Invertebrate Pathology, 37: 73-79. Blumberg D. and Goldenberg, S., 1992. Encapsulation of eggs of two species of Encyrtus (Hymenoptera: Encyrtidae) by sol~ scales (Homoptera: Coccidae) in six parasitoid-hostinteractions. IsraelJournal of Entomology, 25-26: 57-65. Blumberg, D. and Luck, R.F., 1990. Differences in the rates of superparasitism between two strains of ComperieUa bifasciata(Howard) (Hymenoptera: Encyrtidae) parasitizingCalifornia red scale (Homoptera: Diaspididae): an adaptationto circumvent encapsulation? Annals of the Entomological Society of America, 83:591-597. Blumberg, D. and Swirskii, E., 1982. Comparative studiesof the development of two species of Metaphycus (Hymenoptera: Encyrtidae),introduced intoIsraelfor the control of the Mediterranean black scale,Saissetia oleae (Olivier)(Homoptera: Coccidae). Acta OEcologica/OEcologica Applicata, 3: 281-286. Blumberg, D. and Swirsld, E., 1984. Response of three soR scales (Homoptera: Coccidae) to parasitization by Metaphycus swirskii. Phytoparasitica,12: 29-35. Blumberg, D. and Swirski, E., 1988. ColonizationofMetaphycus spp. (Hymenoptera: Encyrtidar for control of the Mediterranean black scale, Saissetia oleae (Olivier)(Homoptera: Coccidae). In: R. Goren and K. Mendel (Editors),Proceedings of the Sixth InternationalCitrus Congress, Tel Aviv, Israel,pp. 1209-1213. Blumberg, D., Wysoki, M. and Hadar, D. 1993. Further studiesof the encapsulationof eggs of Metaphycus spp. (Hymenoptera: Encyrtidae) by the pyriform scale,Protopulvinariapyriformis (Homoptera: Coccidae). Entomophaga, 38: 7-13. Bouletreau, M., 1986. The genetic and coevolutionary interactionsbetween parasitoidsand theirhosts. In: J.K. Waggr and D. Greathead (Editors),Insect Parasitoids. 13th Symposium of the Royal Entomological Society of London, pp. 169-200. Brewer, R.H., 1971. The influence of the parasite ComperieUa bifasciata How. on the populations of two species of armoured scale insects,AonidieUa aurantii (Mask.) and A. citrina (Coq.) in South Australia. Australian Journal of Zoology, 19: 53-63. Brewer, F.D. and Vinson, S.B., 1971. Chemicals affectingthe encapsulationof foreign materialsin an insect. Journal of Invertebrate Pathology, 18: 287-289. Bronskill, J.F., 1960. The capsule and itsrelationto embryogenesis of the ichneumonid parasitoidMesoleius tenthredinis Morl. in the larch sawfly, Pristiphora erichsonii (Htg.). Canadian Journal of Zoology, 38: 769-775. Carton, Y. and Bouletreau, M., 1985. Encapsulation abilityof Drosophila melanogaster: a genetic analysis. Developmental and Comparative Immunology, 9:21 I-219. Compere, H., 1961. The red scale and its natural enemies. Hilgardia,31: 173-278. Debolt, J.W., 1991. Behavioral avoidance of encapsulation by Leiophron uniformis (Hymenoptera: Braconidae), a parasitoidof Lygus spp. (l-lemiptera:Miridae): relationshipbetween host age, encapsulating ability,and host acceptance. Annals of the Entomological Society of America, 84: 444-446.
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Ecology Dijkerrnan, H.J., 1990. Suitability of eight Yponomeuta species as hosts of Diadegma armiUata. Entomologia Experimentalis et Applicata, 54: 173-180. Edson, K.M., Vinson, S.B., Stoltz, D.B. and Summers, M.D., 1981. Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid's host. Science, N.Y., 211: 582-583. EI-Shazly, N.Z., 1972. Der Einfluss von Ernahrung und Alter des Muttertieres auf die hamocytare Abwehrreaktion yon Neomyzus circumflexus (Buck.). Entomophaga, 17: 203-209. Flanders, S.E., 1942. Abortive development in parasitic Hymenoptera, induced by the food-plant of the insect host. Journal of Economic Entomology, 35: 834-835. Flanders, S.E. and Bartlett, B.R., 1964. Observations on two species [of] Metaphycus (Encyrtidae, Hymenoptera) parasitic on citricola scale. Mushi, 38: 39-42. Giordanengo, P.L. and Nenon, J.P., 1990. Melanization and encapsulation of eggs and larvae of Epidinocarsis lopezi by its host Phenacoccus manihoti; effects of superparasitism and egg laying patterns. Entomologia Experimentalis et Applicata, 56: 155-163. G6tz, P., 1975. Immunoreactions in insects. In: Animal Research and Development. Institute for Scientific Co-operation, Eugen Gobel, Tubingen, Vol. 1, pp. 44-56. G6tz, P., 1986. Encapsulation in arthropods. In: M. Brehelin (Editor), Immunity in Invertebrates. SpringerVerlag, Berlin, pp. 153-170. G6tz, P.and Boman, H.G., 1985. Insect immunity. In: G.A. Kerkut and L.I. Gilbert (Editors), Comprehensive Insect Physiology, Biochemistry and Pharmacology. Pergamon Press, Oxford, UK. Vol. 3, pp. 453-485. Hart, W.G., 1972. Compensatory releases of Microterysflavus as a biological control agent against brown sot~ scale. Environmental Entomology, 1: 414-4 19. Hu, S.M.K., 1939. Observations on the development of filarial larvae during the winter season in Shanghai region. American Journal of Hygiene, 29: 67-74. Krell, P.J., 1991. Polydnaviridae. In: J.R. Adams and J.R. Bonami (Editors), Atlas of Invertebrate Viruses. CRC Press, Boca Raton, Florida. pp. 321-338. Lynn, D.C. and Vinson, S.B., 1977. Effects of temperature, host age and hormones upon the encapsulation of Cardiochiles nigriceps eggs by Heliothis spp. Journal of Invertebrate Pathology, 29: 50-55. Maund, C.M. and Hsiao, T.H., 1991. Differential encapsulation of two Bathyplectes parasitoids among alfalfa weevil strains, Hypera postica (Gyllenhal). The Canadian Entomologist, 123: 197-203. Messenger, P.S. and Van den Bosch R., 1971. The adaptability of introduced biological control agents. In: C.B. Huffaker (Editor), Biological Control. Plenum Press, New York, pp. 68-92. Morris, R.F., 1976. Influence of genetic changes and other variables on the encapsulation of parasites by Hyphantria cunea. The Canadian Entomologist, 108: 673-684. Muldrew, J.A., 1953. The natural immunity of the larch sawfly Pristiphora erichsonii (Htg.) to the introduced parasite, Mesoleius tenthredinis Morley, in Manitoba and Saskatchewan. Canadian Journal of Zoology, 31: 313-332. Nappi, A.J., 1973. The role of melanization in the immune reaction of larvae of Drosophila algonquin against Pseudeucoila bochei. Parasitology, 66: 23-32. Nappi, A.J., 1974. Insect hemocytes and the problem of host recognition of foreignness. In: E.L. Cooper (Editor), Contemporary Topics in Immunology. Plenum Press, New York, Vol. 4, pp. 207-224. Nappi, A.J., 1975. Parasite encapsulation in Insects. In: K. Maramorosch and R.E. Shope (Editors), Invertebrate Immunity. Academic Press, New York, NY, pp. 293-326. Paraskakis, M., Neuenschwander, P. and Michelakis, S., 1980. Saissetia oleae (Oliv.) (Hom. Coccidae) and its parasites on olive trees in Crete, Greece. ZeitschriR fiir angewandte Entomologie, 90: 450-464. Parker, F.D., 1971. Management of pest populations by manipulating densities of both hosts and parasites through periodic releases. In: C.B. Huffaker (Editor), Biological Control. Plenum Press, New York, NY, pp. 365-376. Price, P.W., 1986. Ecological aspects of host plant resistance and biological control: interactions among three trophic levels. In: D.J. Boethel and R.D. Eikenbarry (Editors), Interactions of Plant Resistance and Parasitoids and Predators of Insects. Ellis Horwood Ltd. Publishers, Chichester, UK, pp. 11-30. Puttler, B., 1967. Interrelationship ofHypera postica (Coleoptera: Curculionidae) and Bathyplectes curculionis (Hymenoptera: lchneumonidae) in the eastern United States with particular reference to encapsulation of the parasite eggs by the weevil larvae. Annals of the Entomological Society of America, 60: 1031-1038. Puttler, B. and Van den Bosch, R., 1959. Partial immunity of Laphygma exigua (Hubner) to the parasite Hyposoter exiguae (Viereck). Journal of Economic Entomology, 52: 32%329. Ratcliffe, N.A., 1982. Cellular defence reactions of insects. Fortschritte der Zoologic, 27. Zbl. Bakt. Suppl. 12: Immune Reactions to Parasites. Fischer, Stuttgart, FRG, pp. 223-244. Ratner, S. and Vinson, S.B., 1983. Phagocytosis and encapsulation: cellular immune responses in Arthropoda. American Zoologist, 23: 185-194. Reed, D.K., Hart, W.G. and Ingle, S.I., 1968. Laboratory rearing of brown sof~ scale and its hymenopterous parasites. Annals of the Entomological Society of America, 61 : 1443-1446. Salt, G., 1955. Experimental studies in insect parasitism. VIII. Host reactions following artificial parasitization. Proceedings of the Royal Society, London, B, 144: 380-398. Salt, G., 1959. Experimental studies in insect parasitism. XI. The haemocytic reaction of a caterpillar under varied conditions. Proceedings of the Royal Society, London, B, 151: 446-467.
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Salt, G., 1963. The defence reactions of insects to metazoan parasites. Parasitology, 53: 527-642. Salt, G., 1968. The resistance of insect parasitoids to the defence reactions of their hosts. Biological Reviews, 43: 200-232. Salt, G., 1970. The Cellular Defence Reactions of Insects. Cambridge Monographs in Experimental Biology, No. 16. Cambridge University Press, Cambridge, UK, 118 pp. Salt, G. and Van den Bosch, R., 1967. The defense reaction of three species of Hypera (Coleoptera, Curculionidae) to an ichneumon wasp. Journal of Invertebrate Pathology, 9: 164-177. Schneider, F., 1950. Die abwehrreaktion des Insektenblutes und ihre Beeinflussung durch die Parasiten. Vierteljahrsschrit~ der Naturforschung Gesellschafl in Zfirich, 95: 22-44. Shapiro, M., 1969. Immunity of insect hosts to insect parasites. In: G.J. Jackson, R. Herman and I. Singer (F_Aitors), Immunity to Parasitic Animals. Appleton, New York, NY, Vol. I, pp. 211-228. Smith, J.M., 1957. Effects of the food plant of California red scale, Aonidiella aurantii (Mask.) on reproduction of its hymenopterous parasites. The Canadian Entomologist, 89: 219-230. Stoltz, D.B., Krell, P., Summers, M.D. and Vinson, S.B., 1984. Polydnaviridae - A proposed family of insect viruses with segmented, double-stranded, ctrcular DNA genomes. Intervirology, 21" 1-4. Streams, F.A., 1971. Encapsulation of insect parasites in superparasitized hosts. Entomologia Experimentalis et Applicata, 14: 484-490. Turnbull, A.L. and Chant, D.A., 1961. The practice and theory of biological control of insects in Canada. Canadian Journal of Zoology, 39: 697-753. van Alphen, J.J.M. and Visser, M.E., 1990. Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology, 35: 59-79. Van den Bosch, R., 1964. Encapsulation of the eggs of Bathyplectes curculionis (Thomson) (Hymenoptera: Ichneumonidae) in larvae of Hypera brunneipennis (Boheman) and Hypera postica (Gyllenhal) (Coleoptera: Curculionidae). Journal of Insect Pathology, 6: 343-367. Van den Bosch, R. and Dietrick, E.J., 1959. The interrelationships of Hypera brunneipennis (Coleoptera: Curculionidae) and Bathyplectes curculionis (Hymenoptera: Ichneumonidae) in southern California. Annals of the Entomological Society of America, 52: 609-616. Van Driesche, R.G., 1988. Field levels of encapsulation and superparasitism for Cotesia glomerata (L.) (Hymenoptera: Braconidae) in Pieris rapae (L.) (Lepidoptera: Pieridae). Journal of the Kansas Entomological Society, 61: 328-331. Van Driesche, R.L., Bellotti, A., Herrera, C.J. and Castillo, J.A., 1986. Encapsulation rates of two encyrtid parasitoids by two Phenacoccus spp. of cassava mealybugs in Columbia. Entomologia Experimentalis et Applicata, 42: 79-82. Viggiani, G. and Mazzone, P., 1977. Notizie preliminari sulla introduzione in Italia di Metaphycus aff. stanleyi Comp. e Diversinervus elegans Silv. (Hym. Encyrtidae), parasiti di Saissetia oleae (Olivier). Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', 37: 171-176. Vinson, S.B., 1990. How parasitoids deal with the immune system of their host: an overview. Archives of Insect Biochemistry and Physiology, 13: 3-27. Vinson, S.B., 1993. Suppression of the insect immune system by parasitic Hymenoptera. In: J.P.N. Pathak (Editor), Insect Immunity. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 171-187. Visser, M.E. and van Alphen, J.J.M., 1987. Metaphycus helvolus (Hymenoptera" Encyrtidae), a biological control agent of Coccus hesperidum (Homoptera: Coccidae). Mededelingen van de Faculteit Landbouwwetenschar en Rijksuniversiteit, Gent, 52:319-328. Walker, I., 1959. Die Abwehrreaktion des Wirtes Drosophila melanogaster gegen die zoophage Cynipide Pseudeucoila bochei Weld. Revue Suisse de Zoologic, 66: 569-632. Whitcomb, R.F., Shapiro, M. and Granados, R.R., 1974. Insect defense mechanisms against microorganisms and parasitoids. In: M. Rockstein (F_xlitor), The Physiology of Insecta, 2nd edition. Academic Press, New York, NY, Vol. 5, pp. 447-536.
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Sql'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.
389
Chapter 1.4 Techniques 1.4.1 Collecting and Mounting YAIR BEN-DOV and CHRIS J.HODGSON
INTRODUCTION Only a few species of soft scale insects can be identified by studying their general live appearance, host plant or infestation site, while many cannot even be placed in a genus! Therefore, the majority of species have to be determined by microscopic study of carefully processed, slide-mounted specimens. This need for adequately prepared specimens was recognized even in the middle of the last century (e.g., Signoret, Targioni Tozzetti). Subsequent workers, such as Green (1896), Newstead (1903) and Steinweden (1929) proposed specific methods for the preparation and mounting of scale insects for microscopic study and these have recently been refined and improved, e.g., Cilliers (1967), Kozarzhevskaya, (1968), Williams & Kosztarab (1972) and Wilkey (1990). This chapter discusses the collection and storage of Coccidae and then outlines methods which should allow preparation of high quality microscope slides, both from fresh material and from that which has been stored for long periods (either in liquid or dry). It concentrates mainly on nymphal and adult female stages, but includes a short section on adult males. It also outlines methodologies for restaining previously mounted material for further study.
COLLECTION Soft scale insects may occur on any part of their host plants, from the roots to the fruit. Some species are fairly obvious, due to the presence of white ovisacs and thick, sometimes brightly coloured, wax covers, but others are not easily detected, either because they often blend with the environment or because they are concealed. A collector may increase his success by looking for intensive ant activity, honeydew droplets and/or sooty mould. On trees, soft scales are commonly present on the branches (particularly in protected and shaded parts of the trunk), leaves, in bark crevices, forks between twigs or other sheltered areas of the plants. On all plants, it is important to pay special attention to such neglected areas as roots, root crowns, leaf sheaths, both sides of grass leaves, fruits, galls and areas under bark flakes. In addition, specimens can often be found on dried plant material in herbaria. Whilst some Coccoidea may be found in leaf litter (e.g., mealybugs and eriococcids) soft scales are almost never found away from their host plant. Male soft scales are often found closely associateA with the females but the male crawlers of several species settle on different parts of the host plant or even on different plants, when they can be difficult to associate with their conspecific females. Males can also be collected in suction traps, on
Section 1.4.1 references, p. 395
390
Techniques
coloured, sticky traps or at light sources and the correct association of these males with their conspecific females might be impossible. This is, of course, not the case when they have been attracted by sex pheromones. In order to secure high-standard, slide-mounted specimens, it is almost essential to collect the teneral adult female within a short period following its final moult because, in most species, the body then expands and the dorsum becomes sclerotised. Collecting young specimens is comparatively easy in multivoltine species because the populations generally include nymphal instars and various ages of adult female. However, with univoltine species, especially those from cool and temperate regions, special efforts are often required to obtain such specimens, as they are generally only available for a short period each year.
PRESERVATION AND STORAGE Whilst it is strongly recommended to mount material on slides immediately after collection, it may be necessary to store it for future study. In any case, it can be useful to store the excess material for later examination.
Wet preservation Although specimens which have been stored in various liquids do not generally make as satisfactory slides as those made from dried material, good preparation can be made even years later with care and patience. It is here recommended that the best storage media is acid alcohol, either acetic acid alcohol or lactic acid alcohol (see Table 1.4.1.1). The problem with these media is that the alcohol can quickly evaporate and the specimens then dry out. Because of this, the liquid neeAs to be topped up from time to time. The best storage containers are glass bottles with a metal screw-on cap and a thick rubber washer. Alternatively, the small bottles can themselves be stored in large bottles full of alcohol, which can be easily topped-up when necessary. Whilst much heavier and requiring careful packaging, liquid-stored material travels much better than dried material, but every effort should be made to remove all trapped air. Air bubbles in the bottle can be almost as damaging as the jolting of dried material. As with all stored material, the bottles should be individually labelled, preferably with full collection and other data.
Dry preservation Specimens collected even one hundred years ago and kept in a dried state can be made into excellent slides. Storage of material in a dry state is, therefore, an option but needs care because many Coccidae contain much water and so need to be dried out before storage, either by gentle heating or by keeping them in a dry atmosphere (perhaps with silica gel). However, as with storage in alcohol, there are problems with the storage of dry material. Firstly, the specimens may be damaged by museum beetle, which can be devastating. The stored scales, therefore, need to be kept in air-tight containers, preferably with naphthalene. Secondly, the dry insects become extremely brittle and can easily lose their setae, legs and antennae. This can be a major problem if the material is handled or moved around much. On the other hand, they do not need to be checked at such regular intervals as material stored in liquids if they are stored in solid, reasonable insect-proof cabinets. Dried stored specimens should be kept in small cardboard, glass or plastic containers, preferably wrapped in tissue paper rather than cotton wool to prevent the specimens from moving. They should then be stored in strong, insect-proof cabinets. Sending dried material through the post is not recommended as the juddering will knock the specimens together and cause much damage. All specimens need to be labelled as fully as possible.
Collecting and mounting
391
SLIDE PREPARATION There are a number of publications outlining various staining and mounting techniques for scale insects, such as Cilliers (1967) and Williams and Kosztarab (1972) for the Coccidae, McKenzie (1967) and Williams and Granara de Willink (1992) for the Pseudococcidae and Wilkey (1990) for the Diaspididae. Whilst these methods are suitable for soft scales, we consider that many of them are not always satisfactory due to the larger size of many adult soft scale females. It is also here considered that, for all stages, including the nymphs and adult males, only permanent mounts, using Canada balsam, are useful and valuable for taxonomic study.
Procedure for preparing permanent microscope slides Firstly, the best slides will always be made from freshly collected material. Whatever the age of the material, the methodology usually involves the same five or six stages, i.e. initial fixation, maceration, dehydration, staining, cleating, final dehydration and mounting. The exact procedures used by workers can vary considerably, each person evolving their own preferred methodologies. However, the following procedure should be tried in the first instance and should allow the preparation of high quality microscope slides of all stages of soft scales for permanent storage. The recipes for the various chemicals used below are given in Table 1.4.1.1. Comments and alternative procedures are given after this methodology.
Initialfixation: live specimens should be fixed in a mixture of acetic acid alcohol (see Table 1.4.1.1) for 1-2 minutes. All specimens should be fixed, even if they are going to be mounted immediately. If necessary, material can also be stored in acid alcohol for long periods (see under preservation and storage above). 0
3i.
3ii.
0
0
Maceration: make an incision (probably best medio-laterally in the abdomen) and transfer to 10 % potassium hydroxide (KOH) at room temperature for 12-24 hours. Clearing specimens with KOH can be quickened by slight warming, but it is strongly recommended that this should never exceed 40~ as specimens which have been boiled or over-heated can be unstainable. Heavily sclerotised specimens can be left in cold KOH for at least a week. Dehydration: transfer, by means of a small spatula, to water and gently pump or press out body contents. The pumping out of body contents and the general handling of specimens needs to be done very gently and special care should be taken not to break off the various appendages and setae, which are almost certainly needed for identification. Nonetheless, clearing the body of all contents is vital and the procedures towards staining should not be continued until as much contents as possible has been removed. Transfer to clean water and then gradually add glacial acetic acid (GAA) to replace the water until the concentration of GAA = about 70% and then transfer to 100% GAA. Staining: add to the 100% GAA solution (in which the specimens are contained) acid fuchsin, at the rate of one drop to every 1-2 cc GAA; retain in staining solution for 1-24 hours. Washing: transfer to GAA to wash out excess stain.
Section 1.4.1 references, p. 395
392
Techniques 0
Q
Clearing: if any wax or fatty material is still present on or in the specimens, add a drop of xylene to the GAA solution to dissolve the wax; retain for 15-30 minutes. Final fixation" transfer to oil of cloves for 24 hours. Although 24 hours is not essential, this should ensure the full displacement of water (dehydration) from the specimens, which otherwise could cloud the Canada balsam.
0
Mounting: place a small drop of Canada balsam on the slide and transfer the specimen to it. Gently push the specimen so that it is at the bottom of the drop of Canada balsam and then cover with a cover-glass. Except with very convex specimens, the cover-glass should not be pressed down. It is recommended to use No. 0 or thinner cover-glasses to allow their use at oil-immersion magnifications. Placing the cover glass over a freshly-prepared slide may result in the specimen drifting away from under the cover-glass. To avoid this, place the specimen in a minute drop of Canada balsam and arrange it on the slide; then place the slide in a covered petri-dish (to prevent dust particles from sticking to the Canada balsam) and allow the surface of the drop of balsam to dry between 15 minutes and 24 hours. Then place a drop of Canada balsam on the cover-glass and cover.
0
Label slide. The future scientific value of the specimen will depend on the data on the slide. Unless the accession book is kept with the slides, no collection data will be available and the slides are almost useless. An unlabelled slide is useless.
10.
Keep slides to cure at 40~ for 4-6 weeks. Slides should not be cured for longer than about 6 weeks, as this may cause darkening of the Canada balsam.
TABLE 1.4.1.1 Chemicals and formulae Acid akohois: a. acetic acid alcohol: b. lactic acid alcohol:
4 parts 96 % ethyl alcohol to 1 part glacial acetic acid. 2 parts 96 % ethyl alcohol to 1 part lactic acid.
Acid fuchsin stain:
either dissolve about 0.7g acid fuchsin in 300 cc lactophenol or 0.5g acid fuchsin + 25cc 10% HCI + 300 cc water.
Carbol xylene:
3 parts xylene to 1 part carbolic acid crystals.
Chloral-phenol:
warm equal parts by weight of chloral hydrate and phenol until liquid. This will keep in a liquid form for several months but needs to be stored in a dark bottle.
Lactophenol:
composed of phenol 100g + 100 cc lactic acid + 100 cc glycerine + 200 cc water.
IT NEEDS TO BE STRESSED THAT SEVERAL OF THESE CHEMICALS ARE CARCINOGENIC AND THEY SHOULD BE HANDLED AND DISPOSED OF WITH GREAT CARE.
ALTERNATIVE METHODS AND PROCEDURES In the following notes, the numbers refer to the points in the above procedure. 9
Initial fixation: an alternative acid alcohol is lactic acid alcohol (see Table 1.4.1.1.). Soft scales can present a number of problems: (i) many specimens of soft scales are covered in wax which can be difficult to remove and (ii) their dorsum may be heavily sclerotised. In addition, stored material can offer
Collecting and mounting
393
particular problems: alcohol-stored specimens can be difficult to prepare. On the other hand, dried specimens are best completely rehydrated before treatment with KOH. Under these conditions, it can be beneficial to soak specimens in Decon 90 for about 12-24 hours (Banks and Williams, 1972). It has been found that Decon 90 produces very soft and malleable, specimens from which the test and other contents can be easily removed. In addition, with small specimens, it may not even be necessary to transfer to KOH at all, so long as the body contents is completely removed. Following use of Decon 90, specimens neexl to be thoroughly washed, otherwise troublesome granulations can appear - although these can be removed by soaking in 1% acetic acid.
Maceration: species which are rather membranous can present problems in
0
determining the distribution of the ducts and pores. These are almost always critical for the identification or description and it will be important to determine to which surface they belong. This can be overcome by cutting the specimens round the margin and then mounting the two halves on the same slide. Whilst this needs practice and care, it is best done under a binocular microscope using two fine needles or a very fine pair of scissors, either prior to maceration in KOH or once it has been cleared and is in 95 % alcohol.
Dehydration: an alternative to using lactophenol and GAA for dehydration is to
0
use alcohol. Using this method, the specimen is transferred through a range of alcohol concentrations (30 %, 50 %, 70 %) to 96 %. The specimen should be left in each of these for at least 5 minutes and preferably longer. If the specimen still contains granules of wax at this stage, or some of the waxy test still adheres, the specimen should be transferred to 100% alcohol for about 5 mins and then into carbol xylene for about 5 mins. It should then be placed back in the absolute alcohol, GAA or acetic acid alcohol and stained as above. If the specimen still does not clear, it can be taken down through the alcohols and macerated again in KOH, although it is much better to leave it in the original KOH for the correct period of time. .
Staining: membranous specimens can be hard to stain and so it may be necessary to increase the number of drops of acid fuchsin to 2-3 drops in each 2 cc of acetic acid alcohol - or, of course, the specimen can be left in the stain for longer. The specimens should then be washed several times in GAA or absolute alcohol to ensure complete removal of all water.
.
0
"
Washing: excess stain can also be washed out using 95 % alcohol. Clearing: See 3 above. In addition, specimens can also be cleared in cold chloral-phenol or by heating it gently for a few minutes (Martin, 1987). Final fixation: this can also be done in xylene, although this does make the specimens more brittle than oil of cloves. An alternative medium is histolene. It should be noted that xylene is carcinogenic and is therefore dangerous.
"
Mounting: several synthetic mounting media have been introduced recently (e.g., Emexel, Euparol, Piccolyte). Specimens mounted in some of these media shrink within 2-3 years and the media darkens, making the specimens unusable for taxonomic study and so they are not recommended.
Section 1.4.1 references, p. 395
394
Techniques REMOUNTING OLD SLIDES Acid fuchsin stain tends to fade from permanent-mounted specimens after about 10 years. It is, therefore, often necessary to remount and restain old slide-mounted specimens, especially when undertaking taxonomic revisions. However, specimens can only be stained a few times and so this should only be undertaken if absolutely necessary. The following notes might be helpful to those requiting to remount slides. lit
0
0
Q
0
Remove the labels from the slides by immersion in water, so long as the writing is in pencil or indian ink. This is strongly recommended because the ink of handwritten labels often fades in the course of the remounting procedure. It is probably a wise precaution to photocopy the slide before starting the process, so that you have a copy of the label for later use. If a lot of slides are to be remounted, the glass of each slide should then be labelled with an identification mark to ensure that they are identifiable, either in indian ink or with a diamond glass marker. As most mounting media dissolve in xylene, it is recommended that this should be tried first. Place the slide with the cover-glass downwards in xylene in a tightly-closed petri-dish. Depending on the age of the slide, loosening of the cover-glass may require two or more days. We have successfully remounted 100year old slides, which necessitated up to seven days to soften and dissolve the Canada balsam. Leave the slide face-down in the xylene until the cover-glass separates from the slide when the slide is gently lifted. Do not attempt to force the separation of the cover-glass, otherwise the specimens will be damaged and setae, legs and antennae can be broken. As soon as the specimens are loose in xylene, transfer them either to glacial acetic acid or to absolute alcohol and then stain and mount as outlined above for preparation of permanent slides. Some students of the last century used to mount specimens in a water-soluble mounting media. If the mountant does not dissolve in xylene, try water.
MOUNTING AND STAINING OF ADULT MALES Adult male coccids are very fragile and special care is often necessary in handling and transferring them through the staining procedure. In addition, whilst the immature stages and adult females tend to be dorso-ventrally flattened, the body of adult males is cylindrical and normal mounting procedures tend to distort the body and the true relationships of structures then becomes very difficult to determine, particularly those laterally. Nonetheless, it may be necessary to stain and mount as described above if the specimen is to be stored permanently, although extra care will need to be taken in transferring the specimens through the solutions to prevent damage and also to ensure that there is little or no shrinkage. The latter can be reduced if small amounts of one chemical is gradually added to the other chemical before the specimen is transferred. However, for a proper study and understanding of male structure, it is necessary to follow the techniques developed by workers specialising in male taxonomy (e.g., Theron, 1958; Ghauri, 1962; Giliomee, 1967; Afifi, 1968).
Collecting and mounting "
395
Maceration: the specimens should be cleared of muscle and soft tissue in 10% KOH, this can be warmed gently for about 1 hour; alternatively they can be kept in cold KOH at least overnight or a little longer.
11,
Dehydration: the specimens are then washed in distilled water and dehydrated by passing through a series of ethyl alcohol solutions from 30 % to absolute alcohol.
0
.
Q
Staining" the specimens should then be transferred to a solution of Chlorazol Black E (this is not washed out by either alcohol or terpineol) for about 0.5-1.0 hour. Washing: excess stain is removed by returning the specimen to absolute alcohol. Ghauri (1962) found that this process, which can take several hours, could be quickened by adding a few drops of pyridine. Mounting and storage: the method favoured by the above specialists is the flotation technique of Pantin (1948). Terpineol is placed in a small dish and absolute alcohol carefully added so that the terpineol and alcohol form two separate layers, the alcohol on top. The specimens are then transferred to the dish where they will initially lie in the alcohol layer above the terpineol, but will then slowly sink as the alcohol is gradually replaced by the terpineol; this gradual replacement prevents shrinkage. The alcohol is then decanted and the specimens transferred to fresh terpineol, in which they can be stored for some years. The specimens can then be examined in terpineol (in a cavity slide for instance) from any angle, so that the true relationships of the various structures can be determined.
REFERENCES Afifi, S., 1968. Morphology and taxonomy of the adult males of the families Pseudococcidae and Eriococcidae (Homoptera: Coccoidea). Bulletin of the British Museum (Natural History), Entomology Supplement 13. 210 pp. Banks, H.J and Williams, D.J., 1972. Use of the surfactant, Decon 90, in the preparation of coccids and other insects for microscopy. Journal of the Australian Entomological Society, 11: 347-348. Cilliers, C.J., 1967. A comparative biological study of three Ceroplastes species (Hem., Coccidae) and their natural enemies. Entomology Memoirs, Department of Agricultural Technical Services, Republic of South Africa, 13: 1-59. Ghauri, M.S.K., 1962. The morphology and taxonomy of male scale insects (Homoptera: Coccoidea). British Museum (Natural History), London. 221 pp. 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. 168 pp. Green, R.E., 1896. The Coccidae of Ceylon. Part 1. Dulau & Co., London. 101 pp. Kozarzhevskaya, E.F., 1968. Methods of preparing slides for Coccid (Homoptera, Coccoidea) determination. Entomologicheskoe Obozrenie, 47: 248-253. Martin, J.H., 1987. An identification guide to common whitefly pest species of the world (Homoptera, Aleyrodidae). Tropical Pest Management, 33: 298-322. McKenzie, H.L., 1967. Mealybugs of California with Taxonomy, Biology, and Control of North American Species (Homoptera; Coccoidea; Pseudococcidae). University of California Press, Berkeley. 526 pp. Newstead, R., 1903. Monograph of the Coccidae of the British Isles. Vol. 2. Ray Society, London. 270 pp. Pantin, C.F.A., 1948. Notes on Microscopical Technique for Zoologists. Cambridge University Press, Cambridge. 75 pp. Steinweden, J.B., 1929. Bases for the generic classification of the coccoid family Coccidae. Annals of the Entomological Society of America, 22: 197-245. 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 + 42 figs. Wilkey, R.F., 1990. Collection, preservation and microslide mounting. In: D. Rosen (Exlitor), Armoured Scale Insects, their Biology, Natural Enemies and Control. Vol. 4A. Elsevier, Amsterdam, pp. 345-352. Williams, D.J. and Granara de WiUink, M.C., 1992. Mealybugs of Central and South America. C.A.B. International, Wallingford. 635 pp. 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: 1-215.
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So.ft Scale Insects - Their Biology. Natural Enemies and Control
Y. Ben-Dov and C.J. Hodgson (Editors) 1997 Elsevier Science B.V.
397
1.4.2 Laboratory and Mass Rearing MIKE ROSE and STEVE STAUFFER
INTRODUCTION It may be necessary to rear coccids in the laboratory for a number of reasons. Some soft scales have been cultured to examine their effects on the biochemistry and physiology of economically or ecologically significant host plants (Schaffer and Mason, 1990; Speight, 1991), but most species have been cultured for studies on higher trophic levels and have emphasized biosystematic, ecological and behavioral research on coccid pests and/or their natural enemies. Historically, the great majority of coccid cultures have been for establishing and maintaining cultures of natural enemies for use in applied biological control programs conducted against a pest species. In fact, of the more than seventy publications cited here, forty-two deal primarily with the rearing or biological study of parasitic Hymenoptera. Therefore, any review of coccid rearing methodologies must necessarily emphasize procedures inherent in the introduction and subsequent culture or mass rearing of natural enemies. Nevertheless, the techniques and principles described here are applicable to rearing requirements in general. Prior to the introduction of new natural enemies, particularly parasites (referred to as parasitoids by other hymenopterists and in various Sections of this book) through foreign exploration or collaboration, it is usually necessary to establish and develop laboratory cultures of several scale insect species to serve as both natural and unnatural hosts (DeBach, 1964). The introduction of new natural enemies by direct release in the field may be a more immediate and simple strategy than by insectary culture. However, this approach may be precluded by several factors: the possession of only small numbers of natural enemies initially; the possibility that unwanted organisms might also be introduced; the complicated and/or unknown reproductive modes of the natural enemies, and the current quarantine regulations. Newly introduced parasite species are often obtained from host species not present in the area of introduction. In such cases, several appropriately chosen, often closely related, host species, including the target pest species, should be available from cultures for initial exposure to the new parasites. Thus, ideally, the scale insect species selected for culture would include: (1) the target species, (2) the original host of the imported parasites, and (3) some readily cultured, closely-related, unnatural hosts. This strategy maximizes the probability of initiating viable laboratory cultures of the parasites. The rearing of scale insect predators presents slightly different problems to those experienced when rearing parasites. Most predators require large quantities of eggs and young scale insects as prey. For example, Mani and Krishnamoorthy (1990) found that individual larvae of the coccinellid Cryptolaemus montrouzieri Mulsant consumed an average of 3,766 eggs of Chloropulvinaria psidii (Maskell) during an average laboratory lifetime of 17.6 days. Unnatural hosts that are highly fecund could, therefore, prove very advantageous when rearing predators. In addition, some predators require the
Section 1.4.2 references, p. 416
398
Techniques
presence of male scale insect nymphs to ensure successful completion of their larval development. Nohara and Iwata (1988) found that the nitidulid Cybocephalus gibbulus (Erichson) needed the nymphs of at least seventy male armored scale insects to complete development and these authors speculated that the nymphs of male scale insects were more suitable food for young predator larvae than female nymphs. This could also be true for soft scale predators. In classical biological control programs, the goal is to establish new natural enemies by introducing them into the field where they can assist in regulating the pest. In such programs, laboratory cultures may only be necessary for relatively short periods. Longer lasting cultures may be required in other types of programs, ranging in size from small laboratory studies on the biology and behavior of natural enemies to large mass cultures for augmentative colonization. Regardless of the type of program, culture systems for natural enemies consist of host plant material on which the host insect is reared, which, in turn, then supports the predator or parasite. In this regard, it is important to note that populations of a given species of scale insect vary in their susceptibility to parasitization by natural enemies. For example, the encyrtid Metaphycus luteolus (Timberlake) is a highly effective parasite of Coccus hesperidum L. in California and elsewhere (e.g., in Russia, 1959) but, during the late 1950's, attempts to introduce M. luteolus into the citrus groves of southern Texas were unsuccessful because the Texas populations of C. hesperidum proved unsuitable for the development of the parasite (Bartlett and Ball, 1966). Some years later, Hart (1972) reported that, in order to avoid high rates of egg encapsulation, it was necessary to rear the encyrtid Microterys nietneri (Motschulsky) (=M. flavus (Howard)) in Californian populations of C. hesperidum rather than in Texan populations. The work of Bartlett and Ball (1966) and, in particular, that of D. Blumberg (Blumberg, 1976, 1977, 1988, 1991; Blumberg and DeBach, 1981; Blumberg and Goldenberg, 1992; Blumberg, et al., 1993) has done much to elucidate the mechanisms of parasite egg encapsulation by various soft scale species. Blumberg (1982) also showed that it was possible to significantly reduce encapsulation in C. hesperidum by exposing the scale insect to either high or low temperatures for varying lengths of time. Using his method, Blumberg successfully reared Metaphycus swirskii Annecke and Mynhardt on temperature-weakened C. hesperidum, a species that otherwise successfully resisted its development. Coccids must be reared on living plants or on plant parts, such as their fruit. Our review of the literature has shown that no artificial diets appear to have been developed for coccids; in particular, the difficulties of preventing contamination by pathogens and of suppressing putrefaction of an artificial nutrient substrate (which must support the development of a sessile organism with sucking mouthparts for a period of weeks or even months) have not been overcome (R.K. Morrison, personal communication, 1993). Host plant selection should be based on several broad criteria. Foremost, the host plant must be acceptable and nutritionally adequate so that the scale insects develop into maximum-sized adults at a high enough rate and at a suitable sex ratio to allow an increase in population size with each generation (Clausen, 1940; Muegge and Lambdin, 1989b; Argov et al., 1987). In the case of mass culture systems adapted for the 'Equilibrium Method of Parasite Production' (DeBach and White, 1960), there must be an absolute minimum of at least one suitable scale insect host produced for each reproducing female parasite during each exposure period. Another important requirement is a continuous excess of healthy host plant material free of other pests and chemical residues. Fruits and other plant parts must be capable of withstanding periods of storage and of supporting the development of both the scale insect and its parasites for a period of some weeks. Other desirable qualities of the host plant material include: (i) suitable size for handling, (ii) resistance to injury and subsequent rotting, and (iii) a sufficient surface area to support a large scale insect
399
Laboratory and mass rearing
Table 1.4.2.1 Rearing methods and environmental conditions for the maintenance of various soft scale insect cultures.
Coccid
References
Lab Host(s)
Plant part(s)
Conditions * C, % RH
Eisa et al., 1991
Psidium guava L.
plant
28-1- 2", 65-t- 5 %
Argov and R6ssler, 1988
Myrtus communis L.
plant
22-27", 80-t- 10% 12L:12D
Argov et al., 1987
Myrtus communis L. Hedera helix L.
plants plants
22-27 ~ 80+ 10% 12L: 12D
Ben-Dov, 1972
Citrus (limena) t
rooted leaves detached leaves
?
rooted leaves fruits
26*
..... Ceroplastes floridensis Comstock
Hedera helix L.
Ben-Dov, 1970
Citrus limetta Cucurbita moschata var. "Hyuga"
?
20-22 ~
Ceroplastes pseudoceriferus Green
Kawai and Tamaki, 1967
Cucurbita moschata var. "Hyuga ~
fruits
Ceroplastes rusci (L.)
Ben-Dov, 1970, 1972
Cucurbita moschata var. "Hyuga"
fruits
20-22 ~
Coccus hesperidum L.
Blumberg and Goldenberg, 1992
Cucurbita moschata
fruits
24+ 2", 60-70%
Muegge and Lambdin, 1989a,b
Ci trullus vul g aris var. "citroides "
fruits 16L:8D
2 7 " + 2, 60+ 10%,
Asplenium nidus L.
plants
Nerium oleander L. Dieffenbachia (sequina)
plants plants
"glasshouse"
Hart, 1983
Citrullus vulgaris var. "citroides "
fruits
26.5 ~
Kfir et al., 1983
Citrullus vulgaris var. "citroides "
fruits
Blumberg, 1982
Cucurbita sp. Nerium oleander L.
fruits plants
Blumberg and DeBach, 1981
Citrullus vulgaris vat. "citroides "
fruits
27 ~, 50-60%
Kfir and Rosen, 1980
Cf trullus vul g aris var. "citroides "
fruits
26.7 ~, constant darkness
Ingle et al., 1979
Cucurbita moschata
fruits
Vinson et al., 1978
Ci trullus vul g a ris var. "citroides "
fruits
Blumberg, 1976
Nerium oleander Cucurbita sp.
plants fruits
Kfir et al., 1976
Cf trullus vul g aris var. "citroides "
fruits
Visser and van Alphen, 1987
Section 1.4.2 references, p. 416
loom
temperature
26.5 ~
400
Techniques
TABLE 1.4.2.1 (continued)
Coccid
References
Lab Host(s)
Plant
part(s)
Conditions
*C, %RH
Ingle et al., 1975
Ci trullus vul g a ris var. "citroides "
fruits
Kfir et al., 1975
Citrullus vulgaris var. "citroides"
fruits
Jarraya, 1975
Cucurbita sp. var. "russe "
fruits
25 +2", 65+5%
Pappas and Tzoras, 1975
Citrus limon Citrus medica
plants plants
25-28", 65-70% 25-28*, 65-70%
Samsinakova and Kalalova, 1975
Citrus sp.
plants
"glasshouse"
Hart and Ingle, 1971
Citrus paradisi
potted seedlings
Avidov and Podoler, 1970
Citrullus vulgaris var. "citroides"
fruits
25 ~
Ben-Dov, 1970
Citrus limetta
rooted leaves
26 ~
Reed et al., 1968
Citrullus vulgaris var. "citroides "
fruits
26.5 *
Bartlett and Ball, 1966
Citrullus vulgaris var. "citroides "
fruits
Bartlett and Lagace, 1961
Citrullus vul garis var. "citroides "
fruits
26.7*, constant darkness
Citrus sp. Gardenia augusta
seedlings seedlings
25 ~ 25 ~
Bess, 1958
Citrus sinensis
plants
Hawaii, outdoors, July-March
Blumberg and Goldenberg, 1992
Cucurbita moschata
fruits
Cucurbita moscham
fruits
24 ~
Solanum tuber, sum
sprouts
24 ~
Pefia et al., 1987
Carica papaya
plants green fruits
27+ 2*, 75+ 3%, 10L:14D
Blumberg and Goldenberg, 1992
Hedera helix Fatsia japonica
plants plants
Blumberg, 1991
Hedera helix Schefflera (arboricola) z
plants plants
"greenhouse" 2 "insectary"
Pulvinaria sp.
Muzaffar and Ahmad, 1977
Cucurbita maxima
fruits
25+ 2*
Pulvinaria regalis Canard
Speight, 1991
Aesculus hippocastanum 171ia cordata T. europa T. platyphyllos Acer pseudoplatanus
plants plants plants plants plants
Oxford, UK, outdoors
Solanum tuber, sum
detached sprouts
24:!: 2*, 60-70%
Coccus hesperidum
(continued)
Coccus viHdis (Green)
Parasaissetia nigra (Nietner)
Su and Lin, 1986
Ben-Dov, 1978
var. "Butternut"
Philephedra tuberculosa
Nakahara and Gill Protopulvinaria pyriformis
(Cockerell)
Pulvinaria Blumberg and urbicola Cockerell Goldenberg, 1992
401
Laboratory and mass rearing
TABLE 1.4.2.1 (continued) Conditions *C, % R H
Coccid
References
Lab Host(s)
Plant part(s)
Pulvinariella mesembryanthemi (Vallot)
Wilk and Kitayama, 1981
Carpobrotus edulis
plants
Saissetia coffeae (Walker)
Blumberg and Goldenberg, 1992
Solanum tuberosum
detached sprouts
24+ 2 ~, 60-70%
Blumberg, 1988
Solanum tuberosum
sprouts
22-26 ~ 60%
Walter, 1988
Trichilia emetica Solanum tuberosum
plants green sprouts
9
Ibrahim and Copland, 1987
Solanum tuberosum var. "Comet 90"
green sprouts
18, 20, 22, 24, 26, 28, 30 ~
Blumberg and Swirski, 1977
Solanum tuberosum
detached sprouts plants fruits
22-26 ~ 60 %,
Adhatoda vasica s Citrullus vulg a ris var. "citroides " squash ~
Saissetia oleae (Olivier)
9
"glasshouse" 9
fruits
Blumberg, 1976
Solanum tuberosum
detached sprouts
9
Ben-Dov, 1970
Cucurbita moschata var. "Hyuga ~
fruits
20-22 ~
Blumberg and Goldenberg, 1992
Solanum tuberosum
detached sprouts
24+ 2 ~ 60-70%
Argov and R6ssler, 1988 Solanum tuberosum
sprouts
Blumberg, 1988
Solanum tuberosum
sprouts
Blumberg, 1982
Solanum tuberosum
detached sprouts
Blumberg and DeBach, 1981
Solanum tuberosum
sprouts
27 ~, 50-60%
Viggiani and Mazzone, 1980
Solanum tuberosum
sprouts
23-250, 60-80%
Clematis vitalba
plants
Solanum tuberosum
detached sprouts plants
22-260, 60%
Blumberg and Swirski, 1977
Nerium oleander
22-26 ~, 60%
"glasshouse"
Ben-Dov, 1970
Citrus (limena) 1
rooted leaves
26 ~
Smith, 1921
Solanum tuberosum
detached sprouts
?
Saissetia privigna De Lotto
Muzaffar and Ahmad, 1977
Cucurbita maxima
fruits
25 -1- 2 ~
Toumeyella sp.
Schaffer and Mason, 1990
Guaiacum sanctum
plants
"glasshouse", 25-30 ~
Notes to Table 1.4.2.1 1 This species does not appear in the 1976 edition of Hortus Third. 2 Greenhouse temperature - 14.5 18.5 o. 3 This host produced good mother stock, but was less convenient than potato sprouts for rearing parasites. 4 Squashes of the Butternut, Russian and Mediterranean strains were used with satisfactory but inconsistent results.
Section 1 9
references, p. 416
Techniques
402
population (see DeBach and White, 1960; Blumberg and Swirski, 1977; see particularly Argov et al. (1987) for greater detail). Examples of host plants that have been utilized for laboratory and greenhouse rearing of coccids are summarized in Table 1.4.2.1. Ben-Dov (1993), Gill (1988, 1987), Hamon and Williams (1984) and the Sections in Chapter 3.3 of this volume provide references to Coccidae - host plant associations. These associations could also prove valuable in the development of rearing methodologies for coccid species not shown in Table 1.4.2.1. Scale insect cultures are initiated by transferring the eggs and mobile first-instar nymphs (crawlers) to scrupulously clean (free of other organisms and toxic materials) host plant material. Continual infestation of clean host plant material takes place in the space assigned to the mother or master culture. Infestation can be accomplished by several methods: the mother culture can be placed in direct contact with, or immediately above, the clean host plant material to allow auto-transfer of mobile nymphs; or mobile first-instar nymphs can be mass-collected (e.g., by light attraction) and transferred; or eggs and nymphs may be hand-collected from reproducing females and then transferred to clean hosts, but this is much the most time consuming method. However, the hand collection of egg masses (e.g., from Pulvinaria spp.) or the lifting of the body of suitable scale species when initiating cultures often exposes developing parasites, predaceous mites and the eggs and larvae of other organisms that may be present in field collected material. Of course, any organisms other than the specific scale insect sought for culture should be removed during the initiation of the culture. In many rearing schemes, crawlers have been mass-collected using a lighted collector box (Fig. 1.4.2.1) modelled after those developed by DeBach and White (1960) and then adapted for use with soft scale insects by Bartlett and Lagace (1961). These crawler collecting cages are designed to take advantage of the phototropic nature of scale crawlers. Shelves (Figs 1.4.2.2, 1.4.2.3) have also been used for crawler collection in mass rearing programs. Crawlers gathered in this manner are then gently brushed or knocked onto host plant material.
i!
l
Fig. 1.4.2.1. Light box for collecting the crawlers of Coccidae, suitable for laboratory cultures.
Many coccids, such as C. hesperidum, remain mobile beyond the first instar. Transfer of such species can be induced by allowing infested leaf and/or stem cuttings to desiccate
Laboratory a n d
mass
rearing
403
while in contact with suitable replacement host plants or fruits. For example, at Texas A&M University, colonies of C. hesperidum were initiated by inducing young nymphs to move from infested cuttings of Malabar spinach, Basella alba L., to fruits of Citrullus vulgaris Schrad var. "citroides" and Cucurbita moschata var. "All-Season''.
285/8, ,~~ Y 20"
Fig. 1.4.2.2. A large collector for the crawlers of Coccidae. The light source is in front of the collector. Adapted from DeBach and White (1960).
L/
IV
Fig. 1.4.2.3. A segment of a large crawler collector, suitable for mass-rearing. Adapted from DeBach and White (1960).
Section 1.4.2 references, p. 416
404
Techniques As with all culture techniques, the newly infested host plant material should be dated and then moved immediately away from the mother culture when the crawlers have settled. This settling is generally done in the dark to avoid the crawlers crowding at points of light. All material infested on the same date should be held in an area separate from the mother culture. This isolation of the culture components is the surest means of reducing contamination by other organisms. Dating allows rapid selection of scale insects of known age and stage of development. In addition, uncontaminated excess material can be readily utilized to increase the size of the mother culture when the reproductive stage is reached. It is always necessary to ensure that the old material is discarded and to infest enough material for regular replenishment of the mother culture. The discarding of older material from the mother culture helps to eliminate both disease and the subsequent deterioration of host plant material; it also reduces the risk of contamination by other pests that may have been initially overlooked or that may invade it. Mite populations, in particular, tend to increase on older host material that has become desiccated and covered with debris. To help ensure that contamination of host plant material and scale insect cultures does not occur, isolated working space with temperature and humidity control is required. A clean, well-ventilated storage area for uninfested host plant material is necessary. Separate space for the mother culture and for the other culture material must be available, and this space must be completely isolated from the clean host plant material and any natural enemy cultures. Field collected material should never be brought into the rooms containing the clean host plant material or laboratory cultures. Following the establishment of a mother culture, a protocol must be devised to ensure self-perpetuation. Given that the selected host plant supports the scale insect, culturing becomes a matter of regular discarding of old, used material and then of reprovisioning with fresh host plants. The reprovisioning with clean uninfested host plant material serves two primary functions: (1) the maintenance and increase of the mother culture, and (2) the supply of scale insect host material for exposure to natural enemies and for other studies. Obviously, the greater the size of the mother culture, the greater the number of scale insects available for other uses such as natural enemy cultures. Procedures for the care and maintenance of scale insect cultures must be stringent. The order of handling the components of the culture is of the utmost importance. Uninfested host plant material is always handled first. Generally, the clean host plant material is examined for the presence of pests, physical damage and decomposition. This can be accomplished when the host plant material is cleansed; in most cases, fruits are washed with water, wiped with a clean cloth and then dried on racks that allow complete air circulation. Fruit rots (i.e. species of the genera Rhizopus, Alternaria, Botrytis, Fusarium, Sclerotinia, etc.) can be a severe problem when cucurbit fruits are used as hosts. This can be minimized by harvesting during dry weather and by handling all fruits carefully to avoid wounds, bruises and other injuries that might serve as points of entry for pathogens. Fruits should be stored in cool, dry conditions and inspected regularly. Any fruits showing signs of infection should be removed from the storage area. As a means of surface disinfection, plant pathologists at Texas A&M recommended dipping cucurbit fruit in a 3 % solution of sodium hypochlorite. The clean, air-dried, uninfested host plant material is then held in well-ventilated, insect tight containers or rooms until infested. Because some kinds of host material may desiccate or develop rots near the stem and blossom ends of the fruit, it may be advisable to seal and protect a portion of some types of host material with paraff'm wax. The waxing of small fruit can also provide a barrier against abrasion and thus can decrease the number of damaged hosts that must be culled. Further, the application of wax limits the surface area that is infested by scale insects and allows for easier handling and collecting of crawlers. Waxing is accomplished by melting white paraffm over a low heat (electric kettle) and briefly immersing the portion of the host to be covered. A natural dye may be added to make the wax more visible.
Laboratory and mass rearing
405
Secondary pests can become major problems in scale insect cultures. For example, the citrus red mite, Panonycus citri (McGregor), the two-spotted spider mite, Metatetranychus urticae (Koch), and a mite in the genus Tyrophagus (Acari: Acaridae) have caused problems in cultures of C. hesperidum at Texas A&M University. The methods used to reduce mite infestations have included discarding older fruit, gentle washing with warm water and a soft camel's hair brush, and the release of such mite predators as Phytoseiulus persimilis Athias-Henriot, P. longipes Evans and Galandromus (=Metaseiulus) occidentalis (Nesbitt). Mealybug species, especially Pseudococcus longispinus (Targioni Tozzetti) and Planococcus citri (Risso) have also been troublesome. Isolation or segregation of infested fruits, along with the release of the encyrtid parasites Anagyrus fusciventris (Girault) for P. longispinus, and Leptomastidea abnormis (Girault) and Leptomastix dacO,lopii Howard for P. citri, have proven to be generally effective against these pests. In Israel, the brown lacewing, Sympherobius sanctus (Tjeder) (Neuroptera; Hemerobiidae), was utilized to control unwanted mealybugs in Saissetia oleae (Olivier) cultures grown on potato sprouts (Argov and R6ssler, 1993). These authors also reported (1993) the control of the potato tuber moth, Phthorimaea operculella (Zeller), a long-time problem when potato tubers are used as hosts, by treatment with 0.3 % Thionex (endosulfan) at the time of sowing potato tubers and then every three to four days thereafter. Honeydew can also be a major problem with such coccids as C. hesperidum, by coating the host plant material, interfering with crawler mobility, collecting airborne debris, promoting the growth of saprophytic molds, causing handling difficulties and, in severe cases, smothering settled scale populations. Excessive honeydew can also trap small parasites and cause larger species to spend an excessive amount of time grooming, thereby interfering with rearing efforts. Gentle washing with warm water prior to crawler production and then as needed thereafter, will help to alleviate these problems. It is important to point out that moderate honeydew production is not harmful and may be beneficial in parasite cultures because honeydew is known to be a highly nutritious food source as it is rich in amino acids and sugars (Ewart and Metcalf, 1956). Vinson et al. (1978) demonstrated that the honeydew of C. hesperidum improved host location and oviposition by the encyrtid Microterys nietneri [ = Microterysflavus], while Heidari and Copland (1993) found that honeydew of Pseudococcus aj~nis (Maskell) [ =Pseudococcus viburni (Signoret)] on the leaves of Bergenia cordifolia (Haw.) Sternb. increased the searching time of Cryptolaemus montrouzieri. The discovery of low-level contamination requires regular diligent searching and therefore daily examination of all material (i.e. the clean host plants, the infested host plants and the mother culture) affords the best assurance that contamination and decomposition will be discovered before major losses occur. Contaminated material should be removed immediately and destroyed, as should plant material that has begun to decompose. The preceding overview of scale insect culture is necessarily general. The selection of laboratory host plant material is dependent on local resources, while the rearing methods must be designed to work in the available facilities. Success in the culture of scale insects in the laboratory will inevitably depend on (i) the selection and continuous availability of suitable host plant material, (ii) the initiation of a pure mother culture, (iii) the isolation of the culture components under adequate environmental conditions and (iv) on regular diligent care. Once a suitable host plant has been found and the culturing facilities established, the success of the culture is in the hands of the researcher. We have selected four species of scale insects to further illustrate the principles of rearing methodology: S. oleae, C. hesperidum, Ceroplastes floridensis Comstock, and Philephedra tuberculosa Nakahara and Gill. The first three species have been reared for
Section
1.4.2 references, p. 416
406
Techniques
various laboratory studies and for the propagation of their natural enemies -- particularly parasitic Hymenoptera -- in several countries and for many years. Whereas these three species appear to be thelytokous, the fourth, P. tuberculosa, is biparental and has recently become a problem in the southern United States.
Saissetia oleae (Olivier) The black scale, S. oleae, has a worldwide distribution (Ben-Dov, 1993; Gill, 1988; Hamon and Williams, 1984) and is believed to be of African origin (Smith, 1921; Gill, 1988). Historically, this uniparental species has been considered a major pest of citrus and olive and is currently of particular concern to growers in central California (Daane and Caltagirone, 1989; M.W. Carpenter and K. Daane, personal communication, 1993). Research on its' biological control brought about the need for continuous laboratory culture of S. oleae for parasite introductions, rearing, colonizations and research. Over time, S. oleae has been considered the most injurious coccid pest in California (Gill, 1988). In 1921, H.S. Smith stated that S. oleae "is given first rank as a pest of citrus fruits in California". In the same paper, Smith (1921) restated the prophetic observation made by C.P. Lounsbury that S. oleae was not a pest in South Africa, except when attended by the Argentine ant, Iridomyrmex humilis (Mayr). Smith (1921) also described the importation of Metaphycus lounsburyi (Howard) into California from Australia in 1918. This was later followed by the importation of Metaphycus helvolus Compere from South Africa in 1937 (Flanders, 1942). Numerous other natural enemies of S. oleae have been imported into California; many of them are important natural enemies of S. oleae elsewhere in the world (Bartlett, 1978). Laboratory cultures of S. oleae have traditionally been reared on either green potato sprouts (Smith, 1921; Blumberg and Swirski, 1977; Viggiani and Mazzone, 1980; Blumberg and DeBach, 1981; Blumberg, 1982, 1988; Argov and Rrssler, 1988, 1993; Blumberg and Goldenberg, 1992) or shoots of Nerium oleander (Finney and Fisher, 1964; Blumberg and Swirski, 1977; Bartlett, 1978) (Table 1.4.2.1). Currently there are projects in California and Israel that require laboratory and mass production of S. oleae. In California, augmentative colonizations of Metaphycus helvolus are required to regulate populations of S. oleae on olive in the central valley and on citrus in the intermediate and interior bioclimatic regions. In both cases, there is a parasite supply problem due to lack of parasite production and high rearing costs (M.W. Carpenter and K. Daane, personal communication, 1993; Daane, et al., 1991). In California, S. oleae is reared on rooted cuttings of N. oleander. This culturing method has not seen substantial change for some 40 years (Firmey and Fisher, 1964) and the methodology described here is currently used by culturists at the Fillmore Citrus Protective District (FCPD) Insectary (M.W. Carpenter, personal communication, 1993). The procedure begins by rooting oleander cuttings, 30 cm long by 1.5-2 cm in diameter, planted about 12-13 cm deep in a soil mix of equal parts loam, sand and peat moss in 4 litre pots. These cuttings are grown out-of-doors (Fig. 1.4.2.4) for about 2 years and, when they reach 1.5-2m in height during the third year of growth, they are used to culture the scale and its parasite, Metaphycus helvolus. Plants that are forced to grow more rapidly are too spindly and weak to survive scale infestation. Some 180 third-year oleander plants are held in each of 19 insectary rooms that measure about 35 m2. The rooms are equipped with sloping floors for drainage and have windows on the east and west sides for light and ventilation. The windows are covered with fine mesh netting. The ceilings are approximately 2.5 m high and are equipped with four 2.5 m fluorescent bulbs simulating natural light. Temperature is maintained between 21-27 ~ The FCPD Insectary generally dedicates at least two rooms to scale insect mother cultures in each parasite rearing rotation, each of which lasts a period of 28 or more days.
Laboratory and mass rearing
407
Fig. 1.4.2.5. Oleander cuttings infested with S. oleae from the mother culture and used to supply crawlers. Photo by M.W. Carpenter.
408
Techniques
Fig. 1.4.2.6. The light attraction device used by the Fillmore Citrus Protective District lnsectary, California, USA, to collect Saissetia oleae crawlers from infested oleander cuttings. Photo by M.W. Carpenter.
The mother culture is also maintained on oleander. Twigs bearing reproductive female scale insects are cut from the mother plants and held in trays with wire mesh bottoms to allow the crawlers to freely disperse (Fig. 1.4.2.5). Crawlers are collected daily in light attraction devices ("shadow boxes") that hold the boxes with twig cuttings (Fig. 1.4.2.6). The clean plants are initially inoculated with crawlers in a unique manner. Five ml lots of crawlers are knocked onto a sheet of paper and then blown by the culturist over the tops of the plants. The room is then made dark for 24 hours. This is repeated over a period of several days in each insectary room. There is no absolute volume of crawlers per room or plant; rather the plants are inspected by the culturists to determine that the crawlers have successfully settled and are evenly distributed on the oleander foliage. Oleander plants in the insectary rooms are generally irrigated once or twice a week and all plants are inspected during each irrigation. About 12 days after the last inoculation with crawlers, the honeydew is washed off by showering plants with water. The need to wash off the honeydew thereafter is determined by the culturist; each washing replaces an irrigation. At 21-25 days after crawler inoculation, the scale insects disperse from the leaves to the stems. At this time, the plants are carefully washed and allowed to dry. Prior to use for parasite production, the top portion of each major stem (above the third and below the second leaf axil) that bears S. oleae is removed and these cut twigs are transferred to inoculate other cohorts of clean plants by placing the cut twigs directly onto oleander plants. These twigs are then removed about 2 weeks later when the scale insects have dispersed. When the remaining scale insects are about 30 days old under FCPD Insectary conditions, the plants with pruned tops are ready for exposure to M. helvolus. The insects are then in their late second and early third instars. Initially, 5,000 parasites are
Laboratory and mass rearing
409
released into each 35 m: room. A second release of 8,000 - 10,000 parasites per room is made five to ten days later. Adult F1 M. helvolus begin to emerge 24-28 days following the initial release and are attracted by light to a screened window, where they are collected into 25 x 200 mm tubes with a vacuum aspirator; 500 parasites per tube (Fig. 1.4.2.7). Each room produces an average of 150,000 adult M. helvolus or about 2.5 million for each parasite rearing rotation. Following each parasite production cycle, the oleander plants are cut back to about 0.75 m tall and recycled through the outdoor nursery. Recycled plants are used once again when two years old and then discarded. The methodology described here has proven satisfactory for the FCPD Insectary because it is a grower cooperative. The parasites are released in the field only where warranted (i.e. not in all groves) but the costs are shared by all cooperative members. However, the cost of such labour intensive methods is currently too high for growers outside a cooperative such as the FCPD. This was borne out in 1992 when many California citrus growers, in areas where S. oleae populations were even or single brooded, wanted to purchase M. helvolus as an alternative to chemical control of S. oleae. Because of the increased demand, the cost of M. helvolus escalated, reaching US$ 70 per 1000 adult parasites. At the recommended rate of 1000 per acre, the costs to growers for parasites greatly exceeded the cost of standard chemical treatment. It is obvious that more cost effective mass rearing methods are needed for S. oleae and M. helvolus.
Laboratory rearing methods utilizing potato sprouts have been developed in Israel where major natural enemy importation, colonization and evaluation programs for S. oleae have been conducted since about 1975 (Blumberg and Swirski, 1977; Argov and R6ssler, 1988), along with numerous biological studies of natural enemy species.
Fig. 1.4.2.7. The collection of adult Metaphycus helvolus with a vacuum aspirator at the Fillmore Citrus Protective District Insectary, California, USA. Photo by M.W. Carpenter.
Section 1.4.2 references, p. 416
410
Techniques Blumberg and Swirski (1977)obtained optimal conditions for rearing S. oleae on green potato sprouts (Table 1.4.2.1) and discuss several key rearing methods. Their general culture methodology includes growing sprouted potato tubers in moist sea sand or on plastic sponges in shallow trays with water rather than in boxes with soil mixes. This method provides completely green sprouts and allows easy detection of rots. Further, the roots are cut off the tubers just before inoculation with scale crawlers from N. oleander grown in soil under greenhouse conditions. Detaching the sprouted potatoes allows for cleaner and easier handling. Blumberg and Swirski (1977) further emphasize several important technical points: i.e. that healthy, medium to large and dormant tubers should be utilized; that twice weekly treatments with endosulfan can prevent infestation with the potato tuber moth, Phthorimaea operculella, which can cause severe damage and rotting to the culture; that Planococcus citri populations can be reduced by the parasites Anagyrus pseudococci (Girault) and Leptomastidea abnormis; that bleached sprouts are unsuitable for S. oleae, and that sanitary conditions are important to all aspects of the culture technique. In a recent review of a major natural enemy importation and rearing program in Israel, Argov and Rrssler (1993) described their rearing methods which were based on those of Blumberg and Swirski (1977), except that all the tubers were sprouted in moist sea sand under greenhouse conditions (Table 1.4.2.1). Argov and Rrssler (1993) cut the tuber roots when the sprouts reached 10 cm in length and held the detached sprouts in a closed cage to retain moisture. The sprouts were inoculated either with eggs or with crawlers that had been collected in a light attraction devise (see Fig. 1.4.2.1). At times, direct transfer was achieved by placing ovipositing female scale insects on clean sprouts. Newly infested sprouts were held in closed plastic cages for development. Mealybug infestations in the rearing containers were controlled by the brown lacewing, Sympherobius sanctus. More than 4.8 million parasites were reared by Argov and Rrssler (1993) using this methodology. There may be potential for the incorporation of this methodology into a mass rearing scheme for M. helvolus in California. According to K. D a a e (personal communication, 1993) the greatest problem encountered with potato tubers for mass rearing in California are rots that cause the sprouts to become unsuitable for S. oleae and thus for M. helvolus. This was also true in the 1930's when the FCPD Insectary tried unsuccessfully to use sprouted potatoes to mass rear S. oleae and M. helvolus (M. W. Carpenter, personal communication, 1993). This may be an area where biological control of plant pathogens could be integrated into an overall rearing program.
Coccus hesperidum L. The cosmopolitan brown soft scale, C. hesperidum, was described by Linnaeus in 1758. Its geographic origins and the details of its dispersal throughout the growing regions of the world have long since been lost. Based on the complexity of the parasite fauna, Annecke (1964) speculated that C. hesperidum might have originated from Africa. In the early days of the California citrus industry, C. hesperidum was considered to be one of the worst scale insect pests, comparable in its destructiveness to the black scale, S. oleae (Timberlake, 1913; Ebeling, 1959). Today, however, C. hesperidum is rarely a problem due to the wide distribution of effective natural enemies. Throughout this century and much of the last, the wide host range of C. hesperidum and its ease of culture have made this scale insect the entomological 'lab rat' of choice for an enormous and diverse number of studies, ranging from the mechanisms of parthenogenesis (Nur, 1971) to the relative importance of intrinsic versus extrinsic competitive superiority of parasites (Bartlett and Ball, 1964). While its primary value has always been as an easily cultured host or alternate host for numerous natural enemies (Avidov, 1970a; Bartlett and Lagace, 1961; Bartlett and Ball, 1964; Reed et al., 1968;
Laboratory and mass rearing
411
Hart, 1972; Ingle et al., 1975; Pappas and Tzoras, 1975; Kfir et al., 1976, 1983; Vinson et al., 1978; Kfir and Rosen, 1980; Blumberg and Swirski, 1988; Muegge and Lambdin, 1989a), C. hesperidum has also been utilized in other investigations. These include pest population dynamics (Hart, 1983), the interactions between insect defense systems and parasites (Bartlett and Ball, 1966) and the effect of environment on insect defense mechanisms (Blumberg, 1976, 1977, 1982; Blumberg and DeBach, 1981). Coccus hesperidum has also been a target for the remote detection of pest populations by the analysis of the reflectance characteristics of infested versus uninfested leaves (Gausman and Hart, 1974a,b) and in tests of the efficacy of strains of entomophagous fungi (Samsinakova and Kalalova, 1975). In addition, studies of C. hesperidum have helped to show the unexpected and sometimes counterintuitive effects of pesticides on some pest species (Elmer et al., 1951; Bartlett and Ewart, 1951; Annecke, 1959; Hart and Ingle, 1971; Hart, 1983). Other investigators have used C. hesperidum to study: the effect of ants on scale insect populations (Annecke, 1959; Avidov, 1970b); the sugars and amino acids in insect honeydew (Ewart and Metcalf, 1956), and the role of honeydew in stimulating parasite searching behavior and in parasite retention (Vinson et al., 1978) . Among the characteristics of C. hesperidum that contribute to its usefulness in such a wide variety of studies are the following. It is polyphagous. At one time or another C. hesperidum has been found on nearly all types of plants except grasses (Gill, 1988), although it prefers evergreen, tropical and semitropical species (Gill, 1988). It is multivoltine, with from three to five generations per year outdoors in southern California and up to seven generations per year in greenhouses (Gill, 1988). The generations overlap, so that all stages can be found at the same time. It is also generally parthenogenic; males have never been observed in the U.S., although they have been noted in greenhouses in Russia (Saakyan-Baranova, 1964). And it is ovoviviparous. Some authors report that females will produce an average of 2 to 3 crawlers per day over a 30 to 60 day period (Quayle, 1938), while other investigators have reported numbers as high as 30 to 40 crawlers per day for periods of 60 to 100 days (Hart, 1983). Whatever the reason, the number of crawlers produced in laboratory scale insect cultures has been consistently reported to be three to four times greater than those in the wild (Hart, 1983). Several researchers have developed and ref'med methods for rearing C. hesperidum (Table 1.4.2.1). Bartlett and Lagace (1961) pioneered the use of the citron melon, Citrullus vulgaris Schrad. var. ~citroides'. Reed et al. (1968) adapted the methodology of Bartlett and Lagace to mass rear Microterys nietneri during a period when pesticides were causing upsurges of C. hesperidum in the Rio Grande Valley of Texas. Avidov (1970b) tested various plant species and their parts, such as potato tubers, butternut squash (Cucurbita moschata Duchesne) and citron melon and concluded that only citron melon was a suitable host for brown soft scale in Israel. Pappas and Tzoras (1975) used Citrus medica L. and C. limon (L.) (= C. limonium Risso) to rear brown soft scale as an alternate host for their studies on the parasites of S. oleae. Ingle et al. (1975, 1979) developed equipment and refined procedures for rearing parasites and for making precise measurements of the fecundity of C. hesperidum. At the Biological Control Laboratory, Texas A&M University, we have reared C. hesperidum on four host plants: 1) Ficus benjamina L. rooted cuttings. This was accomplished by placing young Ficus in direct contact with other Ficus trees bearing adult scale insects producing crawlers. Originally expected to be the host plant of choice, this method proved to be more labor intensive, required more space and produced poorer quality scale insects than any of the other plant hosts tested. This may be partly due to our use of F. benjamina rather than the possibly better suited but less available F. nitida.
Section 1.4.2 references, p. 416
Techniques
412
Fig.
1.4.2.8.
Potted
seedling
of Basella alba,
Malabar
spinach,
ready
for
infestation
with
Coccus hesperidum L. crawlers.
2) Basella alba L. (Fig. 1.4.2.8). This rampant, fleshy, tropical vine known as Malabar spinach, was accidentally found to be an excellent host plant for C. hesperidum. In comparison with other methods, B. alba produced the largest and healthiest scale insects. In addition, it proved to be easily grown in the greenhouse, long lasting and to be tolerant of pruning. Infested cuttings placed in a controlled humidity chamber, such as the "Humiditron" (DeBach and Rose, 1985), remained turgid long enough (about 1214 days) to rear one generation of parasites from the scale insects. 3) Citron or 'preserving melon', produces a hard fleshed, watermelon-like fruit that has been used as a C. hesperidum host for many years. We obtained seeds from fruits selected by B. Bartlett in California for rearing C. hesperidum (E. Dietrich, personal communication, 1989). We found, as did Avidov (1970b), that fresh fruits were good hosts but that crawlers did not settle well on older fruits (i.e. after a 3 months shelf life). 4) Park See~ 'All Season' squash (Fig. 1.4.2.9). This hybrid winter squash, probably a cross of Cucurbita moschata and C. maxima varieties, produces small, globular fruits, about 12 centimeters in diameter, on compact vines over a relatively long season. The fruit has good storage qualities and has proved to be an excellent host for C. hesperidum as well as a number of other coccids, pseudococcids and diaspidids reared in Texas. Our experience with these various hosts of C. hesperidum suggests that 'All Season' squash and Basella alba offer several advantages over citron melon, and that relatively more emphasis should be given to the use of these species. In order to achieve this, we have supplied small amounts of the seed of each of these species to various cooperators for evaluation. At Texas A&M University, our C. hesperidum host culture is maintained in a walk-in environmental chamber at a constant 26~ approximately 60% R.H. and constant darkness. Crawlers are collected daily using a small light attraction box (similar to the one shown in Fig. 1.4.2.1, with space for three or four mother squash or citron melons) and then brushed onto the surface of the host plant. Scale insects reach mid-size after
413
Laboratory and mass rearing
a period of approximately 25-30 days, at which point they are removed from the growth chamber and used to maintain the soft scale parasite cultures.
Fig. 1.4.2.9. Squash of the "All Season" variety, suitable for rearing C. hesperidum.
Ceroplastes floridensis Comstock The genus Ceroplastes is a relatively large group and several species are important pests of horticultural plants in many parts of the world (Kawai and Tamaki, 1967; BenDov, 1970; Hamon and Williams, 1984; Argov et al., 1987; Argov and Rrssler, 1988). The thick, waxy cover characteristic of this genus provides protection against insecticides as well as environmental factors (Kawai and Tamaki, 1967). Biological control by natural enemies has been investigated by numerous researchers (Argov et al., 1987). Species of Ceroplastes, particularly C. cirripediformis Comstock and C. floridensis Comstock, are becoming key pests in interior plantscapes in the U.S.A. (see section 3.2.2, this volume). The Florida wax scale, Ceroplastesfloridensis Comstock, has been recognized as the major soft scale pest on citrus in Israel for some twenty-five years (Avidov and Harpaz, 1969). Laboratory rearing methodologies were reported by Ben-Dov (1970) who developed them for biological control studies. Ceroplastes rusci L., the fig wax scale, was also included in these studies (Ben-Dov, 1970). Kawai and Tamaki (1967) used the fruits of the squash, Cucurbita moschata cultivar "Hyuga" to culture C. pseudoceriferus Green (Table 1.4.2.1), while Ben-Dov (1970) utilized two plant hosts for rearing C. floridensis; rooted citrus leaves (Citrus limetta Risso) and "Hyuga" fruits. In the method used by Ben-Dov, the citrus leaves selected for rooting were three to four months old and were removed from the tree with their petiole intact. The entire petiole plus 1 to 2 cm of the leaf-blade were covered with moist sand and held in "humidity saturated containers" at 28-30~ with 12+ hours of light. At 30+ days,
Section 1.4.2 references, p. 416
414
Techniques
about 50 % of the leaves had rooted. When the roots were approximately 5cm long, the leaves were transferred to an aerated aqueous nutrient solution and, when the roots had grown to about 20 cm long, were inoculated with C. floridensis crawlers (see Ben-Dov (1970) for further details). Although Ceroplastes rusci did not develop on rooted citrus leaves, C. floridensis and two other coccids, C. hesperidum and S. oleae, developed and reproduced successfully on this host. Ben-Dov (1970) found that the size of the scale insects reared on rooted citrus leaves was density dependent. When 10 scale insects per leaf were reared at 26 ~ C, they were of "normal" size but when this was increased to 20-30 scales per leaf, their size was only about 50 % of normal. Host size is a primary concern when rearing natural enemy (Clausen, 1940; Argov, et al., 1987; Muegge and Lambdin, 1989b). "Hyuga" squash fruits were considered suitable for inoculation with scale crawlers when they were 10-20cm in diameter and 6-12cm in height. The growing period to produce fruits of a suitable age and size was about three months in Israel and each fruit had a shelf life of some four to five months. Both C. floridensis and C. rusci developed and reproduced on this host. The life cycle for both species was about four months at 20-22~ Ben-Dov (1970) found that a 10 x 6cm fruit could support 80-100 scale insects of near "normal" size, i.e. similar in size to those grown on natural host plants. Furthermore, "Hyuga" was also found to be suitable for rearing Saissetia coffeae (Walker) (Table 1.4.2.1). The Israel Cohen Institute for Biological Control in Rehovot, Israel, has been working on the biological control of C. floridensis since 1980, the major emphasis of their research being the importation, rearing and colonization of parasitic Hymenoptera (Argov and Rrssler, 1988). Realizing the critical importance of vigorous laboratory cultures of host insects for biological control projects, Argov and Rrssler devoted two years to developing rearing methods for C. floridensis (Argov et al., 1987; Argov and Rrssler, 1988). Argov et al. (1987) provided valuable information on the mass rearing of C.floridensis and other coccid species which is generally lacking or difficult to obtain, such as the effects of scale insect density on both rates of survival and size of individuals and the lighting requirements for host plant viability and scale insect production. Argov et al., (1987) tested potato seedlings, squash fruit (Cucurbita moschata) varieties "Hyuga" and butternut, rooted Hedera helix L. and Citrus leaves, and also plants of Laurus nobilis L., Citrus aurantium L., Myoporum laetum G., Raphiolepsis umbellata (Thunb.), Carissa grandiflora (E.H. Mey), Myrtus communis L., H. helix L. and Asplenium nidus L. Of these, M. communis, H. helix and M. laetum plants were selected for further comparative study following preliminary trials. These three plants were compared as hosts for C. floridensis under conditions of 2227~ 80+ 10% RH and 12L: 12D. The light source was a combination of fluorescent and incandescent (10%) lamps suspended 35cm above plant pots (see Fig. 1 in Argov et al, 1987). Plants were inoculated with eggs and crawlers from C. floridensis living on M. communis and H. helix plants. Paper strips were placed in the plant foliage at the time of inoculation to enhance crawler distribution. Argov et al. (1987) found no significant differences in the size of C. floridensis reared on M. communis, H. helix, and M. laetum plants under two light intensities: the photon fluence rates of 200p.mol m2st and 20/zmol m2s~. However, the scale insects were larger and there were also significant differences in rates of development and survivorship between plant species at the higher light intensity. Of the three plant species tested, M. communis provided the fastest developmental time and greatest survivorship by C. floridensis and this host under artificial light at a photon fluence rate of 200~tmol m2s "~ was therefore selected as their best laboratory rearing method (Argov et al., 1987). In a further test comparing scale insect size at photon fluence rates of 200#mol m2s ~ and 50~mol m2s ~, Argov et al. (1987) noted that scale insect size on M. communis was
Laboratory and mass rearing
415
larger at the greater light intensity and that scale insects raised at 50#mol m2s ~ proved to be too small to rear the encyrtids Microterys speciosus Ishii and M. clauseni Compere. The duration of illumination was found to affect both the size of individuals and the sex ratio of C. floridensis populations on M. communis. At eight hours of light, the plant failed, the scale insects were very small and few females were reproducing. At ten hours, the scale insect size and the proportion of reproducing females in the population were still significantly less than at the twelve hours recommended by Argov et al. (1987) for rearing C. floridensis on M. communis (Table 1.4.2.1). Because host size is so important in parasite rearing, Argov et al. (1987) also compared scale insect size at differing densities on both M. communis and H. helix. At relatively low densities (ten per plant) scale insect size was always larger on M. communis than at higher densities. Furthermore, M. communis could support densities up to 500 scale insects per plant that were of suitable size for parasite rearing. Conversely, the size of C. floridensis on H. helix began to decrease when scale insect density reached 200 per plant. Most importantly, the size of scale insects on M. communis at 500 insects per plant was "markedly" larger than those on H. helix at 30 insects per plant. Although M. communb was selected as the optimal host for rearing C. floridensis, Argov et al. (1987) continued to rear the scale insect on H. helix plants. This host plant was certainly less efficient than M. communis but was preferred by some parasite species; that is, certain species of parasites attacked more C. floridensis on H. helix than on M. communis. For example, Argov (unpublished data) has noted that the aphelinid Coccophagus hawaiensis Timberlake showed a distinct preference for hosts on H. helix over those on M. communis under laboratory conditions.
Philephedra tuberculosa Nakahara and Gill Philephedra tuberculosa is a member of a New World genus that ranges from Colombia to the southern border of the United States (Nakahara and Gill, 1985). During the past decade, it has been recorded from some fifty different host plants, including several agriculturally important species and numerous ornamentals. Its short life cycle, high fecundity and the relative paucity of known natural enemies (Pefia et al., 1987) have all contributed to its status as a potentially serious pest. During their investigation of its life history, Pefia et al. (1987) developed a method for rearing this biparental scale insect using one of its preferred hosts, the green fruit and/or plant of papaya, Carica papaya L. Their rearing method (Pefia et al., 1987) was based on those developed by Tashiro (1966) for rearing AonidieUa aurantii Maskell on lemons. This method includes the use of water reservoirs under green papaya fruits. Both the fruits and plants of papaya were inoculated by manually transferring the fully formed ovisacs of P. tuberculosa to either the apical buds or to the upper surface of fruits. Ovisacs were removed when crawlers had eclosed. The mother culture was maintained on entire plants. The first- and second-stage nymphs of this scale insect often dispersed over the same host plant. Second-stage females frequently dispersed to "more succulent tissues" (Pefia et al., 1987), thus providing a method for infesting additional host plant material. Second-stage males dispersed to the foliage to form the male test and to pupate; male production on the fruits only of green papaya was insufficient to maintain a vigorous culture (J.E. Pefia, personal communication, 1993). The winged adult males became fully developed in about 24 days at 27 + 2~ and 75 + 3 % RH, whereas females required about 59 days to reach reproductive age (Pefia
Section 1.4.2 references, p. 416
Techniques
416
et al., 1987). The males lived for only 10 to 22 hours and were able to copulate with females of the same cohort upon emergence. The males were very phototropic, resulting in low rates of mating if they were attracted to light sources for long periods. This problem was corrected by changing the diurnal pattern to 10 hours of light and 14 hours of darkness, which provided adequate mating for maintaining the culture (J.E. Pefia, personal communication, 1993).
SUMMARY Despite the work of such pioneers as H.S. Smith and the more recent efforts of Bartlett, Avidov, Ben-Dov, Blumberg, Argov, Rrssler and others, the rearing of soft scale insects remains at a relatively early stage of development. Most research has concentrated on a handful of common pest species and little is known about the culturing requirements of the majority of soft scale species. The work of Argov et al. (1987) on C. floridensis provides an excellent example of the care and energy that should be devoted to developing rearing methods for coccids and laboratory cultures in general. Research in biological control is, in many cases, absolutely dependent upon laboratory cultures of host species for rearing imported natural enemies. Furthermore, should effective natural enemies be identified, their rapid introduction and full utilization is, to a large degree, governed by the development of efficient and cost-effective methods of mass rearing. The current situation in California with regard to the mass rearing of M. helvolus for augmentative colonizations against S. oleae on citrus is a case in point. Exceptions to the general principles set forth in this chapter will be easy to f'md. Success in rearing, dependent as it is on living plants or plant parts is likely to remain largely a function of the skills and experience of the culturist. These skills and experience are invaluable and need to be passed along to more workers. It is our hope that the information provided here is a step in that direction.
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Bartlett, B.R. and Ball, J.C., 1966. The evolution of host suitability in a polyphagous parasite with special reference to the role of parasite egg encapsulation. Annals of the Entomological Society of America, 59(1): 2-45. Bartlett, B.R. and Ewart, W.H., 1951. Effect of parathion on parasites of Coccus hesperidum. Journal of Economic Entomology, 44(3): 344-347. Bartlett, B.R. and Lagace, C.F., 1961. A new biological race of Microterysflavus introduced into California for the control of lecaniine coccids, with an analysis of its behavior in host selection. Annals of the Entomological Society of America, 54: 222-227. Ben-Dov, Y., 1970. Laboratory rearing of wax scales. Journal of Economic Entomology, 63(6): 1998-1999. Ben-Dov, Y., 1972. Life history of Tetrastichus ceroplastae (Girault) (Hymenoptera: Eulophidae), a parasite of the Florida wax scale, Ceroplastes floridensis Comstock (Homoptera: Coccidae), in Israel. Journal of the Entomological Society of Southern Africa, 35(1): 17-34. Ben-Dov, Y., 1978. Taxonomy of the nigra scale Parasaissetia nigra (Nietner) (Homoptera: Coccoidea: Coccidae), with observations on mass rearing and parasites of an Israeli strain. Phytoparasitica, 6(3): 115-127. Ben-Dov, Y., 1993. A Systematic Catalogue of the SoR Scale Insects of the World (Homoptera: Coccoidea: Coccidae) with data on geographical distribution, host plants, biology and economic importance. Flora and Fauna Handbook, Sandhill Crane Press, Inc. Gainesville, Florida, 536 pp. Bess, H.A., 1958. The green scale, Coccus viridis (Green) (Homoptera: Coccidae), and ants. Proceedings of the Hawaiian Entomological Society, 16(3): 349-355. Blumberg, D., 1976. Extreme temperatures reduce encapsulation of insect parasitoids in their insect hosts. Experientia, 32(11): 1396-1397. Blumberg, D., 1977. Encapsulation of parasitoid eggs in sott scales (Homoptera: Coccidae). Ecological Entomology, 20): 185-192. Blumberg, D., 1982. 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Encapsulation of eggs of two species of Encyrtus (Hymenoptera: Encyrtidae) by sott scales (Homoptera: Coccidae) in six parasitoid-host interactions. Israel Journal of Entomology (1991), 25-26: 57-65. Blumberg, D. and Swirski, E., 1977. Mass breeding of two species of Saissetia (Hom.: Coccidae) for propagation of their parasites. Entomophaga, 22(2): 147-150. Blumberg, D. and Swirski, E., 1988. Colonization ofMetaphycus spp. (Hymenoptera: Encyrtidae) for control of the Mediterranean black scale, Saissetia oleae (Oliver) (Homoptera: Coccidae), in Israel. In: Goern, R. and Mendel, K. (Editors), Proceedings of Sixth International Citrus Congress, Tel Aviv, Israel, March 6-11, 1988. Baraban, Rehovot, Israel & Margrof, Weikersheim, Germany, pp. 1209-1213. Blumberg, D., Wysoki, M. and Hadar, D., 1993. Further studies of the encapsulation of eggs of Metaphycus spp. (Hym: Encyrtidae) by the pyriform scale, Protopulvinaria pyriformis (Hom: Coccidae). Entomophaga, 38(1): 7-13. Clausen, C.P., 1940. Entomophagous Insects. McGraw-Hill Book Co. New York, 688 pp. Daane, K.M., Barzman, M.S. and Caltagirone, L.E., 1991. Augmentative releases of Metaphycus helvolus for control of black scale, Saissetia oleae, in olives. Plant Protection Quarterly, 2: 6-8. Daane, K.M. and Caltagirone, L.E., 1989. Biological control of black scale in olives. California Agriculture, 43(1): 9-11. DeBach, P., 1964. Biological Control of Insect Pests and Weeds. Halsted Press, New York, 844 pp. DeBach, P. and Rose, M., 1985. Humidity control during shipment and rearing of parasitic hymenoptera. Chalcid Forum, 4:11-13. DeBach, P. and White, E.B., 1960. Commercial Mass Culture of the California Red Scale Parasite Aphytis lingnanensis: California Agricultural Experiment Station, Riverside, California, 58 pp. Ebeling, W., 1959. Subtropical Fruit Pests. University of California, Division of Agricultural Sciences, Los Angeles, 436 pp. Eisa, A.A., EI-Fatah, M.A., EI-Nabawi, A. and El-Dash, A.A., 1991. Inhibitory effects of some insect growth regulators on developmental stages, fecundity and fertility of the Florida wax scale, Ceroplastes floridensis. Phytoparasitica, 19(1): 49-55. Elmer, H.S., Ewart, W.H. and Carman, G.E., 1951. Abnormal increase of Coccus hesperidum in citrus groves treated with parathion. Journal of Economic Entomology, 44(4): 593-597. 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. Finney, G.L. and Fisher, T.W., 1964. Culture of entomophagous insects and their hosts. In: DeBach, P. (Editor), Biological Control of Insect Pests and Weeds. Halsted Press, New York, pp. 328-355.
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Techniques Flanders, S. E., 1942. Metaphycus helvolus, an encyrtid parasite of the black scale. Journal of Economic Entomology, 35(5): 690-698. Gausman, H.W. and Hart, W.G., 1974a. Reflectance of four levels of sooty-mold deposits produced from the honeydew of three insect species. Journal of the Rio Grande Valley Horticultural Society, 28:131-136. Gausman, H.W. and Hart, W.G., 1974b. Reflectance of sooty mold fungus on citrus leaves over the 2.5 to 40-micrometer wavelength interval. Journal of Economic Entomology, 67(4): 479-480. Gill, R.J., 1988. The Scale Insects of California. Part 1. The Soft Scales (Homoptera: Coccoidea: Coccidae). Technical Services in Agricultural Biosystematics and Plant Pathology, California Department of Food and Agriculture, Sacramento, California, 132 pp. Hamon, A.B. and Williams, M.L., 1984. The Sot~ Scale of Florida (Homoptera: Coccoidea: Coccidae). Arthropods of Florida and Neighboring Land Areas. Vol. 11. Florida Department of Agriculture and Consumer Services, Gainesville, Florida, 194 pp. Hart, W.G., 1972. Compensatory releases of Microterys flavus as a biological control agent against brown sot~ scale. Environmental Entomology, 1(4): 414-419. Hart, W.G., 1983. Factors Influencing the Population Dynamics of Brown Soft Scale, Coccus hesperidum L. in South Texas [Ph.D. Dissertation]. Texas A&M University, 125 pp. Hart, W.G. and Ingle, S., 1971. Increases in fecundity of brown soft scale exposed to methyl parathion. Journal of Economic Entomology, 64(1): 204-208. Heidari, M. and Copland, M.J.W., 1993. Honeydew: a food resource or arrestant for the mealybug predator Cryptolaemus montrouzieri? Entomophaga, 38(1): 63-68. Ibrahim, A.G. and Copland, M.J.W., 1987. Effects of temperature on the reproduction of Saissetia coffeae and its parasitoids. Insect Science and its Application, 8(3): 351-353. Ingle, S.J., Hart, W.G. and Garza, M.G., 1979. An apparatus to facilitate measurement of fecundity of brown sof~ scales. Southwestern Entomologist, 4(4): 353-356. Ingle, S.J., Hart, W.G. Garza, M.G. and Lara, P., 1975. A modified cage and procedure for rearing parasites of brown soft scale. Journal of Economic Entomology, 68(3): 355-357. Jarraya, A., 1975. Contribution h l'rtude des interactions h6te-parasite chez Coccus hesperidum L. (Hom. Coccidae) et son parasite Coccophagus scutellaris Dalman (Hym. Aphelinidae). I. I~tude exprrimentale du comportement de ponte du parasite. Archives de l'Institut Pasteur de Tunis, 52(4): 415-456. Kawai, S. and Tamaki, H., 1967. Morphology of Ceroplastespseudoceriferus Green with special reference to the wax secretion. Applied Entomology and Zoology, 20): 133-146. Kfir, R., Podoler, H. and Rosen, D., 1975. Presence of males increases the area of discovery of a gregarious parasitoid. Annals of the Entomological Society of America, 68(4)" 707-709. Kfir, R., Podoler, H. and Rosen, D., 1976. The area of discovery and searching strategy of a primary parasite and two hyperparasites. Ecological Entomology, 1(4): 287-295. Kfir, R. and Rosen, D., 1980. Biological studies of Microterysflavus (Howard) (Hymenoptera: Encyrtidae), a primary parasite of soft scales. Journal of the Entomological Society of Southern Africa, 43(2): 223-237. Kfir, R., Rosen, D. and Podoler, H., 1983. Laboratory studies of competition among three species of hymenopterous hyperparasites. Entomologia Experimentalis et Applicata, 33(3): 320-328. Mani, M. and Krishnamoorthy, A., 1990. Evaluation of the exotic predator, Cryptolaemusmontrouzieri Muls. (Coccinellidae, Coleoptera), in the suppression of green shield scale, Chloropulvinaria psidii 0Vlaskell) (Coccidae, Hemiptera) on guava. Entomon, 15(1): 45-48. Muegge, M.A. and Lambdin, P.L., 1989a. Longevity and fecundity of Coccophagus lycimnia (Walker) (Hymenoptera: Aphelinidae), a primary parasitoid of Coccus hesperidum (Homoptera: Coccidae). Journal of Agricultural Entomology, 6(3): 169-174. Muegge, M.A. and Lambdin, P.L., 1989b. Optimal length of Coccus hesperidum L. (Homoptera: Coccidae) for parasitism by Coccophagus lycimnia (Walker) (Hymenoptera: Aphelinidae). Journal of Entomological Science, 24(1)" 96-100. Muzaffar, N. and Ahmad, R., 1977. A note on Saissetia privigna (Hem.: Coccidae) in Pakistan and the breeding of its natural enemies. Entomophaga, 22(1): 45-46. Nakahara, S. and Gill, R.J., 1985. Revision of Philephedra, including a review of Lichtensia in North America and description of a new genus, Metapulvinaria. Entomography, 3" 1-42. Nohara, K. and lwata, M., 1988. Biological study of Cybocephalus gibbulus (Erichson), (Coleoptera, Cyboeephalidae), a predator of the scale insects in the citrus orchards. Proceedings of Faculty of Agriculture, Kyushu Tokai University, 7: 25-31. Nur, U., 1971. Parthenogenesis in Coccids (Homoptera). American Zoologist, 11: 301-308. Pappas, S. and Tzoras, A., 1975. l~levagede parasites de Saissetia oleae Bern. sur un h6te de remplacement Coccus hesperidum L. maintenu sur feuilles enracin~es d'Aurantiacres. Fruits, 30(4): 247-249. Pefia, J.E., Baranowski, R.M. and Litz, R.E., 1987. Life history, behavior and natural enemies of Philephedera tuberculosa (Homoptera: Coccidae). Florida Entomologist, 70(4): 423-427. Quayle, H.J., 1938. Soft brown scale, Coccus hesperidum L. In: Insects of Citrus and Other Subtropical Fruits. Comstock Publishing Co. Inc. Ithaca, N.Y. pp. 96-101. Reed, D.K., Hart, W.G. and Ingle, S.J., 1968. Laboratory rearing of brown soft scale and its hymenopterous parasites. Annals of the Entomological Society of America, 61(6): 1443-1446. Saakyan-Baranova, A.A., 1964. On the biology of the sot~ scale Coccus hesperidum L. (Homoptera, Coccoidea). Entomological Review, 43: 135-147. Samsinakova, A. and Kalalova, S., 1975. Artificial infection of scale-insect with entomophagous fungi Verticillium lecanii and Aspergillus candidus. Entomophaga, 20(4): 361-364.
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Schaffer, B. and Mason, L.I., 1990. Effects of scale insect herbivory and shading on net gas exchange and growth of a subtropical tree species (Guaiacum sanctum L.). Oecologia, 84: 468-473. Smith, H.S., 1921. Biological control of the black scale in California. Monthly Bulletin of the Department of Agriculture, State of California, 10(4): 127-137. Speight, M.R., 1991. The impact of leaf-feeding by nymphs of the horse chestnut scale Pulvinaria regalis Canard (Hem. Coccidae) on young host trees. Journal of Applied Entomology, 112: 389-399. Su, T.-H. and Lin, F.-C., 1986. Biological studies on the symbiosis between the green scale insect and a field ant. Chinese Journal of Entomology, 6(1): 57-68. Tashiro, H., 1966. Improved laboratory techniques for rearing California red scale on lemons. Journal of Economic Entomology, 59(3): 604-608. Timberlake, P.H., 1913. Preliminary report on the parasites of Coccus hesperidum in California. Journal of Economic Entomology, 6(3): 293-303. Viggiani, G. and Mazzone, P., 1980. Metaphycus bartleni Annecke et Mynhardt (1972) (Hym. Encyrtidae), nuovo parassita introdotto in Italiaper la Iotta biologica alia Saissetia oleae (Oliv.). Bollettinodel Laboratorio di Entomologia Agraria 'FilippoSilvestri',Portici,37: 171-176. Vinson, S.B., Harlan, D.P. and Hart, W.G., 1978. Response of the parasitoidMicroterysflavus to the brown soll scale and itshoneydew. Environmental Entomology, 7(6): 874-878. Visser, M.E. and van Alphen, J.J.M., 1987. Metaphycus helvolus (Hymenoptera: Encyrtidae), a biological control agent of Coccus hesperidum (Homoptera: Coccidae)? Mededelingen van de Faculteit Landbouwwetenschappen, RijksuniversiteitGent, 52(2a): 319-328. Walter, G.H., 1988. Activitypatternsand egg production in Coccophagus bartletti,an aphelinid parasitoid of scale insects. Ecological Entomology, 13(I): 95-105. Wilk, B.M. and Kitayama, C.Y., 1981. Host stage preference for depositionof male eggs by Coccophagus cowperi (Hym.: Aphelinidae). Entomophaga, 26(3): 313-318.
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General Index Note 1. Further information can be found in the following indexes: Index to Coccoidea Taxa, Index to Names of Parasitoids, Predators and Pathogens, and Index to Plant Names. Note 2. Numbers in italics refer to pages with figures. The terms 'male ~ and 'female ~ refer to the adult stages. l st-instar nymph xi, 338, 344, 369 appearance 32 - behaviour 34 - characters 32, 143-156 - character states 152-155 - classification 151-155 -collection of 402, 402, 403, 408, 412 Coccoidea: 158, 165, 168, 170, 173, 176, 181, 183 lecanoid Coccoidea: character states: 161 settling 404 2nd-instar male: puparium 337 2nd-insizr nymphs: coccid 344-347 appearance 36 characters 37 colonisation sites 415 male wax test ix, xi, 113 3rd-insizr nymph: coccid: characters 39 8-shaped pores: see eight-shaped pores
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alar lobe 26, 27, 28 alar setae 29, 142, 247 Aldabra Atoll 339 Aleurocanthus husaini 284 Aleurocanthus woglumi 281,282 Aleurocybotus indicus 282, 284 Aleurocybotus sp. 282 Aleyrodidae/-icolae 274, 281,282, 284 alkaloids 364 Alps 292 Alternaria limicola 285 Alternaria sp. 404 alternation of generations 207 amnion 257, 258, 259 amniotic cavity 258,259 amniotic membrane 259 anal apparatus 87, 88 anal cleft: female 6, 114, 116, 122, 158, 159, 168, 178, 185,246, 271,272, 338 50, 51 - nymphs 36, 37, 40, 158, 168, 246 anal lobes: female 167, 168, 170, 175, 178, 187, 246 -nymph 146, 158, 161, 165, 167, 168, 170, 173, 176, 181, 183,239,246 anal lobe seize: female 126,246 - nymph 246 anal opening: prepupa/pupa 42 anal opercula: see anal plates anal plates: female: structure I1, 12, 15, 16, 17, 88, 89, 116, 122, 124, 158, 159, 168, 175, 178, 181, 185, 186, 187, 190, 196, 246, 271,272, 273,337 - function 124 - evolution 124 male test ix, xi, 50, 51 - nymphs 32, 33, 36, 39, 40, 161, 165, 168, 169, 170, 176, 181,246 anal plate seize: female 15, 16, 122, 124, 272 - nymphs 32-34, 39, 40, 42, 145, 146, 151, 152-155 anal process: see caudal process anal ring: female 15, 16, 122, 125, 158, 159, 168, 170, 175, 176, 178, 181, 183, 185, 271, 273, 273, 274 - function 15, 125 - nymphs 32, 35, 36, 39, 40, 89, 88, 146, 146, 161, 165, 170, 176, 183 anal ring seize 88, 89, 273, 273, 274 anal ring wax glands 88, 89, 104 wax production 104 -structure 104 - pores 273 anal sclerotisation: female 115, 116, 124 -
abdominal seize 162 abdominal seize: male: see dorsal or ventral seize abdominal pleural seize 247 abdominal pleurites 163,247 abdominal sclerites: male 139 abdominal sternites 26, 27, 28, 163, 176 abdominal tergites 26, 27, 28, 141, 163,247 abdominal ventral seize: male 247 Acarina 404, 405 accessory glands 85, 85 Achaetobotrys 276 Aclerda berlesii: honeydew source 294 host plants 294 Aclerdidae: female characters 158, 159, 160, 164 male characters 162, 163, 165, 165 no. genera 158 no. species 158 nymphal characters 158, 161,164, 165 -phylogenetic relationships 165, 231, 233-25, 240, 241 Acrogenotheca elegans 279 Actinocymbe 277 acuminate scale: see Kilifia acuminata additional sclerite 26, 27, 28 aedeagus 26, 27, 28, 142, 163,247 - structure 87 Africa 190, 193,291,338-340, 410 Afro-tropical region 365 agricultural practices 343 Agrogenotheca elegans 279 Aithaloderma 276 Aithaloderma clavatisporum 279 -
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422 anal tube: female 15, 88, 158, 160, 168, 181, 185, 186, 196, 270, 271,273,273 anal tubercle: female 183 anatrepsis 258, 259 Anderson's scale: see Cribrolecanium andersoni ano-genital fold: female 271,272 - nymph 39, 145 associated structures 116, 122, 125 Anonychomyrma sp.: myrmecophyte associations 365 Anopeltis 276 Anoplolepis custodiens: amount of honeydew collected 364 association with pest outbreaks 361 coccid protection 361 coccid transport 355 effects of ant exclusion 358 geographic distribution 358 Anoplolepis longipes: association with pest outbreaks 361,362 effects of ant exclusion 357 geographic distribution 357 - transport of fungal spores 356 Anopulvinaria cephalocarinata: dorsal tubercle -
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98 ant activity: indication of presence of coccids 389 ant-coccid interactions 87, 89, 354, 351-370 facultative 352 obligate 352 ant plants: see myrmecophytes ante-anal setae 26, 27, 29, 247 antemetaspiracular setae 26, 27, 29, 141,247 antennae: female 10, 17, 116, 133, 135, 160, 167, 168, 170, 175, 178, 181, 185, 186, 190, 196, 246, 338 male 23, 26, 27, 139, 162, 178, 247 - nymphs 32, 36, 37, 39-41, 43, 149, 150, 151-156, 161, 170, 173, 176, 183,246 antennal bristles 26, 27 antennal setae: nymphs 32, 37 antennal tubercles: female 13 Antennatula pinophila 279 AntennularieUa 276 Antennulariella fuliginosa 276 Antennularielliaceae 275,276 anteprosternal setae 26, 27, 29 anterior margin setae: female 145, 271, 272 - nymphs 39, 40 anterior metasternal setae 26, 27, 29, 142 anterior postalare ridge 25, 26, 27 anterior notal wing process 25, 26, 27 anterior tentorial pit 26, 27 antibiotic effects: ants 356 ants 351-370, 411 aggression and coccid protection 361,362 antibiotic secretions from metapleural glands 356 as scavengers 352 - benefits of coccids to 363-364 - benefits to coccids vii, 270, 352-356 - coccid transport 354, 355,369, 370 disturbance of predators/parasites vii, ix, 356-361 dominance and co-dominance 363 - effects of attendance on plant growth 333 - effects on coccid development rate 357 - effects on coccid excretion 357 - effects on coccid survival 358, 359 -
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- effects on honeydew elimination 15 effects on parasitism 362 effects on pest status 352 - exclusion studies 356-361,360, 363 - formation of protective covers ix, 355 - honeydew 352 insect groups attended 352 obligate coccid associations 196,352, 368 - predation of coccids 252, 363,369 - sanitary benefits to coccids 353 secondary effects of ant activity 352 - solicitation of honeydew 353 - specificity of coccid sp. attended 353, 368, 369 transport of fungal spores 356 anus: female 170, 270, 274 male 26, 27, 28, 163 - nymph 173 appearance: female 5-20, 111-136 - colour: intraspecific variation 203,207, 208 -derm: female 6, 15, 115, 128, 158, 159, 176, 185, 186, 190, 193, 196, 338 - derm: nymphs 32, 37, 143, 152-156 female 158, 168, 170, 196, 254 male: 162 - shape: intraspecific variation 203,207, 208 female 254 - size: intraspecific variation 203,207, 208 - volume: female 254 Aphididae/-inae/-oidea 270, 282, 283,292, 294, 296,298, 309,324, 3 2 5 , 3 5 1 , 3 5 2 , 381 aphids: see Aphididae Aphis gossypii 283 Aphis spiraecola 283,284 apical seta 26, 27, 29, 271 apical (capitate) setae 141 apodemes 23 apterous male 183 Argentine ant: see Linepithema humile Arie 285 Armenia 206 arrhenotokous races 264, 265 arrhenotokous reproduction 204, 207 articulatory sclerotisation: see tibio-tarsai articulation ascomycetes 275 Asia 190, 291 Asterinaceae 275 Asterolecaniidae: female characters 159, 160, 166, 167 male characters 162, 163,167, 168 - nymphal characters 161,166, 168 -phylogenetic relations 167, 231, 235 Auchenorrhyncha 79 Aureobasidium pullulans 263,264 Aureobasidium sp. 275 Australian region 215, 216, 217, 222-224, 226, 365 - coccid species richness 222 - monotypic coccid genera 222 - no. coccid genera 222 - no. coccid species 222 Australia 190, 2 8 1 , 3 4 3 , 3 5 1 , 3 5 8 , 365,376 Austria 292 Austro-Oriental region 223,224, 226,227 - monotypic coccid genera 223 - species richness 223 Austrolichtensia hakearum: with ants 351 auxiliary sclerites 28
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axillary wing sclerites 26, 27
Azadirachta indica: see neem Azerbaidjan 280 Azores 279 Azteca alfari group: myrmecophyte associations 366 Azteca longiceps 365,366 Azteca pittieri complex: myrmecophyte associations 365,366 Azteca sp.: effects of ant exclusion 357, 359,
360 - general 357, 360, 363,368 geographic distribution 357 harvesting of coccids 363 myrmecophyte associations 366 possible use as a biocontrol agent 370 -
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bacteria: encapsulation 375 bacteria-like micro-organisms 264-266 basal membraneous area 26, 27, 28 basal rod 26, 27, 141 basal sockets, setae: female 117, 127 basalare 25, 26, 27, 140, 239, 247 Basella alba vine: for culturing 412 basiconic sensilla: female 10, 133, 135 basisternal setae 26, 27, 29, 142 basisternum 25, 140, 162, 247 beech bark disease 326 Bemisia argentifolia 282 Bemisia tabaci 282, 284 Benin 281 Benlate 285 benomyl 285 bilocular pores: female 19 - nymph 144, 145, 156 - structure 119, 121 - see also dorsal microductules binapacryl 285 biocontrol 347 biocontrol agents: ants 370 biological strains: effects on encapsulation: 379, 381 birds 2 9 1 , 2 9 5 , 2 9 7 , 307, 309 black mildews 275 blastoderm 257, 258, 259 body shape: female 158, 168, 170, 196 -male 162 body size: male 246 Bordeaux mixture 285 Botrytus 404 brachial plate: female 159, 183 Brachymyrmex heeri: coccid transport 355 Brazil 295,297 breadfruit: see A rtocarpus altilis brown apricot scale: see Parthenolecanium corni brown scale: see Parthenolecanium corni brown soft scale: see Coccus hesperidum Bulgaria 294 Burkino Faso 282, 284
myrmecophyte associations 366 Canada 282, 359 capitate setae 141 Capnobotrys 278 Capnobotrys dingleyae 279 Capnobotrys neesii 279 Capnocifferia 276 Capnocrinum 276 Capnocybe 278 Capnodaria 276 Capnodiaceae 275, 276 Capnodium 276,282, 284 Capnodium citri 280, 281,284, 285 Capnodium citricola 279 Capnodium juniperi 278 Capnodium ramnosum 284 Capnodium salicinum 276 Capnodium walteri 277, 282 Capnophaeum 276 Capnophialophora 278 Capnosporium 278 Cardiococcinae: female characters ix-xi, 186, 187, 188 geographic distribution 187 no. species 187 no. genera 187 -phylogenetic relationships 231, 233-235, 240, -
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241 carmine dye 62 caterpillars 381 Caucasus 205 caudal process: female 15, 114, 115, 187, 272 function 114 caudal extensions 26, 27, 28, 141,239, 247 caudal lobes: prepupa/pupa 42 Central America 193, 318 Central Asia 2 0 5 , 2 0 6 , 2 2 5 Central Europe 215 Ceramoclasteropsis 276 Ceramothyrium 277 cerarii 175 ceriferous wax scale: see Ceroplastes pseudoceri-
f erus Cerococcidae: female characters 159, 160, 168,
169 no. genera 168 no. species 168 nymphal characters 161, 169, 170 -phylogenetic relations 168, 235 Ceronema africana: general appearance 7 Ceroplastes: geographic distribution 224 Ceroplastes brevicazMa: anal area 16 Ceroplastes ceriferus: field characters viii nymphal characters 153 Ceroplastes destructor: aqueous material in test 55 -"honeydews" 64 hydrocarbons in test 58 lipids in test 64 secretion of "honeydews" 68 terpenoids in test 59 waxes in test 56 Ceroplastes floridensis: culturing conditions 399 encapsulation 378 geographic distribution 280 host/parasitoid interactions 384 host plants for cultures 399 mass rearing 413-415 - nymphal dispersal 341 -
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calico scale: see Eulecanium cerasorum California 215, 282, 294, 297, 339, 343-347, 358, 359, 379, 3 8 1 , 3 8 3 , 3 9 8 , 4 0 6 , 4 0 9 , 410 Callebaea 276 cambium 324, 326 campaniform pore/sensilla: female 10, 32, 37, 133, 134, 135 - nymph 32, 37, 149, 246 Camponotus sp. vii, 357
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Ceroplastes japonicus: aqueous material in test 55 hydrocarbons in test 58 - life cycle 253 lipids in test 64 secretion of test 68 terpenoids in test 58, 60 - types of honeydews 66 waxes in test 56 -
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Ceroplastes pseudoceriferus: aqueous material in test 55 - culturing conditions 399 filamentous ductules 96 - "honeydews" 66, 67 - host plants for cultures 399 hydrocarbons in test 58 lipids in test 64 - secretion of "honeydews" 67, 68 secretion of test 67, 68 terpenoids in test 58-60 - types of "honeydews" 66, 67 waxes in test 56 Ceroplastes rubens: aqueous material in test 55 - culturing conditions 399 -"honeydews" 66 - host plants for cultures 399 hydrocarbons in test 58 lipids in test 64 terpenoids in test 58-60 - types of honeydews 66 waxes in test 56 Ceroplastes rusci: culturing conditions 399 geographic distribution 358 Ceroplastes sinensis: Ceroplastes-type pores 106 - entomophagous fungi 335 filamentous ductules 108 geographic distribution 335 host plants 335 - preopercular pores 98 spiracular disc-pores 95 test 7 Ceroplastes sp.: female 92 appearance 92 Ceroplastes-type glands 97 -cytology 107 gland systems 107 structure 106 Ceroplastes-type pores 68 - distribution 120 18, 187 - function 68, 120 - structure 119, 120 Ceroplastinae: female characters 186, 187, 189 - geographic distribution 188, 225 no. genera 187 - no. species 187, 225 -phylogenetic relationships 231, 233-235, 240, -
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Chatham Is. 295 China 196, 204, 2 1 5 , 2 8 3 , 3 0 3 - 3 1 9 China wax: see pela wax Chinese wax scale: see Ceroplastes sinensis Chloropulvinaria floccifera: anal apparatus 88 - ejection of honeydew 88 female reproductive system 84, 85 - multilocular disc-pores 95 - ovarioles 85 - salivary pump 74 tubular duct 96 Chloropulvinaria psidii: tubular duct 96 chlorosis 327 chorion 259 Cicadellidae 282, 351 cicatrix 26, 27, 28, 141,247 Cinara cupressi 293 Cinara pectinatae 299 Cinara sp. 292 circuli 175 Cissococcinae: female characters 186, 189, 190 geographic distribution 190 -phylogenetic relationships 231, 233-235, 240, -
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241 Ossococcus 337, 338 Cissococcus j~dleri: female characters 338
chaetotaxy 29 Chaetothyriaceae 2 7 5 , 2 7 7 Chaetothyrium 277 Chaetothyrium cirri 284, 285
galls 337 - geographic distribution 337, 338 citricola scale: see Coccus pseudomagnoliarum cladistic analysis: lecanoid Coccoidea 229 Cladomyrma sp.: cultivation of coccids 369 - myrmecophyte associations 366 Cladosporium 275 classification: history: Coccidae 185 - Coccoidea 157 claw denticle: female 10, 134 male 247 -nymphs 32, 38, 161, 170,246 claw digitules: female 10, 26, 27, 29, 133, 134, 186, 193,246 -nymphs 32, 38, 4 0 , 4 1 , 151, 161,246 claw: female 10, 133, 134 male 26, 27, 28 - nymphs 32, 38, 40, 4 1 , 1 5 0 clistostomatic glands 97 closed pores: female 118, 119 definition 93, 97 structure 93 cluster pore plates: female 159, 170 clypeolabral shield: female 10, 116, 133, 136, 338 coccid: as trophobionts ix, 369 damage 352 development rate: effects of ants 357 - effects on encapsulation 377-379, 3 8 3 , 3 8 4 effects on host plant 323-334 excretion: effects of ants 357 host plant: effects on encapsulation 378, 379, 383-384 movement: transport by ants 354, 355, 369, 370 - species: effects on encapsulation: 375-376 strain: effects on encapsulation 379-381 survival: effects of ants 358, 359 coccid-ant interactions 351, 352, 354, 353-355,
Chaetothyrium guaraniticum 277 character-state changes: phylogeny 250
coccid-host plant associations 402
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241 Ceroplastodes zavattarii: anal area 16 cervical sclerite 26, 27 Chaetophoma quircifolia 282
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360, 367, 368
425
General Index coccid-myrmecophyte interactions 367 Coccidae: colour: female 5, 114 - f e m a l e characters 5-20, 111-136, 158, 167, 168, 170, 173, 175, 176, 178, 181, 185, 186, 187-198 general appearance 5, 6, 7 - growth 5 - life cycle 5 male: characters 23-30, 139-142 - morphology 5-20, 11-137 no. species 185 no. genera 185 shape 114, 254 - shape: intraspecific variation 203,207, 208 5, 114,254 - size: intraspecific variation 203,207, 208 size: parasitoid preference 414-415 Coccidae genera: no. described 216 - no. per geographic region 216-219, 226 potential number 215 Coccidae species: no. described 213 no. endemic per region 217 - no. per geographic region 216-218, 220, 221 potential number 215 ratio to genera:species 217 Coccinae: no. tribes 190 Coccini: female characters 186, 190, 191 geographic distribution 190 no. genera 190 no. species 190 - phylogenetic relationships 231, 233-235, 240, 241 Coccus: geographic distribution 224, 280 Coccus alpinus: geographic distribution 280 Coccus celatus: geographic distribution 357 - host plants 357, 362 - with ants 352 Coccus hesperidum: alimentary tract 78 cultures 412, 413 - culturing conditions 399-400 dermal wax 92 dorsal microductule 101 dorsal simple pore 98 - early embryo 258 - embryo 258 - encapsulation 380, 3 8 1 , 3 8 2 filter chamber 78, 79 geographic distribution 280, 358 host/parasitoid interactions 384 host plants 358 host plants for cultures 399-400 - midgut 80 nymphal characters 152 nymphal dispersal 341 simple pore 98 wax secretion 92 Coccus longulus: host plants 362 Coccus pseudomagnoliarum: encapsulation 380 Coccus viridis: culturing conditions 400 - geographic distribution 280, 357 host plants 357 - host plants for cultures 400 interactions with ants 355 - on coffee 89-90 Coleoptera 213,307, 308,382, 383 collecting 389-390 collection of parasites 409, 413 Colombia 2 9 1 , 2 9 5 , 2 9 7 , 415 colony size 207 -
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colour: intraspecific variation: female 203, 207, 208 Connecticut 339 connections between zoogeographic regions 223 copper oxychloride 285 corpora allata 84 corpora cardiaca 84 cosmopolitan genera/species 218, 220, 222, 224, 225,227 costal complex 28 cottony camellia scale: see Chloropulvinaria
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cottony grape scale: see Pulvinaria vitis cottony maple scale: see Neopulvinaria innumerabilis cottony vine scale: see Pulvinaria vitis cover: see test coxa: male 26, 27, 28 coxal apical seta: male: 142 coxal bristles: male 26, 27, 29, 142 coxalpores 160, 175, 181 coxal process: female 133, 134 cranial apophysis 23, 26, 27, 140, 162, 247 crawler dispersal: see nymphal dispersal crawlers: see 1st instar-nymphs Crematogaster afn'cana laurenti: myrmecophyte association 365 Crematogaster africana schumanni: myrmecophyte association 365 Crematogaster borneensis: cultivation of coccids 369 - specificity of coccid associations 369 Crematogaster brevispinosa: coccid transport 355 Crematogaster dohrni: coccid association 253 effects of ant exclusion 357 - geographic distribution 357 Crematogaster laurenti: myrrnecophyte association 365 Crematogaster lineolata: coccid protection 361 effects of ant exclusion 359 - geographic distribution 359 Crematogaster macarangicolus: myrmecophyte association 366 Crematogaster treubi: myrmecophyte association 366 - coccid transport 355,369 effects of ant exclusion 357, 358 - geographic distribution 3 5 7 , 3 5 8 myrmecophyte association 366 cribriform plates: female 11, 16, 19, 159, 168, 178, 181, 196 - function 113 structure 99, 116, 119, 121 Cribrolecanium andersoni: geographical distribution 280 Crimea 206 Croatia 294 cruciform ducts/pores: see ventral microducts crumena 75 Cryptococcidae: female characters 159-160, 171 no. genera 170 - no. species 170 - nymphal characters 161, 171 phylogenetic relations 170 Ctenarytaina thysaneura 282 cultivar susceptibility 347 cultures: artificial diets 398 - cleanliness 402 - conditions for success 405 -
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cultures (cont.): costs 409 - criteria for host selection 398 disinfection 404 handling 404 host plants 399-402, 406, 411-415 host plant rots 404, 410 importance of male scales 398 isolation 404 - monitoring 405 parasitoid collection 409, 413 parasitoid release 409 - rearing conditions 399-401,406-416 use of unnatural host plants 397 culturing methodologies: Ceroplastes floridensis 413-415 - Coccus hesperidum 410-413 - Philephedra tuberculosa 415-416 - Saissetia oleae 400-410 culturing biocontrol agents 397-416 culturing techniques 397-416 cupule-shaped pores: female 16, 19 Curculionidae 383 cuticular wax: female test: function 58 Cyphococcinae: female characters 186, 193,194 geographic distribution 193 no. genera 193 no. species 193 -phylogenetic relationships 231, 233-235, 240, -
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Cyprus 281 cytogenic data: intraspecific variation 204 Czech Republic 292 Czechoslovakia 204, 206 Dactylopiidae: female characters 159, 160, 170, 172, 173 male characters 162-163, 173 no. species 170 nymphal characters 161,172, 173 phylogenetic relations 173 Decacrema sp.: coccid associations 368,369 Delphacidae 283 derm: female 6, 15, 115, 128, 158, 159, 176, 185, 186, 190, 193, 196, 338 - nymphs 32, 37, 143, 152-156 dermal areolations: female 9, 15, 115, 116 dermal markings: female 114, 115 dermal microspines: see dermal spinules dermal pores 68 types 93 dermal spinules/spicules: female 13,122, 128 distribution 128 - nymphs 35 Dermaptera 284 Deuteromycotinae 263 deuterotokous reproduction 204, 207 developmental rate: temperature 345,346 Dialeurodes citri 284 diapause 205 - summer 347 winter 347, 348 digestive system 73 Diptera 295 disc pores: male 162 - see also simple/preopercular pores/disc-pores disc-pores: multilocular: female 9, 12, 13, 17, 18, 68, 92, 95, 160, 168, 176, 178, 246 female: distribution 99, 120, 128 multilocular: effects of parasitoids 208 -
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multilocular: function 104, 208 multilocular: male 30 multilocular: secretions 95 multilocular: structure 95, 99, 104 multilocular: see also pregenital disc-pores disc-pores: pregenital: distribution 129 female 13, 116, 122, 129, 160, 168, 185-187, 193, 196,246 pregenital: function 129 pregenital: nymphs 32, 36, 39, 40, 170, 173, 183, 185 pregenital: secretions 129 - pregenital: size 129 structure 116, 122, 129 disc-pores: quinquelocular: female 9, 11, 12, 13, 17, 18, 113, 167, 170 quinquelocular: nymphs 170, 173, 183 quinquelocular: see also spiracular disc-pores disc-pores: spiracular: female 68, 92, 95, 102, 129, 130, 132, 160, 167, 176, 178, 181, 185, 186, 190, 193, 196, 246, 309 - spiracular: cytology 100 distribution 99, 129, 130, 132 spiracular: function I00, 129 spiracular: gland systems 100 spiracular: nymphs 33, 35, 38, 39, 42, 43, 68, 149, 151, 156, 161,239, 246 spiracular: secretions 129 - spiracular: size 129 spiracular: structure 95, 99, 100, 101, 116, 122, 128, 129 discal setae 271 discoidal pores: female 17 - see simple/preopercular pores dispersal: and fecundity 341 - by man 339 - crawler 339-342 distance 341 height 340 - nymphal behaviour 340-342, 344, 345 - period 344 - survival 339 - wind 339,340 stage 251 distribution: intraspecific variation 207, 208 diterpenoids: female test 59, 62 Dolichoderinae 351,362 Dolichoderus bituberculatus: see D. thoracicus Dolichoderus taschenbergi: coccid protection 361 effects of ant exclusion 359 - geographic distribution 359 Dolichoderus thoracicus: coccid protection 361 effects of ant exclusion 357 geographic distribution 357 possible use as a biocontrol agent 370 domatia ix, 364, 367, 368 - forms 365,366 dormancy 347-348 dorsal abdominal setae: male 26, 27, 29 dorsal derm: female 14, 246 dorsal ducts: nymph 152-155 dorsal head setae: male 26, 27, 29, 141,247 dorsal lobes: female 187 dorsal ocular setae 26, 27, 29, 141, 247 dorsal pores: female 18, 118-121, 187 - nymphs 35, 39, 42, 143, 151-155 dorsal pleural setae 26, 27, 29 dorsal nficroducts: see dorsal microductules -
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427
General Index dorsal microductules" female 12, 19, 93, 173, 185 - cytology 105 - distribution 118 gland systems 105 - function 105, 118 - ,lymphs 35, 39, 144, 145 structure 98, 101, 117, 118 dorsal setae: distribution 15, 16, 118 15, 16, 116, 118, 159, 170, 175, 183, 185-187, 193 1 6 , 1 6 , 1 1 7 , 118 size 118 - types 118 dorsal setae: nymphs 35, 39, 40, 42, 143, 152155, 161, 168, 173, 1 8 5 , 2 4 6 , 3 3 8 dorsal tubular ducts: 2nd-instar male 53 2nd-instar male: suture pattern 35 159, 160, 167, 185, 186, 190, 193, 196 - nymphs 35, 39, 144, 145 dorsal tubercles: distribution: female 9, 12, 14, 19, 20, 98, 99, 105, 107, 185-187, 193, 196, 204, 206 185-187, 193, 196 - frequency: female 19 - geographic variation 204-206 - n y m p h s 39, 40, 42, plant host effects on 204 secretions 107 structure: female 19, 20, 98, 99, 107, 119, 123 dorsometaspiracular setae 141 dorsospiracular setae 26, 27, 2 9 , 2 4 7 Dothidiales 275 Drepanococcus chiton: host plants 362 drought 3 3 1 , 3 3 3 , 3 4 7 dry wax vii, viii, 68 ducts: definition 97 ducts: dorsal: nymph: 152-155 ducts: filamentous: female 18, 19, 68, 96, 97, 120 ducts: macrotubular: female 175, 176 ducts: microtubular: female 114, 121, 122, 126, 159, 175, 176, 185, 186, 193,246 - microtubular: nymph 246 ducts: satellite: female 20 ducts: structure 97 ducts: submarginal chambered 123 ducts: tubular: female 102, 158, 168, 170, 173, 175, 181, 186, 187, 208, 246 - tubular: nymph 185 see also dorsal and ventral tubular ducts ductules: definition 97 -
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Echinothecium 276 ecological forms 203 ecosystems 217, 218, 220, 225 edaphic conditions 3 4 3 , 3 4 6 eggs 260, 397, 402, 4 0 5 , 4 1 4 Coccidae: number laid 255 Coccidae: wax coating 255 Egypt 2 8 3 , 3 4 4 eight-shaped pores: female 93, 160, 167, 168, 176, 178, 181, 185 - n y m p h 161, 168, 170, 181,246 structure 119, 120 embryonic development 257-259 emergence: male 254 -
-
-
encapsulation 375-384, 380, 398 - coccid age 378,379 - definition 375 - description 375 - effects of coccid host 375-376 effects of coccid host races 398 effects of coccid host strain 379-381 effect of coccid's age 377-379, 3 8 3 , 3 8 4 effects of coccid's physiological condition 381382 effects of host plant 378,379, 383-384 effects of temperature 398 environmental effects 3 8 1 , 3 8 2 - factors effecting 377-384 - genetic variation 376 - haemocyte types 375 intensity of host reaction 376 - melanisation 375 - methods of avoidance 376 parasitoid eggs and larvae 380 - percentage 3 7 8 , 3 7 9 , 3 8 1 - 3 8 4 - period of 375 - process 375 - superparasitism 377, 382 - susceptibility 376 - temperature effects 376, 378, 379, 382, 383 - types 375 endemic genera 215, 217, 220, 222 endemic species 215, 217, 222, 223 endosulphan 410 endosymbionts 170, 173, 178, 181, 183, 261-266 contamination 264 cultivation of 264 history 261 localization 264 - morphology 261 - movement during development 265 - numbers per coccid individual 264, 265 phagocytosis 264 - reproduction 261 - significance 266 - size 261 transmission 261,265 England 207, 2 7 9 , 3 3 9 , 3 4 6 entomopathogenic fungi 308, 309, 356, 357, 360, 411 environment: effects on encapsulation 3 8 1 , 3 8 2 environmental conditions: ant shelters 356 epicranium 162 epiphytic fungal species 276-278 episternum 25 Ericents pela: I st-instar nymphs 309 - 2nd-instar nymphs 307, 309 - colony 92 discussion of name 303 - dispersal 3 0 6 , 3 0 7 - distribution 305 - ecological requirements 305 - eggs 306 harvesting 313 - host plants 307, 308 - life cycle 3 0 5 , 3 0 6 management 313 natural enemies 307 - number of instars 306 - overwintering 3 0 6 , 3 0 7 - prepupa 306, 307, 310, 313, 315 -pupa 3 0 6 , 3 0 7 , 3 1 0 -
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428
Ind~r
Ericerus pela (cont.):
"seed" production 305, 312 sex differentiation 307 sex ratio 304, 307 Eriochiton: phylogenetic relationships 231, 240,
- symbiont transmission 263 Europe 205,207, 275,279, 292-294, 296, 299, 304 European fruit lecanium: see Parthenolecanium
-
-
corni
241
European peach scale:
Eriococcidae: female characters 159-160, 174, 175 geographic distribution 173 male characters 162, 163,175 no. genera 173 no. species 173 nymphal characters 161,174, 176 - phylogenetic relationships 176, 231,240, 241 Eriococcus coriaceus: effects on host plants 329 Eriopeltinae: female characters 186, 195, 196 geographic distribution 196 no. genera 196 - n o . species 196 -phylogenetic relationships 231, 233-235, 240,
see Parthenolecanium
persicae evolution 214, 222, 225 excretory system 83 extrafloral nectaries 354, 367, 368 in relation to domatia 368 eyes: simple: male 23, 26, 27, 162, 252, 254 pigmentation 252 eyespots: female x, xi, 10, 116, 127, 185, 186, 190, 193, 196,246 - nymphs 32, 36, 37, 42, 147,246
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241 -
status 196
-
Eriopeltisfestucae: dorsal cone-like setae 16 geographic distribution 154 ovisac 7 Eriosoma lanigerum 298 Ethiopian region 215, 216, 217, 219,222-226 monotypic coccid genera 222 no. coccid genera 222 - no. coccid species 222 - coccid species richness 222 Etiennea ferox: female morphology 9 Etiennea petasus: dorsal tubercle 98 tubular duct 96 ventral microduct 95 Etiennea viUiersi: dorsal tubercle 98 - female morphology 12, 14 Euantennaria 277 Euantennaria mucronata 279 Euantennaria tropicicola 278 Euantennariaceae 2 7 5 , 2 7 7 Eucalymnatus tessellatus: nymphal characters 152 Euceramia 277 Eulachnus rileyi 283 Eulecaniinae: female characters 186, 193, 194 geographic distribution 193 no. genera 193 no. species 193 -phylogenetic relationships 231, 233-235, 240, -
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241 Eulecanium: geographic distribution 224 Eulecanium cerasorum: ventral tubular duct 96 Eulecanium ciliatum: host plants 294 Eulecanium franconicum: host-induced differences 208
Eulecanium paucispinosum: parasitoid-induced differences 209 Eulecanium sericeum: host plants 294 - honeydew source 294 - no. species 225 entomophagous fungi 336 - geographic distribution 334, 336 host plant 334, 336 nymphal characters 153 - symbionts 263
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241 - status 196 filter chamber 269 - function 78, 79 - structure 74, 78, 78, 79, 79, 80 filter gut 296 fire ant: see Solenopsis geminata flagellar segments: antennae 24 Flatidae 2 8 3 , 2 9 4 fleshy setae: female 10, 133, 135,246 -male 26, 27, 29, 139, 141, 142, 162 - nymph 32, 37, 149 floral nectaries 354 Florida 2 0 5 , 2 1 5 , 2 8 1 - 2 8 3 Florida wax scale: see Ceroplastes floridensis flower-shaped pores: structure 119, 120 food bodies: ant interactions 367, 368 Forficula auricularia 284 Formica exsectoides: coccid protection 361 effects of ant exclusion 359 - geographic distribution 359 Formica obscuripes: effects of ant exclusion 359 - geographic distribution 359 Formicidae/-inae 3 5 1 , 3 6 2 France 182, 205,206, 281,292, 343 fraxinus aphid 309 fringe setae: see anterior margin setae frontal tubercles: see antennal tubercles -
Eulecanium spp.: geographic distribution 225 Eulecanium tiliae:
Far East 204 fat cells 264 fatty acids 314, 318 fecundity: in relation to dispersal 341 feeding damage 323-324 feeding site: effects on mortality 254 selection 252 femoral setae: nymph 152-155 femur: male 26, 27, 28 fertilization: Coccidae 86, 257 fertilizers 345 - effects on honeydew production 297 effects on host plant responses 332 field characters: see appearance figure-of-eight pores: see eight-shaped pores filamentous ducts: female 18, 19, 68, 96, 97, 120 Filippia follicularis: nymphal characters 153 Filippiinae: female characters 186, 195, 196 geographic distribution 196 - no. species 193 -phylogenetic relationships 231, 233-235, 240,
334,
429
General Index fruit rots 404
Fumago vagans 275 Fumagospora 276 fungal spores: transport by ants 356 fungi 309 - encapsulation 375 fungi 326 furca 25, 26, 27, 247 furcal pit 25, 26, 27
Galandromus occidentalis 405 galls: 112, 190, 325,337-338 Gascardia madagascariensis: colony 92 gena 23, 26, 27, 162, 165,247 genal setae 26, 27, 29, 141, 162, 247 generation time: effects of temperature 345,346 generations: number of: see voltinism genital capsule 163 genital setae 26, 27, 29 genital style 87 genotypes 346 genotypic variation: host plant resistance 331 geographic effects: intra-specific variation 204-208 geographic races: effect on encapsulation: 379 Georgia (USA) 282-284 geotaxic responses: Coccidae 252, 344 geotropism 340 germ band 258, 259, 260 germ cells 257 Germany 292 Ghana 339 gland cells: 2nd-instar male 310 glandular pouch 26, 27, 28, 141, 163,247, 310 glandular tubercles: see dorsal tubercles Gleosporium 309 Gondwanaland 214 gravity 344 Greece 2 9 3 , 2 9 6 , 2 9 7 , 299, 3 4 3 , 3 7 9 , 3 8 1 green coffee scale: see Coccus viridis green shield scale: see Chloropulvinaria psidii grey citrus scale: see Coccus pseudomagnoliarum growth phases: adult female 254 guava scale: see Chloropulvinaria psidii guava mealy scale: see Chloropulvinaria psidii Guizhou Province 304, 3 0 5 , 3 0 7 gum acacia 285
Himalayas 196 Holarctic region 193, 215, 216, 217, 219, 224, 226 Homoptera 75,278, 279, 351,352, 363 honey: % from honeydew 292 honeybees 291-299, 303 honeydew 307 honeydew and bees 291-299 role of apiculturists 298 honeydew 269-274 age of scale 2 9 6 , 2 9 9 amounts harvested by ants 364 amounts per scale 296 - ants 2 9 6 , 2 9 9 , 3 3 3 - aphids 270 - association with sooty moulds 352, 356, 357, 359, 360 attractiveness to Argentine ant 364 - attractiveness to bees 2 9 5 , 2 9 6 - cause of coccid mortality 87 - coccid contamination 325, 326, 333, 357-359, 360, 361 - collecting 389 -composition 2 6 9 , 2 7 8 , 3 6 3 , 3 6 4 - definition 269 - detrimental effects 269 - distance ejected 353 effects of ants on production 353 - effects on coccid behaviour 353 effects on parasitoids 405 - effects of removal 356 -ejection 87, 88, 89, 104, 270, 274 ejection strategies 296 elimination: effect of ants 15 - eliminating organs: morphology 269-274 - frequency of production 353 host plant effects 296 insect behaviour 411 intra-plant variation in quality 364 - location by bees 295 non-secretion of 168 - origin 269 production in domatia 368 palatability to ants 364 rate of production 296 - relationships with sooty mould 275-290 - resource removal 324 secondary plant substances 364 - soil fertility 297 solicitation by ants 363 - sooty moulds 3 2 5 , 3 2 6 , 3 2 8 , 333 - sources 291-295 washing cultures 405,408 waterstress in host plant 297 - whiteflies 270 hop aphid 284 Hot~isciomyces 278 host plant effects 203 - on Coccidae 254, 343,346 - on hibernation 207 - on intraspecific variation 203,205-208 on sex ratio 208 - on synchronization with phenology 244-246 host plant: effects of Coccidae on plant viii, 331,323-333 - apical dominance 330 - architecture 330 - biomass 3 2 9 , 3 3 0 -
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-
-
-
-
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-
habitats: herbs 218 - roots 215,217, 218, 225 rushes and grasses 215, 218, 220 - woody plants 218, 220 haemocytes: types 375 haemolymph 264, 266 hair-like setae: male 26, 27, 29, 141 halteres: see hamulohalteres haltere setae 142 hamulohalteres 26, 27, 28, 139, 140, 163,247 Hawaii 280, 282, 2 8 3 , 3 5 7 head capsule: evolution 74, 75 structure 74 head shape: male 2 3 9 , 2 4 6 head structure: male 23, 139-140 Hemiptera 74, 76 hemispherical scale: see Saissetia coffeae Heteropsylla cubana 282 Heteroptera 75 hibernation: Coccidae 207 -
-
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Index
430 host plant (cont.): effect of fertilizers 332 - flower and fruit production 330 - impact on photosynthesis 326 leaf area 327, 328 leaf loss 328, 329 leaf production 328, 329 host plant condition 331 insect population density 332 - nitrogen loss 324 - nutrition 343,347 nutrient content 328 - photosynthate loss 324 plant weight 329 population size 324 - resource removal 324 - root production 328-330 root/shoot ratio 330 - secondary plant chemicals 332 - shoot growth 328 - stem growth 324 water relations 328 host plant dieback 326-332 host plant responses: stress 332 host-adapted species: encapsulation 376 host-induced variation 8 host plants used for culturing 406-416 Hunan Province 305 Hyaloscolecostroma 276 hydrocarbons 314, 318 Hymenoptera (general) 295, 303, 307, 308, 352, 354, 392 Hymenoptera: see also Parasitoid Index hypopygial seize 124, 125,272 -
geographic distribution 358 Israel 340, 341, 343, 344, 376, 379, 381, 383, 4 0 5 , 4 0 6 , 4 0 9 , 4 1 3 , 4 1 4 , 420 Italy 294, 343,344
-
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iceplant scale: see Pulvinariella mesembryanthemi immature stages: morphology 31-43 mounting and staining 391-394 published descriptions 44-46 insecticides 343 - effects 252 instars: Coccidae 246 integumentary glands: ultrastructure 91-108 inter-antennal seize: female 13,116, 131 - nymphs 35, 40, 42, 149 internal anatomy 73-89, 74 interocular ridge 23, 26, 27, 140, 247 intersegmental sensillae (antennae): female 133, 135 intraspecific variation 203-210 caused by parasitoids 203 -colour: female 203,207, 208 cytogenic data 204 - generations 205,206 - Parthenolecanium corni 203-206 - Pulvinaria vitis 207 - reproduction 204, 206, 207 seasonal development 204-207 sex ratio 204-206,208 - shape: female 203,207, 208 - size: female 203,207, 208 invaginated bilocular tubercles: nymph 144, 145 inverted duct tubercles: female 19 Icerya seychellarum: effects on host plant 324 lllinoia liriodendri 324 India 318, 353,357, 358 Iridomyrmex humile: see Linepithema humile Iridomyrmex scrutator 365 Iridomyrmex sp.: effects of ant exclusion 358 -
-
-
-
-
-
Japan 204, 304, 315 Java 357 Jingdong Province 305 kairomones female test 60-61 kaiztrepsis 259 Kazakhsizn 206 Kermes quercus: honeydew source 292 host plants 292 Kermesidae: female characters 159, 160, 176, 177 male characters 162, 163, 176, 179 no. genera 176 no. species 176 nymphal characters 161, 176, 177 -phylogenetic relationships 178, 231, 235 Kilifia acuminata : nymphal characters 152 Korea 204, 304 Krassilshschik's cell 86, 257 -
-
-
-
-
-
labial seize: nymph 246 labium: female 10, 116, 133, 135, 136, 160, 170, 173, 175, 176, 178, 181, 185, 190, 338 -nymph 32, 161, 165, 168, 170, 176, 181,246 large anterior bristles 29 lateral margin seize 34, 39, 271 lateral pronoizl sclerite 26, 27 lateral pronoizl seize 26, 27, 29 lateropleurite 25, 26, 27 leafhoppers: see Cicadellidae Lecanium sp.: symbionts 263 symbiont transmission 263 Lecanodiaspididae: female characters 159, 160, 178, 179 male characters 162, 163. 180, 181 no. genera 178 no. species 178 nymphal characters 161, 180, 181 phylogenetic relationships 178, 181, 231, 240, 241 lecanoid Coccoidea: female: character states 159-160 character states 162-163, 165, 168, 170, 173, 176, 181, 183 lecanoid group: phylogenetic relationships 230-235, 240-241 leg seize: nymph 32, 151, 156 legs: female 9, 10, 17, 160, 167, 168, 170, 175, 178, 181, 183, 185, 186, 190, 196, 246, 338 - male 28, 140, 142, 252, 254 - nymphs 32, 36, 38, 40, 42, 43, 150, 151-156, 170, 173 -size 132 structure 116, 132, 133 variation 132 Lepidoptera 213 Leptoxyphium fi~mago 285 Leptoxyphium sp. 279 Liaoning Province 304 Lichtensia sp: geographic distribution 224 life cycle: Coccidae 345 life history: Coccidae 251-255, 253 -
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:
General Index
431
light: effects 251,344 Limacinia fernandeziana 279, 280 Limacinia musicola 279 Linepithema humile 406 association with pest outbreaks 352, 361 attractiveness of honeydews 364 effects of ant exclusion 358, 359 - geographic distribution 358,359 - predation on coccids 363 lipids 63-66, 3 1 5 , 3 6 3 , 3 7 0 composition by weight 64 locular pores: definition 93 locular pores: see Ceroplastes-type pores long brown scale: see Coccus longulus -
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-
Macrophya fraxina 309 macrotubular ducts: see ducts: macrotubular Madagasian region 216, 217, 223,224 - monotypic coccid genera 223 - no. coccid genera 222 - no. coccid species 222 - species richness 222, 223 Malaysia 369 male: general characters x, 23-30, 26 male test 49-54 appearance ix, xi, 49-53, 52 composition 49 dorsal habitus variation 50, 52 - function 49 intrageneric patterns 53 structure ix, 51 suture patterns ix, 49, 50, 52, 53 malphigian tubules: number 83 structure 83 Mametia louisieae: female morphology 17 Mancozeb 285 mango shield scale: see Milviscutulus mangiferae Manitoba 339 Margarodidae: honeydew sources 295,297 margin 126 marginal setae: female 8, 11. 12, 14, 17, 18, 117, 126, 158, 160, 175, 181, 185-187, 190, 193, 196, 208, 246 female: distribution 8 - female: frequency 126 female: effects of parasitoids: 208 -nymphs 32, 41, 144, 147, 151-156, 161, 165, 170, 176, 181 -nymph: frequency 147 shape 143, 151 - nymph: types 147 shape 8, 11, 12, 14, 17, 18 structure 117, 126 marginal ridge 25, 26, 27 Massachusetts 294 media 26, 27, 28 medial pronotal setae 26, 27, 29, 141 median crest 23, 26, 27, 246 median ridge 25, 26, 27, 140 Mediterranean black scale: see Saissetia oleae Mediterranean region 181, 215, 218, 223, 225, 226,344, 381 melanisation: associated with encapsulation 375 mesepimeron 25, 26, 27, 162 mesepisternum 26, 27 mesoderm development 259 mesopleural apophysis 25, 26, 27 mesopleurai ridge 25, 26, 27 -
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mesopleural wing process 25, 26, 27 mesopostnotum 25, 26, 27 mesoprephragma 140 mesothoracic spiracle: male 25 mesothorax: male 25 Messinea conica: tubular duct 96 Metacapnodiaceae 278,285 Metacapnodium 278 Metacapnodium juniperae 278, 279 metamerisation 259 metamorphosis 252 Metaphycus alberti: see Parasitoid Index metapleural apophysis 25, 26, 27 metapleural glands: antibiotic secretions from 356 metapleural ridge 25, 26, 27, 247 metapleural wing process 25, 26, 27 Metapolophium dirhodum 283 metapostnotum 25, 26, 27 metasternal apophysis 162, 247 metasternal plate 163 metasternal setae 163 metasternum 26, 27, 28 metatergal setae 26, 27, 29 Metatetranychus urticae 405 metathoracic leg flaps 170 metathoracic spiracle: male 28 metathorax 25 Metcalfa pruinosa 283 metepimeron 25, 26, 27 metepisternum 26, 27, 239 Micrococcidae: - female characters 159, 160, 181, 182 - male characters 162, 163, 183, 184 - no. genera 181 - no. species 181 - nymphal characters 161, 182, 183 -phylogenetic relations 183, 234, 235 microctenidia: nymphs 32, 150, 151 microducts: dorsal: see dorsal microductules ventral: see ventral microducts microtubular ducts: distribution 126 159, 175, 176, 185, 186, 193,246 - function 114, 121 - nymph 246 structure 121, 122 Microxyphium columnatum 285 mid-gut 269 midcranial ridge 23, 26, 27, 140, 162, 247 migration 345 Milviscutulus mangiferae : - field characters x geographic distribution 358 host plants 358,362 - nymphal characters 152 mites 404, 405 see also acarophagous habit and under predatory species in Predator Index Moldavia 205, 206 monotypic genera 215,218, 220, 222, 223 Morocide 285 mortality 252 Moscow 206 moult and moulting 251-254 mounting and staining: age of material 390 - female 391-394 - procedure 391-393 mouth opening: male 23, 26, 27 -
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Index
432 mouth tubercle: male 162 mouthparts: female 10, 74, 133, 135, 167, 190, 338 male 252, 254 - nymphs 32, 38, 149 multilocular disc-pores: see disc-pores: multilocular mycetocytes 264 mycorrhiza: role in plant resistance 330 - symbiosis 330 myrmecophytes: ant-coccid associations 365-367, 367 benefits to ants 367 benefits to plants 367 - coccid establishment 3 6 9 , 3 7 0 - development 369 plant species associated with 365-366 structure 364 Myrmelachista sp.: myrmecophyte associations 366 Myrmicinae 351 Myzolecaniinae: female characters vii, ix, x, 186, 196, 197 geographic distribution 196 no. genera 196 -phylogenetic relationships 231, 233-235, 240, 241 Myzolecanium sp.: within ants nest 368
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Niger 282, 284 Nigeria 281-284 nigra scale: see Parasaissetia nigra Nilaparvata maeander 283 Nitidulidae 398 non-myrmecophyte chambers: ant associations 369 - coccid associations 369 construction 369 North America 204, 205,275,339-341 Norway 292 nut scale: see Eulecanium tiliae nutrient sink 330 nymphal dispersal: see also dispersal nymphs: taxonomic characters 143-156 mounting and staining see immature stages -
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-
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Nassonov pheromone 299 natural enemies 333, 347, 353, 354, 356-363, 370 natural enemies: see also biocontrol Nearctic region 215, 216, 217-219, 224-226, 348 no. coccid genera 218 - no. coccid species 218 - coccid species richness 218 necrosis 324 nectaries 295 neem 285 nematodes encapsulation 375 Neolecanium silveirai: cupule-shaped pores 16 neometabolism 251 Neopulvinaria innumerabilis : - honeydew source 294 host plants 294 nymphal characters 152 - symbionts 263 neoteny 251 Neotropical region 215, 216, 217, 219, 220, 223-227, 3 6 5 , 3 6 6 , 3 6 9 - monotypic coccid genera 220 no. coccid genera 220 - no. coccid species 220 - coccid species richness 220 Netherlands, The 283,379, 381 New England 294 New Zealand 196, 279, 281, 283, 284, 291, 295,297 monotypic genera 222 no. genera 222 - no. species 222 - species richness 222 New Zealand and Pacific region 216, 217, 223-226 New York/New York State 294 New World 207, 415 -
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occiput 162 ocelli: male 26, 27, 140, 162, 165, 247, 254 ocular sclerite 23, 26, 27, 162, 247 ocular setae 162 Oecophylla longinoda: building of protective shelters 356 - coccid associations 353 - dominance 363 effects of ant exclusion 359 - geographical distribution 359 - transport of coccids 355 OecophyUa smaragdina: aggression 3 6 1 , 3 6 2 building of protective shelters 356 - coccid associations 353 - coccid transport 355 - dominance 363 effects of ant exclusion 357, 358 - exclusion effects 3 5 9 , 3 6 0 - geographic distribution 357, 358 % parasitism associated with presence 361, 362 - transport of coccids 354 transport of fungal spores 356 Oecophylla sp.: possible use as a biocontrol agent 370 oesophagus 74 Old World 207 oocyte 257, 265 development 86 structure 86 oogenesis 257 open pores 118, 119 definition 93, 97 structure 93 Oregon 294, 297 - monotypic coccid genera 222 - no. coccid genera 222 - no. coccid species 222 -coccid species richness 222 ostioles 175 outgroups 229, 231-234, 239-241 ovarioles 257, 265 ovary: structure 85, 85 overwintering: Coccidae 344-347, 355 oviparity 2 5 9 , 2 6 0 ovisac x, 193, 196, 208, 210, 225, 246, 254, 255 - function 111 size 113 -types 5, 17, 112-113 ovoviviparous reproduction 259, 260 -
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General Index Pacific region 215,224, 226 - monotypic coccid genera 222 - no. coccid genera 222 - coccid species richness 222 Palaearctic region 193, 196, 204, 213, 216, 217-221,223-227, 348 monotypic coccid genera 218 no. coccid genera 218 no. coccid species 218 coccid species richness 218 Panonychus citri 405 Panonychus ulmi 405 Papua New Guinea 352, 358, 359, 361, 369 Papyrius nitidus: aggressiveness 361,362 association with coccids 361 % parasitism associated with presence 362 Paralecaniini: female characters 186, 190, geographic distribution 190 no. genera 190 no. species 190 -phylogenetic relationships 231, 233-235,
433
-
153 215,
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-
365,
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-
-
361,
191
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-
240,
241 Paralecanium carolinensis: female morphology 8 paraopercular pores: see preopercular pores Parasaissetia: encyrtid parasitoids/hyperparasitoids 496 geographical distribution 224 Parasaissetia nigra: culturing conditions 400 geographic distribution 281, 358 host/parasitoid interactions 384 host plants 358 nymphal characters 153 parasitoids/parasites/parasitism: 208, 210, 307, 3 0 8 , 3 5 3 - 3 5 5 , 3 6 1 , 3 7 0 , 375,397 - ant interactions 353,354, 356-359, 361,370 cause of intraspecific variation 203 - collection of from culture 409, 409 - effects on coccids 208, 209, 210 effects on tubular ducts 208 encapsulation 375-384 mass rearing 397-416 see also natural enemies/biocontrol parastigmal processes: male test 50, 51, 52 parenchyma 324 Parodiopsidaceae 275 parthenogenetic reproduction 203,206-208,297 Parthenolecanium: geographic distribution 224 Parthenolecanium corni: ecological forms 203 effect of fertilizer 298 geographic distribution 204, 281 - geographic variation 203 host plants 292, 294 -honeydew source 292, 294 - intraspecific variation 203-206 - life cycle 245, 253, 345 nymphal characters 153 no. host plants 203 sex ratio 203 - transfer experiments 203 - voltinism 2 0 3 , 2 0 5 , 2 0 6 Parthenolecanium fletcheri: geographic distribution 292 - honeydew source 292 -
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
effects of fertilizer on honeydew 298 - honeydew source 292 host plants 292 tentorium 77 Pan~s major 309 pathogens 356, 360, 361 pedicel 23, 26, 27, 257 pela wax 311,314, 316 - commercial production 305 chemical properties 314 climatic conditions 304 effects of fertilization 313 effects of pruning 313 extraction 315,316 geographic distribution 304 - history 303,304, 312 physical properties 315 - production 304, 309, 312, 313 - secreting periods 304, 309, 310 -uses 303,317 - yield 309 pela wax scale: see Ericen~s pela penial lobe: prepupa/pupa 42, 43 penial sheath 26, 27, 28, 142, 163, 183, 247, 252, 254, 310 Pennsylvania 205,282 Peregrinus maidis 282 peripheral wax fringe: male test ix, xi, 50, 51 peritreme: female 26, 27, 28, 33, 130, 133, 132 Perkinsiella saccharicida 282 pest outbreaks: ants associated with 52, 61 Phaeosaccardinula 277 Phaeoxyphiella 276,277 phagocytes 266 pharynx 74, 76 Pheidole megacephala 352 - behaviour: coccid protection 361,362 effects of ant exclusion 357 geographic distribution 357 Pheidole sculpturata: association with pest outbreaks 352, 362 pheno-immunity 346 Philephedra tuberculosa: culturing conditions 400 geographic distribution 281 host plant for cultures 400 mass rearing 415-416 Philidris cordatus: myrmecophyte associations 365 phloem 324, 326 phloem sap: uptake 323 - value as food 325 Phoenict~rus auroreus 309 phoresy 339 Phorodon humuli 284 photoperiod response: Coccidae 205, 252, 340, 344 phototropism 340 Phragmocapnias 276 Phragmocapnias betle 279 Phthorimaea operculeUa 405, 410 -
-
-
Parthenolecanium rufulum:
-
-
-
host plants 292
Parthenolecanium persicae: dorsal tubercle 98 Parthenolecanium quercifex: nymphal characters
-
-
-
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Index
434 phylloplane 278 Phyllostroma myrtiUi: honeydew source 292 host plants 292 phylogenetic analysis: character matrix 248-249 characters and character states 246-247 material used 244-245 - methodology 229 phylogenetic relationships 230-233,238-241 phylogenetic trees 230, 231-235, 240, 241 phylogeny/relationships: lecanoid Coccoidea 165, 167, 168, 173, 176, 178, 181, 183 phylogeny 229-242 Physokermes hemicryphus: amount of honeydew produced 296 geographic distribution 292 - honeydew source 291-299 host plants 292, 294 nymphal characters 153 Physokermes piceae: coccid with honeydew 293 - honeydew 293 - honeydew collection by bee 293 phytopathogenic fungi 275 pigeon pea: see Cajanus cajan pigments: female test 62, 65 pilzorgan 265 Plagiolepis longipes: see Anoplolepis longipes plant hormones 205 plant pathogens: coccids as vectors 326 plant resistance/susceptibility: see cultivar susceptibility plant sap: composition 79 plates: cribriform: female 159, 168, 178, 181, 196 plates: see also anal plates pleural sclerotisation 141 pleural wing process 239 pleurites: see abdominal pleurites Plokamidomyces 278 plum lecanium: see Sphaerolecanium pnmastri pocket-like sclerotisations: derivation 124 distribution 124 12, 14, 20, 190, 193, 196 function 124 structure 116, 119, 124 pocket-like tubercles: see pocket-like sclerotisations Podomyrmex laevifrons 368 Podomyrma sp.: myrmecophyte associations 365 Poland 206,292 Polychaeton juniperi 278 Polychaeton salicinum 276 Polychaeton spp. 279 polydnavirus 376 polymorphism 203 polyphagy 203-207 pore types: female 118-121, 128-131 pores: anal ring wax 273 bilocular: female 19 bilocular: nymph 144, 145, 156 bilocular: structure 119, 121 bilocular: see also dorsal microductules campaniform: female 10, 32, 37, 133, 134, 135 - Ceroplastes-type: female 18, 68, 93,108, 119, 120, 187 closed: female 93, 97, 118, 119 160, 175, 181 - cruciform: see ventral microducts -
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cupule-shaped: female 16, 19 - dark-rimmed: see simple/preopercular pores - dermal 68 - disc: see simple or preopercular pores discoidal: female 17 discoidal: see simple pores female 18, 118-121, 187 -dorsal: nymphs 35, 39, 42, 143, 151-155 female 93, 160, 167, 168, 176, 178, 181, 185 -eight-shaped: nymph 161, 168, 170, 181,246 eight-shaped: structure 119, 120 figure-of-eight: see pores: eight-shaped flower-shaped: structure 119, 120 female 13, 118-121, 128-131 - locular: see Ceroplastes-type pores -open 93, 97, 118, 119 - paraopercular: see preopercular pores female 116, 122, 130 distribution: female 18, 19, 99, 107, 108, 120, 185, 193 female 98, 116, 119, 120, 185, 193 -preopercular: nymphs 36, 39, 40 structure: female 9, 12, 98, 99, 116, 119, 120 quinquelocular: see spiracular disc-pores satellite 119, 120, 123 female 13, 19, 118, 119, 120, 131 simple: female structure 97, 98, 108, 118, 119, 120, 131 - simple: nymphs 35, 36, 39, 40, 144, 145, 161 tarsal campaniform: see pore: campaniform translucent: female 246 trilocular: female 175 -trilocular: nymph 35, 144, 145, 176 tubercular: female 19 ventral: female 13, 128-131 ventral: nymphs 35, 39, 144, 149 postalare 25, 26, 27 posterior metaspiracular setae 141 posterior metasternal setae 26, 27, 29, 142, 247 posterior notal wing process 25, 26, 27 posterior postalare ridge 25, 26, 27 postertor tentorial pit 26, 27 posterior tentorial arm 26, 27 postmesospiracular setae 26, 27, 29, 142 postnotal apophysis 25, 26, 27 postoccipital ridge 162, 246 postocular ridge 23, 26, 27, 140, 162, 247, 247 posttergital setae 26, 27, 29, 141,247 posttergite 23, 26, 27, 142 pre-antennal pores: female 116, 122, 130 pre-antennal pore: nymphs 39 prealare 25, 26, 27 precoxal ridge 25, 26, 27 predation: ants 352 predators/predation 308, 309, 353-355, 361, 362, 397,398,405 - ant interactions 353,356-359, 361,362, 370 predatory mites 403,405 pregenital disc-pores: see disc-pores: pregenital pregenital setae: female 13, 116, 131, 186, 189, 190, 196 - nymphs 32, 39, 152-155 preocular ridge 23, 26, 27, 140, 162, 176,247 preopercular pores: distribution: female 18, 19, 99, 108, 120, 185, 193 -
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General Index
435
preopercularpores (cont.): function 108, 120 gland systems 108 nymphs 36, 39, 40 female 9, 12, 98, 99, 116, 119, 120 preoral ridge 23, 26, 27, 140, 165 prepupa 4 9 , 2 5 1 , 2 5 2 , 253 characters 41 prescutal ridge 25, 26, 27 prescutal suture 25, 26, 27 prescutum 25, 26, 27, 247 preservation and storage 390-391 prevulvar setae: see pregenital setae pro-episternum 23, 26, 27 Prociphilus fraxini 309 pronotal ridge 23, 26, 27 propleural apophysis 23, 26, 27 propleural ridge 23, 26, 27 prosternal setae 26, 27, 29, 141 prosternum 23, 26, 27 protection: ant behaviour associated with 352-354, 361 prothorax: male 23 Protopulvinaria pyriformis : lst-instar female morphology 33 - 2nd-instar female morphology 36 - 3rd-instar female morphology 40 - culturing conditions 400 -encapsulation 378,379, 380, 382 field characters x geographic distribution 280 host/parasitoid interactions 384 host plants for cultures 400 nymphal characters 152 pruning 347 Pseudococcidae: female characters 159, 160 male characters 162, 163 nymphal characters 161 phylogenetic relationships 231 Pseudomyrmex ira: myrmecophyte associations 365 Pseudomyrmex sericeus group 365 - myrmecophyte associations 365,366 Pselutomyrmex sp.: association with swollen acacia thorns 368 - harvesting of coccids 363,369 Pseudomyrmex viduus: myrmecophyte associations 366 Pseudophilippia quaintancii: l st-instar female morphology 33 2nd-instar female morphology 36 2nd-instar male morphology 38 - 3rd-instar female morphology 40 - 3rd-instar male (prepupa) morph 42 4th-instar male (pupa) morphology 43 nymphal characters 154 Pseudopulvinariinae: phylogenetic relationships 231, 233-235, 240, 241 female characters 186, 196, 197 geographic distribution 196 no. genera 196 PsyUa pyri 282 Psylla pyricola 282 Psyllidae/-inae/-oidea 282, 296 Pterocallis alni 283 Pterochloroides persicae 283 Pulvinaria: geographic distribution 224, 280 -
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Pulvinaria acetqcola: nymphal characters 152 Pulvinaria crassispina: parasitoid-induced differences 209 Pulvinaria floccifera: see Chloropulvinaria floccifera Pul~qnaria innumerabilis : see Neopulvinaria innumerabilis Pulvinaria mesembryanthemi." see Pulvinatiella mesembryanthemi Pulvinatqa pistaciae: honeydew source 294 host plants 294 Pulvinaria psidii: see Chloropulvinaria psidii Pulvinaria regalis: culturing conditions 400 host plants for cultures 400 multilocular disc-pore 95 quinquelocular disc-pore 102 spiracular disc-pore 102 tracheae 82 tubular duct 102 Pulvinaria urbicola: culturing conditions 400 host for cultures 400 host/parasitoid interactions 384 Pulvinaria vitis: anal apparatus 273 blastoderm stage 258 differential sexual infestation sites 207 host plants 207 - intraspecific variation 207 invagination process 258 - male/female colonies 207 - reproduction 207 Pulvinaria/-iini: female characters 186, 192, 193 distribution 193, 225 no. genera 193,225 - no. species 193,225 -phylogenetic relations 231,233-235, 240, 241 Pulvinariella mesembryanthemi: culturing conditions 400 entomophagous fungi 334 geographic distribution 334, 358 - host for cultures 400 host plants 334, 358 nervous system 83 - nymphal dispersal 339, 340 - symbionts 263 Pulvinariini: female characters x pupa 49, 251,252, 253, 254 characters 31, 43 - differences from prepupa 43 puparium 162 Pycnonotus sinensis 309 pyriform scale: see Protopulvinaria pyriformis Pyrilla perpusilla 282 -
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quinquelocular 17, 18, 113, -nymph 170, quinquelocular pores
disc-pore: female 9, 11, 12, 13, 167, 170 173, 183 pores: see also spiracular disc-
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radial vein (radius) 26, 27, 28 rainfall 343 - effects 252 Rasutoria 277 rate of development 343 rearing techniques 397-416
Index
436 red wax scale: see Ceroplastes rubens relative humidity 343-346 - effects 251,252, 340 remote sensing: detection of infestations 411 remounting old slides 385 reproduction: effects ofparasitoids: 208 - intraspecific variation: 204, 206,207 reproductive system: female 84, 84, 86 male 87 resin 324 resinous materials: female test 58 respiratory system 80 Rhizopus 404 Rhopalosiphum padi 283,285 Richardiella taiensis: female morphology 11 rodents 309 Romania 2 0 5 , 2 8 3 , 2 9 4 Russia 204-208, 292, 304, 346, 398 -
Saissetia: geographic distribution 224, 225 - no. species 225
Saissetia coffeae: culturing conditions 401 - encapsulation 380, 382 field characters x host/parasite interactions 384 host plants for cultures 401 nymphal characters 281 spiracular disc-pores and wax 92 stigmatic spines and wax 92 Saissetia miranda: culturing conditions 401 - geographic distribution 359 host for cultures 401 host plants 359,362 Saissetia oleae: culturing conditions 401 - early embryo 258 general appearance 7 - geographic distribution 359 host/parasite interactions 384 host plants 359 host plants for cultures 401 mass rearing 406-410 multilocular disc-pore wax 92 - nymphal characters 153 spiracular disc-pores 92 tubular ducts 96 Saissetiini: female characters x, 186,192, 193 geographic distribution 193 no. genera 193 no. species 193 -phylogenetic relations 231,233-235, 240, 241 Saldaalin 206,207 saliva 75, 77 salivary pump: structure 74, 77 salivary sheath 75 saprophytic fungi 275 Sardinia 343 Sarucallis kahawaluokalani 283 satellite ducts: female 20 satellite pores: female 119, 120, 123 sawflies 309 scape: female 23, 26, 27 - nymph 246 Scoriadopsis 276 Scorias 276 Scorias philippensis 279 Scorias spongiosa 279,280 scutal setae 26, 27, 29, 141,247 scutellar foramen 25, 26, 27, 140
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scutellar setae 26, 27, 29, 142, 163 scutellum 25, 26, 27, 139, 142, 247 scutum 25, 26, 27, 140, 162, 247 seasonal development: intraspecific variation 204-207 seasonal history: Coccidae 343-347 secondary plant substances 364 host plant responses 332 segmentation: dorsal: female 7, 116, 246 - nymphs 32, 37, 41, 42 ventral: female 128 Senegal 282 sensilla basiconica 26, 27, 29 sensilla placodeum 26, 27, 29 serosa 257-259 sesterterpenoids: female test 59, 60, 61, 62, 63, -
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64 setae: abdominal 162 - abdominal pleural 247 abdominal ventral 247 alar 29, 142, 247 anal lobe: female 126,246 - anal lobe: nymph 246 anal plate: female 15, 16, 122, 124, 272 anal plate: nymphs 32-34, 39, 40, 42, 145, 146, 151, 152-155 anal ring 88, 89,273, 273, 274 ante-anal 26, 27, 29, 247 - antemetaspiracular 26, 27, 29, 141,247 anteprosternal 26, 27, 29 - anterior margin: female 145, 271,272 - anterior margin: nymphs 39, 40, 145 anterior metasternal 26, 27, 29, 142 apical 26, 27, 29, 271 basisternal 26, 27, 29, 142 capitate 141 - cone-like 16 -discal 271 -dorsal: female 15, 16. 116, 117, 118, 159, 170, 175, 183, 185-187, 193 - dorsal: nymphs 35, 39, 40, 42, 143, 152-155, 161, 168, 173, 185,246,338 dorsal abdominal: male 26, 27, 29 - dorsal head: male 26, 27, 29, 247 - dorsal ocular 26, 27, 29, 141,247 dorsal pleural 26, 27, 29 dorsometaspiracular 141 -dorsospiracular 26, 27, 29, 247 - female 9, 11, 12, 13, 15, 16, 17, 18, 118, 126, 131 - femoral: nymph 152-155 - fleshy: female 10, 133, 135,246 fleshy: male 26, 27, 29, 139, 141, 142, 162 fleshy nymphs 32, 37, 149 - fringe: see anterior margin setae -genal 26, 27, 29, 141, 162, 247 genital 26, 27, 29 hair-like: male 26, 27, 29, 141 haltere 142 - hypopygial: female 124, 125,272 female 13, 116, 131 inter-antennal: nymphs 35, 40, 42, 149 labial: nymph 246 lateral margin 34, 39, 271 lateral pronotal 26, 27, 29 -leg: nymphs 32, 151, 156 marginal: female 8, 11, 12, 14, 17, 18, 117, 126, 158, 160, 175, 181, 185-187, 190, 193, 196, 208, 246 -
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General Index
437
setae (cont.): marginal: nymphs 32, 41, 143, 144, 147, 151, 156, 161, 165, 170, 176, 181 medial pronotal 26, 27, 29, 141 metasternal 163 metatergal 26, 27, 29 - ocular 162 posterior metaspiracular 141 -posterior metasternal 26, 27, 29, 142, 247 postmesospiracular 26, 27, 29, 142 -postmetaspiracular 26, 27, 29, 142, 247 poststernal 247 -posttergital 26, 27, 29,247 female 13, 116, 186, 189, 190, 196 -pregenital: nymphs 32, 39, 152-155 prevulvular: see pregenital prosternal 26, 27, 29, 141 - scutal 26, 27, 29, 141,247 scutellar 26, 27, 29, 142, 163 spiracular: see stigmatic spines subapical 26, 27, 29 submarginal: female 11, 13,116, 132 tegular 26, 27, 29, 142 tibial: nymph 246 trochanter: nymph 152-155 - ventral abdominal: male 26, 27, 29, 141, 239, 247 ventral head 26, 27, 29, 141,247 ventral: female 117, 131 ventral: nymph 35, 39, 42, 144, 149, 151, 156 ventropleural 26, 27, 29 settling 344 sex ratio: intraspecific variation 204-206,208 sexual dimorphism 35,251,254 shade: effects on ant-coccid populations 356 Shanxi Province 305 shellac 291 shelters: 355,359,370 protection, built by ants 355,356 Siberia 207 Sichuan Province 304, 305,307, 318 silkworm 303 simple disc-pores: see simple pores simple eyes: male 23, 26, 27, 140, 162, 252, 254 simple pores: distribution 98, 108 -cytology 108 13, 19, 118, 119, 120, 131 gland systems 108 - nymphs 35, 36, 39, 40, 144, 145, 161 structure 97, 98, 108 Sitobion avenae 283,285,325 slide preparation 391-394 Slovenia 292 sodium hypochlorite 404 Solenopsis geminata: 352 - aggression 361,362 - coccid transport 355 % parasitism associated with presence 361, 362 Solenopsis sp.: pest outbreaks 352 sooty moulds viii, 269, 275-290, 325-328,332 control 285 dispersal 284 - distribution 278,280-283 - effects of ants 326,333 - effects of rain 279,325 - effects on coccoids 323,333, 353,356 -
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effects on plants 280-284, 325-327, 352 food for insects 284 honeydew 353-360 impact on crop value 325 insect interactions 280 - light penetration 326,327 plant interactions 279 remote sensing 285 - specificity 280 South Africa 190, 280, 338, 339, 343, 358, 361, 406 South America 190, 193,280, 318 southern hemisphere 187 Spain 183,281 species complex 204, 207 species:genus ratio 217 species per geographic region 216 sperm bundles 86, 87, 257 spermatheca 85, 85, 86,257 Sphaerolecanium prunastri: nymphal characters 153 - symbionts 263 spiders 307. 309 spiracles: female 10, 80, 81, 81, 116, 132, 133, 160, 183, 186, 190, 196, 338 female structure 116, 132, 133 female variation 132, 133 male 26, 27 - nymphs 33, 38, 42, 149 structure 80, 81, 81 spiracular cleft: see stigmatic cleft spiracular disc-pores: see disc-pores: spiracular spiracular furrow/groove: see stigmatic furrow/groove spiracular peritreme: female 11 spiracular pores: see spiracular disc-pores spiracular sclerotisation: see stigmatic sclerotisation spiracular setae/spines: see stigmatic setae/spines Sri Lanka 279, 280. 357 St Petersburg 206 stellate scale: see Vinsonia stellifera sterility: coccids: effects of parasitoids 210 Sternorrhyncha 79, 296,297 Stictococcidae: phylogenetic relationships 231 Stictolecanium ornatum: appearance of dorsum 16 stigmatic area: definition 116, 126 stigmatic cleft: female 8, 9, 17, 114, 116, 126, 186, 190, 193, 196 - nymphs 37, 149 stigmatic furrow/groove: female 8, 9, 11, 12, 13, 116, 132, 168, 178 - nymphs 32, 38, 149, 156 stigmatic sclerotisation: female 115, 116, 126, 190 - nymphs 33, 39 stigmatic spines/setae: effects of parasitoids 208 - female 8, 8, 9, 11, 17, 18, 160, 168, 176, 181, 185, 187, 190, 196, 246 female: number 9, 10 female: shape 9, 10 - frequency 127 - nymphs 32, 33, 36, 39, 40, 42, 148, 151-156, 161, 170, 176, 181,246 - nymph: types 148 structure 116, 117, 127 wax 100 storage media 390 -
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Index
438
Strigopodia 277 stylets 75, 74, 76 - pathway 75 - penetration 323 subalare 25, 26, 27 subapical setae 26, 27, 29 see lateral margin setae subepisternal ridge 25, 26, 27 submarginal chambered ducts 123 submarginal setae: female 11, 13,116, 132 submarginal tubercles: see dorsal tubercles suboesophageal ganglion 74 sudden death disease: cloves 326 Sulphur 285 superparasitism: effects on encapsulation 376, 377, 382 supporting bars: female 15,122, 125,271,272 suspensorial sclerite 25, 26, 27, 247 suture patterns: male test ix, xi, 49, 50, 52, 53 Sweden 292 Switzerland 206,292 symbiont growth: host regulation 265-266 symbionts: types 264 symbiosis 261,264 -
Tachardiidae: female characters 159, 160, 183, 184 male characters 162, 163, 183 no. genera 183 no. species 183 nymphal characters 161, 183,188 -phylogenetic relationships 183,231,234, 235 Takahashia japonica: ovisac 7 take-off behaviour: coccid nymphs 340, 341 Tapinoma spp.: aggressiveness 361,362 - geographic distribution 359 % parasitism associated with presence 361, 362 tarsal campaniform pores: female 134, 160, 181, 185, 190 -nymph 161, 165, 170, 173, 176, 183,246 tarsal digitules: female 10, 133, 134 male 26, 27, 29 -nymphs 32, 36, 38,41, 161, 183, 185,246 tarsus: male 26, 27, 28, 163 Tasmania 282 taxonomic characters: lst-instar nymph 151-155 Technomyt~zex albiceps: effects on coccids 357 geographic distribution 357 tegula 26, 27, 28 tegular setae 26, 27, 29, 142 temperature 343-346 - effects 251,252 - effects on encapsulation 376, 378, 379, 382, 383 - effects on survival 340 Tenaphalara malayensis 282 tendon-like apodeme 26, 27 Tenthredinidae 309 tentorial pits 23 tentorium: structure 76, 76, 77 tergites: see abdominal tergites terpenoids: in female test 58-62 tessellated scale: see Eucalymnatus tessellatus test: aqueous composition 55, 66-67 attachment to substrate 252 - changes in composition with growth 67 - chemistry 55 -colour 113 -
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composition by weight: Coccidae 55 composition by weight: other Coccoidea 55, 56 - composition: hydrocarbons 58 composition: other components 63 composition: pigments 62-63 composition: ratio of wax components 57 composition: terpenoids 58-62 composition: waxes 55 112, 159, 167, 168, 170, 175, 183, 185-187, 193, 196 functions 55, 113 - "interior honeydew" 55, 66 - nymphs 31, 41 secretion 67, 68 - secretion periods 55 structure 111-114, 252, 254 5, 185 uses to man 55 testes 87 Tetraponera sp. 365 - harvesting of coccids 363, 369 Texas 294, 381,398 Thailand 282 thelytokous reproduction 204, 207 thelytokous races 264, 265 Thiorit 285 Thysanoptera 213 tibia: male 26, 27, 28 tibial setae: nymph 246 tibial spurs: male 26, 27, 142, 163, 165,247 tibio-tarsal articulations: female 10, 186, 193, 246 - nymphs 32, 38 sclerosis 133, 134 Toumeyella liriodendri: entomophagous fungi 335 - geographic distribution 335, 359 - host plants 335,359 Toumeyella numismaticum: nymphal dispersal 341 Toumeyella patvicot~is: geographic distribution 359 host plants 359 Toumeyella sp.: culturing conditions 401 effects on host plant 329 general appearance 7 - geographic distribution 359 - host for cultures 401 host plants 359 tracheal system: structure 81, 82 Transcaucasia 206, 207 transfer experiments: intraspecific variation 203, 207 transitory mycetome 265 translucent pores: female 246 transport: by man 208 Treubiomyces 277 Trialeurodes merlini 282 Trialeurodes vaporariorum 282, 284 triangular plate 25, 26, 27 Trichomerium 276 Trichomerium grandisporum 279 Trichopeltheca 277 Trichopeltheca asiatica 279 trilocular pores: female 175 -nymphs 35, 144, 145, 176 Trinidad 357, 359 Tripospermum myrti 285
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General Index Tripospermum spp. 279 trochanter: male 26, 27, 28 trochanter setae: nymph 152-155 trochantofemur: male 163, 165, 181 trophobionts ix, 352, 369 tubercles: antennal: see antennal tubercles - dorsal: see dorsal tubercles frontal: see antennal tubercles glandular: see dorsal tubercles invaginated bilocular: see invaginated bilocular tubercles - inverted duct: see inverted duct tubercles pocket-like: see pocket-like sclerotisations - submarginal: see dorsal tubercle tubercular pores: female 19 Tuberculatus paiki 282 tubular ducts: 102, 158, 168, 170, 173, 175, 181, 186, 187, 208, 246 2nd-instar male 39 - cytology 103, 104 female 19, 99, 116, 122 female 113, 123, 159, 160, 167, 185, 186, 190, 193, 196 -dorsal: nymphs 35, 39, 144, 145 effects of parasitoids 208 68, 158, 168, 170, 173, 175, 181, 186, 187, 246,309 - function: female 14, 104, 113, 123,208 gland systems 103 male 309, 310, 311 - nymph 185 structure: female 9, 11, 12, 13, 14, 17, 18, 19, 95, 99, 103, 123 female 113, 131, 160, 181, 185-187, 190, 193, 196 nymphs 32, 36, 39, 149 Tunisia 283 Turanian scale: see Rhodococcus turanicus Turkey 293,297, 343 Tyrophagus sp. 405 -
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UK: see United Kingdom Ultracoelostoma assimile: honeydew source 292
host plants 295
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Ultracoelostoma brittini: honeydew source 292
host plants 295 ungual digitules: see claw digitules United Kingdom 206 USA 296-298, 318, 359, 415 USSR 215,343 -
vagina: structure 85 Venetian red dye 62 Venezuela 357 ventral abdominal setae: male 26, 27, 29. 141, 239,247 ventral head setae 26, 27, 29, 141,247 ventral microducts: distribution 99, 105, 130 14, 18, 68, 158, 160, 168, 173, 175, 176, 181, 185, 187, 190, 246 function 130 gland systems 107 - n y m p h 35, 39, 144, 149, 161, 165, 168, 170, 173, 176, 183 - f e m a l e
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structure 95, 99, 107, 117, 130 ventral median ducts: nymphs 152-155 ventral plate 257 ventral pores: female 13, 128-131 ventral pores: nymphs 35, 39, 144, 149 ventral sclerite 26, 27 ventral setae: female 117, 131 - nymphs 35, 39, 42, 144, 151, 156 - nymph: types 149 ventral structures: female 10-13, 128-136 ventral submedian setae: see pregenital setae ventral thickenings: see supporting bars ventropleural setae 26, 27, 29 Vinsonia stellifera: nymphal characters 153 Virginia 2 1 5 ,2 8 3 ,3 4 3 viteUine membrane 257, 259 vitelline nuclei 258 viviparous reproduction 25 voltinism 31, 343-347 - intraspecific variation 205, 206 - Parthenolecanium corni 203 vulva 136, 181,252, 272 position 12 -
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walking speed: coccid nymphs 340 wax(-es)" anal tubes 294, 295 - Ceroplastes 318
female test 56-58 - function 303 - on honeydew 270, 274 wax gland pores 91, 94 - frequency 91 - role in taxonomy 92 wax commercial production 303-319 weeds 347 weevils 308 West Bengal 284 West Indies 357, 359 wet wax viii, 68 Wettasull 285 white wax scale" see Ceroplastes destructor white powdery scale" see Cribrolecanium ander-
soni
white scale of India: see Ceroplastes ceriferus wind 3 2 5 , 3 4 3 , 3 3 9 , 3 4 0 - effects 251,252 wingbuds 252, 254 - prepupa/pupa 42, 43 wing-veins 26, 27 wings 28, 140, 142 Yatesula 277 yeast 325 yeast-like micro-organisms 264-266 yolk 258. 259, 265 Yunnan Province 208, 304, 307
sp." myrmecophyte associations 365 Zambia 280 Zanzibar 359 Zhejiang Province 305 Zimbabwe 181 zoogeography" Coccidae 213-227
Zactyptocerus
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441
Index to Coccoidea Taxa Acantholecanium 115, 131, 135,218 Aclerda 157, 158, 165, 185,239, 244 Aclerda berlesii 294 Aclerda tillandsiae 165,244 Aclerdidae 3, 157, 158, 162, 165, 167, 168, 183,230-242, 244, 248, 249, 295 Akermes 120, 127, 128, 135 Akermes bruneri 128 Akermes cordiae 149, 365 Alecanium 126, 134, 150, 151, 156,223 Alecanium hirsutum 134, 150, 151 Alecanochiton 118, 120, 124, 125, 127, 198, 220, 272 Alecanochiton marquesi 120, 127 Alecanopsis 131,222 Alichtensia 119, 123 Alichtensia attenuata 119 Alichtensia orientalis 143, 156 Allopulvinaria 114, 129-131, 134, 135,222 Anomalococcus 178 Anopulvinaria 119,220 Anopulvinaria cephalocarinata 20, 98, 107 Antandroya 121, 130, 222 Anthococcus 119-121, 126, 131,222, 223 AonidieUa aurantii 55, 61,339,340, 362, 376, 382 Apiomorphinae 157 Archeococcoidea 3 Asterococcus muratae 56, 58, 64 Asterolecaniidae 157, 158, 162, 165, 167, 168, 176, 178, 181, 185, 230-232, 235-238, 241-244, 248,249, 325 Asterolecanium proteae 167, 168, 244 Aulacaspis tegalensis 339-342 Austrolichtensia 124, 125, 222, 272, 273 Austrolichtensia hakearum 351 Bodenheimera 120, 126, 127, 170, 181, 185, 196,218,239, 240, 244 Bodenheimera rachelae 44, 145, 146,244 brown apricot scale: see Parthenolecanium comi brown scale: see Parthenolecanium comi brown soft scale, see Coccus hesperidum Cajalecanium 118, 131, 218 CaUococcus 134 Callococcus acaciae 63, 69 Cardiococcinae 143, 149, 151, 156, 185-187, 232, 236-240, 244, 248,249, 255,272 Cardiococcus 239,240, 244 Cardiococcus umbonatus 113 Caribbean black scale: see Saissetia neglecta Carteria 157, 185 Cerococcidae 56, 58, 158, 162, 167, 168, 170, 176, 178, 181, 230-232, 234-239, 241, 244, 248, 249 Cerococcus 170 Cerococcus quercus 244
Ceronema 123, 145 Ceronema afn'cana 5, 7, 15 Ceronema banksiae 44, 123, 145 Ceronema koebeli 44, 51 Ceroplastes 39, 44, 46-48, 55-64, 66-72, 91, 92, 95, 97-99, 106-109, 185, 187, 217, 218, 220, 222, 223, 225, 239, 240, 244, 303, 318-320 Ceroplastes actiniformis 44 see also General Index Ceroplastes albolineatus 57-59, 63 Ceroplastes beriniae 244 Ceroplastesbrevicauda 16, 44 see also General Index Ceroplastes caesalpiniae vii, viii Ceroplastes ceriferus viii, 29, 44, 53, 56, 97, 142, 148, 151 see also General Index Ceroplastes destructor 44, 53,303,332, 347 see also General Index Ceroplastes dugesii cover, viii Ceroplastes floridensis 44, 48 252, 255, 280, 284, 339,341,344, 378,383,384, 399,405, 413,416 see also General Index Ceroplastes hodgsoni 18, 19 Ceroplastes irregularis 53 Ceroplastes janeirensis 244 Ceroplastes japonicus 44, 63,253 see also General Index Ceroplastes nakaharai 53 Ceroplastes pseudoceriferus 44, 56, 58, 60-62, 70-72, 399 see also General Index Ceroplastes rubens 56, 57, 64, 70-72 see also General Index Ceroplastes rusci 44, 53 262, 263, 294, 358, 399,413,414 see also General Index Ceroplastes sinensis 7, 44, 112, 113, 251, 332, 343 see also General Index Ceroplastes sinoiae 353 Ceroplastidia 240 Ceroplastinae 3, 149, 151, 185-187, 190, 200, 229,232, 236,239, 240, 244, 248, 249,254 Ceroplastodes 134 Ceroplastodes acaciae 53 Ceroplastodes dugesii 144, 148, 150, 151 Ceroplastodes gowdeyi 20 Ceroplastodes zavattarii 16 Chionaspis pinifoliae 327 Chlamydolecanium 218 Chloropulvinaria floccifera 51, 74, 84, 85, 88, 95, 97, 103, 112, 207, 262 see also General Index Chloropulvinaria psidii 13, 45, 97, 113, 132, 262, 397 see also General Index -
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442
Index Cryptococcus fagisuga 324, 326,339-342 Cryptostigma 126, 132, 145, 147, 149, 156,
Chrysomphalus aonidum 57
citricola scale: see Coccus pseudomagnoliarum Cissococcinae 1 8 6 , 1 9 0 , 230, 232-234, 236-239,244, 248,249 Cissococcus 112, 115, 126, 132, 134, 135, 190, 222, 337, 338 Cissococcusfulleri 112, 244, 325,337, 338 Coccinae 3, 151, 185, 187, 190, 193,254, 255 Coccini 186, 232, 239, 240, 244, 248, 249, 254 Coccites 157 Coccus 92, 98, 99, 101, 105, 107-109, 112, 114, 119, 120, 123, 135, 140, 141, 173, 187, 190, 201,217, 218, 220, 222, 223,225,227, 239, 240, 244, 257-260, 352-355, 357, 358, 360-362, 364, 368, 369 Coccus acutissimus 44
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Coccus aequale 51 Coccus alpinus 280 see also General Index Coccus asiaticus 44 Coccus caviramicolus 366 Coccus celatus 352, 362 see also General Index Coccus circularis 366 Coccus formicarii 355, 357 Coccus-group 28 Coccus hesperidum 4, 8, 19, 25, 44, 51,
78-80, 92, 98, 99, 101, 105, 112, 114, 120, 135, 144, 149-151, 207, 208, 244, 252, 254-256, 258-260, 261, 262, 280, 339, 341, 343,353,354, 357, 358,364, 377, 378,380, 381,382, 384, 398-400, 410-412 see also General Index Coccus longulus 362 see also General Index Coccus macarangae 366 Coccus macarangicolus 366
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Coccus ophiorrhizae 51 Coccus penangensis 366 Coccus pseudohesperidum 51 Coccus pseudomagnoliarum 44, 207, 260, 343,
364 -
see also General Index Coccus secretus 366 Coccus tumuliferus 366 Coccus viridis cover, 270, 280, 284, 326,333,
355,357, 360, 400 -
see also General Index Columnea 185 Comstockiella 4 Conofilippia 123, 222
cottony grape scale: see Pulvinaria vitis cottony maple scale: see Neopulvinaria innumerabilis
cottony vine scale: see Pulvinaria vitis Couturierina 114, 119, 132, 222 Cribrolecanium 121, 132, 369 Cribrolecanium andersoni 10, 280, 327 see also General Index Cryptes 114, 117, 130, 222, 239,240 Cryptes baccatus 44, 53, 63. 147 Cryptinglisia 222, 223 Cryptococcidae 158, 162, 170, 324 Cryptococcus 170 -
239, 240, 272, 368 Cryptostigma biorbiculus 147, 365 Cryptostigma endoeucalyptus 44, 145, 147 Cryptostigma inquilina 132, 147,365 Cryptostigma quinquepori 366 Cryptostigma reticulolaminae 366 Cryptostigma spp. 366 Ctenochiton 113, 118, 141,222, 223 Ctenochiton aztecas 143 Ctenochiton depressus 53 Ctenochiton eucalypti 51 Ctenochiton flavus 51 Ctenochiton piperis ix Ctenochiton setT"atus 53 Ctenochiton spinosus 53 Ctenochiton spp. x, xi Ctenochiton viridis x, 44, 51, 156 Cyclolecanium 115, 126, 130, 132, 220, 368 Cyclolecanium hyperbaterum 147, 148, 366
Cyphococcinae 175, 186, 230, 232, 233, 235-239, 244, 248,249,255 Cyphococcus 113, 121, 135,222 Cyphococcus caesalpiniae 244 Dactylopiidae 162, 170, 173, 175,291, 329 170, 173,200, 201 austrinus 339,341 coccus 201, 291 conjitsus 329 Diaspididae 12, 55-58, 61, 157, 168, 257, 295,323. 327, 332, 339, 353, 376 Diaspidites 157 Dicyphococcus 112, 121, 223 Dicyphococcus bigibbus 112 Didesmococcus 118, 120, 129, 131
Dactylopius Dactylopius Dactylopius Dactylopius
Didesmococcus koreanus 53 Didesmococcus unifasciatus 53 see also General Index Drepanococcus 272 Drepanococcus cajani 44, 53 Drepanococcus chiton 362 Drosicha corpulenta 57, 58, 70 -
Edwallia 220 Ericeroides 127, 222 Ericerus 185, 218 Ericerus pela 44, 53, 55, 57, 58, 66, 91, 92,
104, 113, 208,291,303,305-308, 311,314 -
see also General Index
Eriochiton 175,229-231, 236-240, 244 Eriochiton spinosus 244
Eriochitonini 244, 248, 249 Eriococcidae 10, 13, 145, 158, 162, 168, 170, 173, 175, 176, 178, 181, 185,214, 222, 227, 230, 231, 236-240, 244, 248, 249, 295,296, 323,325,329 Eriococcus 239,244 Eriococcus buxi 244 Eriococcus confusus 326 Etqococcus cotqaceus 281, 323, 328,329,333 Eriococcus sp. 63 Eriokermes 176,229 Eriopeltinae 156, 186, 187, 196, 232, 234, 236-240. 244, 248, 249,255
443
Index to Coccoidea taxa Eriopeltis 112, 118, 124, 139-141, 144, 148. 156, 185,200, 217, 223,239,240, 244 Eriopeltis coloradensis 53 Eriopeltis festucae 7, 16, 44, 53, 144, 244, 255 Eriopeltis lichtensteini 44, 53 Eriopeltis rasinae 112 Eriopeltis stammeri 44, 53 Eriopeltis varleyi 53 Etiennea 123, 134, 222, 227 Etiennea cacao 134 Etiennea ferox 9, 44 Etiennea gouligouli 44 Etiennea multituberculatum 19, 44 Etiennea petasus 44, 95, 97, 98, 151,245 Etiennea sinetuberculum 44 Etiennea villiersi 10, 12, 14, 20, 98 Eucalymnatus 107, 115, 135,220, 227, 348 Eucalymnatus tesseUatus 15, 39, 44, 244, 262 see also General Index Eulecaniinae 149, 151, 186, 190, 193, 230, 232-234, 236-240, 244, 248,249, 254 Eulecanium 51, 53 112, 114, 115, 126, 130, 134, 139-142, 187, 217, 218,223, 225, 239, 240, 244, 344, 348 Eulecanium caraganae 44 Eulecanium caryae 51 see also General Index Eulecanium cerasorum 35, 39, 66, 97 see also General Index Eulecanium ciliatum 44, 51 see also General Index Eulecanium douglasi 207 Eulecanium franconicum 44, 53,208 see also General Index Eulecanium giganteum 5 Eulecanium kunoense 44, 262, 264 see also General Index Eulecanium paucispinosum 208, 209 Eulecanium sericeum 44, 294 see also General Index Eulecanium tiliae 44, 51, 112, 130, 134, 151, 207, 223,244, 254, 262-264, 324, 331,344 see also General Index Eumashona 118 Eumashona msasae 10 Eupulvinaria peregrina 207 European fruit Lecanium: see Parthenolecanium corni European peach scale: see Parthenolecanium persicae Eutaxia 99, 113, 119, 121, 124, 131,220 Exaeretopus 134, 187, 217, 218,223 -
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Gascardia madagascariensis 104, 113 Gossyparia spuria 281
vii, 44, 91, 92,
Hadzibejliaspis 123, 130, 134, 218 Hadzibejliaspis stipae 123 Halococcus 121, 125, 131-133, 135,223, 369 Halococcus formicarii 1 2 1 , 125, 131, 133, 135, 273 Hemilecanium 114, 123, 127, 223 Hemilecanium coriaceum 20 Hemilecanium imbricans 19 Hemilecanium recurvatum 365 hemispherical scale: see Saissetia coffeae Houardia 115, 121, 126, 132, 134, 135,369 Houardia mozambiquensis 10 Houardia troglodytes 7, 15, 16, 44 lcetya aegyptiaca 281 Icelya purchasi 57, 66, 79 Icerya seycheUarum 324, 328-330, 332, 339-342 Idiosaissetia 123, 126,222 lnglisia 126, 130, 140, 223, 239, 240, 244 lnglisia leptospermi xi lnglisia malvacearum 53 Inglisia ornata xi, 53 Inglisia patella 35, 144, 145, 147-149, 151 Inglisia sp. xi lnglisia theobromae 244 Inglisia vitrea cover, ix, 10, 105, 148
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fig wax scale: see Ceroplastes rusci Filippia 121, 124, 126, 149, 151, 185, 218, 239, 240, 244, 272 Filippia foUicularis 44, 149, 151,244, 251 see also General Index Filippiinae 151, 156, 185-187, 196, 230, 232-240, 244, 248, 249, 255 Fiorinia externa 332 Florida wax scale: see Ceroplastes floridensis -
Gascardia 113, 127, 129. 240
Kermes cockerelli 244 Kermes ilicis 62 Ketwzes kingi 178 Kermes quercus 168, 176, 200, 292 Kelvnes sylvestris 244 Kermesidae 3, 157, 158. 162, 168, 170, 173, 175, 176, 178, 181, 230, 231, 235-239, 244, 248,249,294, 295 Kerria 157, 201 Kerria lacca 55, 63 Kerriidae 183 Kilifia 107, 118, 124, 132, 134, 135, 144, 146, 148-151,272 Kilifia acuminata 44, 135, 149 see also General Index Kilifia americana 144, 146, 148-151 Kozaricoccus 118, 222 Kozaricoccus bituberculatus 145 Kuwanina 170 -
Lacciferidae 183 Lagosinia 119, 123, 126 Lagosinia strachani 20, 119 Lagosinia vayssierei 44, 143, 149 Lecaniococcus 218 Lecaniococcus ditispinosus 129 Lecanites 157, 185 Lecanium 185, 187 Lecanium comi var. robiniarum 203 Lecanochiton 115, 126, 128, 130 Lecanochiton minor 51, 128 Lecanodiaspididae 3, 157, 158, 162, 165, 167, 168, 176. 178, 181, 185, 230-232, 235-241, 244, 248. 249
Index
444 Lecanodiaspis 181,239 Lecanodiaspis elytropappi 244 Lecanodiaspis quercus 66 Lecanodiaspis sardoa 244 Lecanopsis 120, 185,217, 218 Lepidosaphes ulmi 206 Leptococcus metroxyli 245 Leptopulvinaria 132, 218 Lichtensia 112, 135,223 Lichtensia vibumi 44, 51, 112, 251 see also General Index Limacoccus 229 long soft scale: see Coccus longulus Luzulaspis 148, 156, 185, 187, 200, 217, 218, 227 Luzulaspis frontalis 44, 47 Luzulaspis grandis 112 Luzulaspis luzulae 45, 51 Luzulaspis scotica 45, 51 -
Maacoccus 118, 130 Maacoccus bicruciatus 51 Maacoccus piperis 51 MaconeUicoccus hirsutus 281 Mallococcus 117-120, 170, 178, 181, 185, 187, 196,200, 239, 240 Mallococcus sinensis 15, 148 Mametia 126,223 Mametia louisieae 5, 17, 19 mango shield scale: see Milviscutulus mangiferae Marchalina heUenica 293,296,297 Margarodidae 295-297, 324, 329, 330 Margarodinae 296 Marsipococcus 223 Marsipococcus marsupialis 45, 51, 135 Matsucoccus 324, 330 Matsucoccus acalyptus 330 Matsucoccus feytaudi 324 Matsucoccus paucicicatrices 324 Matsucoccus resinosae 339 Mediterranean black scale: see Saissetia oleae Megalecanium 220 Megalecanium testudinis 114 Megalocryptes 114 Megapulvinaria 117, 118, 126, 134, 135,272 Megapulvinaria maskeUi 118, 331 Megapulvinaria maxima 51, 117, 272 see also General Index Melanesicoccus kleinhoviae 134 Melanesicoccus myrmecariae 13, 16, 129 Melanococcus 272 Membranaria 123,222 Mesembryna 222 Mesembryna fasciata 134 Mesolecanium 115,223 Mesolecanium nigrofasciatum 51, 53, 141 see also General Index Mesolecanium nocturnum 146 Messinea 112, 113, 130, 223 Messinea conica 13, 97, 103, 130, 244 Messinea loisa 112 Metaceronema 118, 121,222, 223 Metapulvinaria 223 Mexican black scale: see Saissetia miranda -
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Micrococcidae 158, 162, 165, 167, 168, 181, 183,200, 229-238, 241,244, 248,249 Micrococcus 181,200 Micrococcus bodenheimeri 244 Millericoccus 220 Milviscutulus 114, 124, 149, 151,222, 272 Milviscutulus mangiferae x, 39, 45, 51, 149, 151,358, 362, 379 see also General Index Mitrococcus 218 Mitrococcus celsus 112 MoUuscococcus 181 Monophlebinae 296 Myzolecaniinae 149, 156, 186, 190, 196, 232-234, 236-241, 244, 248, 249, 254, 272, 273 Myzolecanium 115, 120, 121, 126, 130, 223, 239,240, 244, 369 Myzolecanium kibarae 365,244 Myzolecanium spp. 365 -
Nemolecanium 218 Nemolecanium abietis 53 Neococcoidea 3 Neolecanium 23, 187, 218 Neolecanium comuparvum 19, 45, 51, 139, 149,244 see also General Index Neolecanium silveirai 15, 16, 19, 45 Neolecanochiton 132, 220 Neoplatylecanium 127, 128, 134, 223 Neoplatylecanium cinnamomi 134 Neopulvinaria 223 Neopulvinaria innumerabilis 45, 51,262, 263, 294, 344 see also General Index Neosaissetia 223 Newsteadia floccosa 181 Nt'dularia 185 nigra scale: see Parasaissetia nigra Nuculaspis tsugae 332 -
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Orthezia 157 Orthezia insignis 281 Orthezites 157 Palaeolecanium 114, 120 Palaeolecanium bituberculatum 51,348, 350 see also General Index Paracardiococcus l l4, 127, 129, 135,222 Paracardiococcus actinodaphnis 114 Paracerostegia 240 Paractenochiton 222, 272 Paractenochiton sutepensis 133 Parafairmairia 114, 145, 156, 187, 198, 218, 223 Parafairmairia bipartita 45 Parafairmairia gracilis 45, 156,348 Paralecaniini 186, 232, 234-239, 245, 248, 249,254 Paralecanium 51, 53, ll7, 130, 222, 223 Paralecanium carolinensis 8 Paralecanium expansum 45, 51 Paralecanium frenchii 245 Paralecanium geometricum 51 -
445
Index to Coccoidea taxa Paralecanium macrozamiae 245 Paralecanium marginatum 45, 51 Paralecanium maritimum 5 l, 245 Paralecanium peradeniyense 51 Paralecanium planum 45, 5 l Paralecanium zonatum 51 Paralecanopsis l l6, 120, 129, 133-135 Paralecanopsis formicarum 144-149, 156 Paralecanopsis turcica 45, 120, 129, 133, 135, 145 Parapulvinaria 220 Parasaissetia 115 Parasaissetia nigra 4, 8, 20, 45, 5 l, 149, 262, 264, 281,358, 384, 400 see also General Index Parthenolecanium 98, 107, l 1l, l l8, 124, 218, 223,227, 257, 344, 345,348 Parthenolecanium cerasifex 45,262, 264 Parthenolecanium corni 20, 45, 51, 64, l l l, 124, 144, 203,208,223,245,253,254, 262, 263,266,281,292, 294, 297, 298,344, 345 see also General Index Parthenolecanium fletchel~ 45, 292, 297 see also General Index Parthenolecanium persicae 20, 45, 98, 207, 262 see also General Index Parthenolecanium pomeranicum 45, 5 l, 73, 84, 86 Parthenolecanium putmani 262, 264 Parthenolecanium quercifex 51, 144, 145, 148 see also General index Parthenolecanium rufulum 45, 76, 77, 292, 298 see also General Index pela scale: see Ericerus pela Pendularia 121, 126, 127 Perilecanium 114, 123, 124, 129, 135 Phenacoccus pergandei 64 Phenacoleachiidae 178 Philephedra 123, 140-142, 187, 223 Philephedra crescentiae 53 Philephedra ephedrae 147 Philephedra floridana 281 Philephedra lutea 51 Philephedra tuberculosa 53, 281, 400, 405, 415 see also General Index Philippia 185 PhyUostroma 134, 218,239, 240 PhyUostroma myrtilli 45, 53,292 Physokermes 114, 115, 121, 122, 124, 125, 130, 157, 185,215,223,254, 272, 273,344, 348 Physokermes hemicryphus 45, 122, 130, 147, 149,291,292, 294, 344 see also General Index Physokermes piceae 45, 51,223,262, 292 see also general Index Planococcus citri 79, 281 Planococcus kenyae 280 Platinglisia 114, 130, 132, 134, 220 Platinglisia noacki 114 Platylecanium 130, 135 Platylecanium asymmetricum 53 Platylecanium cribrigerum 135 -
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Platysaissetia ferina 20 Poaspis 114, 130, 131, 134 Poaspis jahandiezi 13, 114, 130 Podoparalecanium 114, 130, 135,222 Podoparalecanium machili 114 Pollinia 157 Porphyrophora crithmi 87 Protopulvinaria 114, 140-142, 144, 145, 149, 151, 187, 272 Protopulvinaria pyriformis x, 32, 34, 37, 39, 41, 45, 144, 145, 149, 151, 245, 280, 376, 377, 378,380, 382, 384, 400 see also General Index Pseudalichtensia 198,220 Pseudaulacaspis 258 Pseudaulacaspis pentagona 57, 66, 332 Pseudococcidae 10, 12, 55, 158, 162, 168, 173, 175, 176, 178, 181, 222, 229-231,233, 245, 248, 249, 295, 296, 323,368 Pseudococcus aj~inis: see Pseudococcus viburni Pseudococcus comstocki 55, 57, 63 Pseudococcus longispinus 87, 245,405 Pseudococcus viburni 245,405 Pseudokermes 132, 134, 223 Pseudokelvnes nitens 134, 144, 151 Pseudophilippia 23, 121, 123, 187, 201, 218 PsetMophilippia quaintancii 13, 19, 32, 33, 36, 38, 40, 42, 43, 45, 53, 100, 144-146, 149,244 see also General Index Pseudopulvinaria 114, 120, 124, 125, 127, 129, 130, 132, 223,239, 240, 245,272 Pseudopulvinaria sikkimensis 13, 39, 42, 45, 198,245 Pseudopulvinariinae 186, 187, 196, 230, 232-234, 236-240, 245,248, 249 Psilococcus 116, 129, 218, 273 Psilococcus ruber 45 Pulvinaria 95, 97, 99, 102-105, 107-109, 141, 185, 187, 203, 204, 207-211, 217, 218, 222, 223, 225, 227, 239, 240, 245, 254-259, 270, 273, 344, 348 Pulvinaria acericola 51,245 see also General Index Pulvinaria aurantii 51 see also General Index Pulvinaria bigeloviae 53 Pulvinaria crassispina 208, 209 Pulvinaria delottoi 45 Pulvinaria dodonaeae 123 Pulvinaria ericicola 53, 105 see also General index Pulvinaria flavescens 45 Pulvinaria horii 45, 56 Pulvinariahydrangeae 45, 53 see also General Index Pulvinaria mesembryanthemi: see Pulvinariella mesembtyanthemi Pulvinaria pistaciae 294, 299 Pulvinatqa regalis 82, 95, 102-104, 131, 329, 331,400 see also General Index Pulvinaria rhois 120 Pulvinaria salicicola 45, 48 Pulvinaria sp. 400 Pulvinaria tessellata 51 -
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446
Index Pulvinaria urbicola 384, 400 see also General Index Pulvinaria vitis 45, 51, 203, 204, 207, 208, 223,227, 245,258, 259, 262, 265,270, 273, 344 see also General Index Pulvinariella mesembryanthemi 45, 51, 83, 254, 262, 263,328, 339, 340, 345,353,358, 401 see also General Index Pulvinariini 186, 232, 237, 239, 240, 245, 248, 249,255 Pulvinarisca 113, 126, 127, 134, 135, 218, 272 Pulvinarisca serpentina 5, 113 Pulvinella 220 Puto 158, 200, 229 pyriform scale: see Protopulvinar~a pyrifot~zis
Signoretia 185 Sphaerolecanium 132, 140-142, 151, 218,344, 348 Sphaerolecanium prunastri 46, 53, 252, 257, 262-264, 344 see also General Index Steingelia gorodetskia 134 stellate scale: see Vinsonia stellifera Stenolecanium esakii 129 Stictococcidae 230, 231, 233-238, 245, 248, 249 Stictolecanium 113, 118, 121, 130, 131,220 Stictolecanium intermedius 245 Stictolecanium ornatum 16, 19 Stictolecanium pujoli 245 Stictolecanium sjostedi 245 Stotzia 127, 215,218,223 Suareziella 130, 223 Symonicoccus 222, 227
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Quadraspidiotus 258 Rastrococcus invadens 281 red wax scale: see Ceroplastes rubens Rhizopulvinaria 218, 225,348 Rhizopulvinariaarenaria 46, 51 Rhizopulvinaria armeniaca 51, 112 Rhizopulvinaria artemisiae 46, 51 Rhizopulvinaria grassei 46 Rhizopulvinaria maritima 46 Rhizopulvinaria saxatilis 46 Rhodesaclerda 158 Rhodococcus 51, 125, 218 255,273 Rhodococcus rosaeluteae 51 Rhodococcusspiraeae 46, 51 Rhodococcus turanicus 46 see also General Index Richardiella 118, 127, 222 Richardiella taiensis 11, 16 -
Saccharipulvinaria icetyi 274 see also General Index Saccharolecanium 117, 118, 129, 133, 136 Saccharolecanium krugeri 133 Saissetia 92, 95, 97, 103, 105, 107, 112, 119, 123, 125, 131, 187, 217, 220, 222, 223,225, 239,240, 245,257, 258, 270, 272, 326,344, 348 Saissetia coffeae x, 7, 46, 51, 92, 103, 105, 112, 131,207, 208, 245,262, 281,355,377, 379, 380, 382, 384, 401,414 see also General Index Saissetia miranda 359, 362 see also General index Saissetia oleae 4, 7, 46, 51, 95, 97, 258, 262, 263,339, 344, 359,376,377,379,384, 401, 405,406, 408 see also General Index Saissetia privigna 401 Saissetia zanzibarensis 270, 353,359 Saissetiini 151, 186, 232, 234, 236-240, 245, 248, 249,254 Schizochlamidia 130, 135 Scythia 112, 126, 130, 218 Scythia craniumequinum 46 Scythia festucae 112 Scythiafestuceti 46, 53 -
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Tachardia aurantiaca 245 Tachardia fici 183,245 Tachardia karroo 245 Tachardiidae 55, 56, 58, 61, 157, 158, 162, 167, 168, 183, 201, 230-239,241, 245, 248, 249,291 Tachardina theae 58, 71 Taiwansaissetia 222 Takahashia 218 Takahashia japonica 5, 7, 46 Tectopulvinaria 119, 121 Tectopulvinaria loranthi 148 tessellated scale: see Eucalymnatus tessellatus lillancoccus 118, 130 Torarchus endocanthium 365 Toumeyella 5, 7, 10, 13, 32, 33, 35, 46, 139-142, 144, 145, 147-151, 187, 196, 215, 218, 229,239,240, 260, 324, 327, 328, 332, 347, 348,359, 360, 361,401 ToumeyeUa cerifera 13, 46, 53, 100, 112, 142 Toumeyella cubensis 46 ToumeyeUa-group 23 Toumeyella lignumvitae vii ToumeyeUa lirioderwlri x, 7, 46, 51, 139, 260, 324, 359,361 see also General Index ToumeyeUa mirabilis 46, 53, 144, 148 ToumeyeUa nectandrae 46 ToumeyeUa parvicornis 33, 35, 46, 53, 145, 147, 148,332, 339, 341,347, 359 see also General Index Toumeyella pini 46, 51, 99 see also General Index Toumeyella pinicola 53, 112, 254, 260 Toumeyella quadrifasciata 46 Toumeyella sonorensis 46, 150, 151, 156 Toumeyella sp. 329,359 Toumeyella virginiana 46, 53 Trijuba 118, 130, 131,223 tuliptree scale: see Toumeyella liriodendri -
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Udinia 118, 124, 125, 127, 272 Udinia newsteadi 365 Ultracoelostoma assimile 295,297, 324 Ultracoelostoma brittini 281 Umwinsia 114, 115, 118, 131
447
Index to Coccoidea taxa Unaspis euonymi 66, 327, 328 Unaspis yannoensis 56
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Vinsonia 39, 46, 185,240 Vinsonia stellifera 5, 46, 53, 148, 151 see also General Index Vitrococcus conchiformis 15, 124 Vittacoccus 114, 120, 132, 218 Vittacoccus longicornis 114
Waricoccus 123, 136, 222, 227 wax scales 3 Wctriella 127, 223,227, 240 Waxiella afn'cana 46 Waxiella zonata 113 Xenolecanium 126, 129, 223 Xylococcinae 296 Xylococculus macrocarpae 296 Xylococcus macrocarpi 294, 297
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449
Index to Names of Parasitoids, Predators and Pathogens Anagyrus fusciventris 405 Anagyrus pseudococci 410 Anicetus beneficus 60 Anthribus lajievorus 308 Aphelinidae 381 - see also General Index Aphytis melinus 61 Aphytis yanonensis 61, 72 Apoanagyrus diversicomis 383 bagworm moths 307, 309
Bathyplectes curculionis 376,381 Braconidae 376, 383 brown lacewing: see Hemerobiidae
Habrolepis rouxi 383 Hemerobiidae 405,410 Hyphomycetes 263 Ichneumonidae 376
lacewings, s e e Neuroptera Leptomastidea abnormis 405, 410 Leptomastix dactylopii 405
Metaphycus helvolus 377, 380, 381,406, 409 Metaphycus lounsburyi 347, 406 Metaphycus luteolus 398 Metaphycus stanleyi 376 Metaphycus swirskii 376,380, 381,398 Metaseiulus longispinus 405 Microterys ericeri 308
Cardiochiles nigriceps 383 Chilocorus kuwanae 309 Chilocorus rubidus 321 Coccophagus hawaiensis 415 Coccophagus rusti 347 ComperieUa bifasciata 376,382 Cryptolaemus montrouzieri 397, 405 Cryptothelea minuscula 309 Cryptothelea variegata 307 Cybocephalus gibbulus 398
Phytoseiulus longipes 405 Phytoseiulus persimilis 405
Cynipidae 383
predatory mites 405
Encyrtidae 376, 381,383 - see also General Index Encyrtus infelix 380, 381 Encyrtus lecaniorum 379 Encyrtus swederi 208 Eulophidae 383 - see also General Index
Galandromus longispinus 405 Gloesporium 309
Neuroptera 405
Parus major 309 Phoenicrurus auroreus 309 Phytoseiidae 405
Pseudeucoila bochei 383 Pycnonotus sinensis 309 ScuteUista caerulea 347 Scutellista cyanea, see Scutellista caerulea Sympherobius sanctus 405, 410 Tetrastichus 308 Tetrastichus ceroplastae 380, 383,384 weevils 307
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451
Index to Plant Names Abies 279 Abies alba 294 Abies cephalonica 294 Acacia 368 Acer negundo 205,206 Acer pseudoplatanus 329, 400 Aesculus hippocastanum 329, 400 Albizia 366 Alnus 207 Amorpha 206 Anacardiaceae 308 Aphania senegalensis 12, 14 Aphanomixis 365 Aquifoliaceae 308 Artemisia 215 Arundo donax 294 Asplenium nidus 399, 414 Atriplex vesicaria 331 Avicennia marina 330, 332 avocado: see Persea americana Barteria 365 Basella alba 403, 412 Betula 207 Blechnum fraseri xi Caesalpiniaceae 369 Calluna vulgaris 208 Calocedrus decurrens 294 Canthium ix, 365 Caragana 205,206 Caragana arborescens 206 Carduus pycnocephalus 347 Carica papaya 400, 415 Carissa grandiflora 414 Carlina corymbosa 347 Carpobrotus edulis 341,358,400 Carya illinoensis 279,327 Caryophillaceae 218 Castanea sativa 292 Cecropia 366,368, 369 Celastraceae 308 Celastrus ceriferus 308 Celtis 346 Chionanthus retusa 308 Cissus 325 Cissus cuneifolia 3337 citron melon 378 CitruUus 358 Citrus 327, 330, 332, 339,340, 344, 345,378, 380, 398-401,405,406, 408-411,413,414 Citrus aurantifolia 285 Citrus aurantium 414 Citrus limon 400 Citrus medica 400, 411 Citrus paradisi 327, 400 Citrus sinensis 284, 347, 400 Cleistanthus polystachyus 18 Clematis vitalba 401
Coccoloba uvifera viii Coffea canephora 362 coffee: see Coffea spp. Cordia 365,366, 368 Corylus 205 Corylus avellana 294 Cotoneaster 205 Crataegus 205,207, 294 Crypteronia 366, 369 Crypteroniaceae 369 Cucurbita maxima 401 Cucurbita moschata 399-401,403,411-414 Cupaniopsis 365 Cyperaceae 215 Cyphomandra betacea 284 Dacrydium 279 Dacryodes edulis 16 Dianthus 215 Dieffenbachia 399 Diospyros 205,206 Diospyros kaki 206 Duroia 366 Elaeis guineensis 16 Ephedra 215,218 Erica 215 Eriobotrya japonica 280 Eryngium campestre 347 Erythrina 358,362 Eucalyptus 323,326, 327, 329 Eucalyptus blakelyi 327, 329 Eucalyptus deglupta 358,362 Eugenia caryophyUata 17 Eugenia jaboticaba 16 Euonymus fortunei 327, 328 Euphorbia pyrifolia 324, 328, 330 Euphorbiaceae 369 Fagus 324 Fatsia japonica 382, 400 Ficus benjamima 411 Ficus carica 294 fig: see Ficus carica Fraxinus 205,208, 324, 331 Fraxinus americana 308 Fraxinus chinensis 307, 315 Fraxinus excelsior 292 Gardenia augusta 400 Gilbertiodendron splendidum 11 Gleditsia 204-206 Gliricidia sepium 362 grapevine: see Vitis vinifera Guaiacum sanctum 327-329, 401 guava: see Psidium guajava Hakea 351 Hedera helix 382, 383,399, 400, 414 Hedycarya arborea xi
Index to plant names
452
Hibiscus syriacus 308 llex 308 Jambosa caryophyllus 359 Juniperus 279 Kibara 365 Kunzea ericoides xJ Laurus nobilis 414 Lecanopteris 366 l.z'gustrum 208 Ligustrum acutissimum 308 Ligustrum lucidum 307 Liriodendron tulipifera 324, 331,358 Macaranga 366, 368, 369 Maclura 205,206 Magnoliaceae 215 Malus 205 Malvaceae 308 Mangifera indica 284, 379 mango: see Mangifera indica Mimosa bracaatinga 295,297 Morus 205,206 Morus alba 332 Myoporum laetum 414 Myristica 365 Myrtus communis 399, 414 Nectria coccinea 326 Nerium oleander 346,378, 399, 401,406 Nothofagus 280, 295 Nothofagus solandri 297, 324 Ochna pulchra 358 oleander: see Nerium oleander Olea europaea 344, 346, 347 olive: see Olea europaea Opuntia 329 Opuntia aurantiaca 339 Opuntia cacti 62 peach: see Persea americana Persea americana 346, 379, 383 Persica 205,206 Persica vulgaris 205 persimmon: see Diospyros kaki Picea abies 291,292, 297 Piceae 215,223 Pinaceae 218 P1"nus 215 lh'nus banksiana 298,332, 347, 359 Pinus edulis 330 Pinus halepensis 293,297 Pinus lambertiana 324 Ptnus pinaster 324 Pinus sylvestris 327 pistachio: see lh'stacia Pistacia 294, 299 Pittosporum undulatum 346 Pluchea indica 284, 3 2 6 , 3 3 3 , 3 5 5 , 3 5 7 plum: see Prunus Poaceae 215 Podocarpus viii, 279 Poncirus trifoliata 347
Populus 207 potato: see Solanum tuberosum Prunus 203-207, 346 Prunus domestica 297 Prunus persica 346 Prunus spinosa 206 Psidium guajava 358,362 Psydrax 365 Quercus Quercus Quercus Quercus Quercus
coccifera 62 petraea 292 roboris 292 robur 292 virginiana 294
Raphanus sativus 297 Raphiolepsis umbellata 414 Rhus succedanea 308 Ribes 205,207 Robinia 203-206 Robinia pseudacacia 206,292, 346 Rosa 205 Rosaceae 218 Rubus 205 Rubus fruticosus 346 Salix 207 Sambucus 279 Sapium 366 Saraca 366,369 Sarothamnus 207 Scaevola taccada 328-330 Schefllera arboricola 383 Solanum tuberosum 378,379, 382, 400, 401 Sophora 206 Sorbus 207 Spiraea 204, 207 Steganthera 365 sweet lime 378,384 Syringa josikaea 308 Syzygium aromaticum 326 Taxus 279 Terminalia sericea 358 Thespesia populnea 362 Thuja occidentalis 292, 297 7ilia 275 1ilia cordata 329, 400 Trichilia emetica 401 Triplaris 365 Triticum aestivum 325 Tsuga 332 tuliptree: see Liriodendron tulipifera
Uhnus 205,275,281 Ulmus glabra 292 Vaccinium myrtiUus 292 Vaccinium uliginosum 208 Verbenaceae 308 Vitaceae 337 Vitex 308 Vitex lucens xi Vitis vinifera 204 Xylopia 9
