THE AMERICAN COCKROACH

THE AMERICAN COCKROACH

edited by

William). Bell Professor o/Entomology and Physiology & Cell Biology University o/Kansas and

K. G. Adiyodi Professor o/Reproductt've Physiology and Director, Vatsyayana Centre 0/ Invertebrate Reproduction Calicut University

LONDON NEW YORK CHAPMAN AND HALL

First published 1982 by Chapman and Hall Ltd

11 New Fetter Lane, London EC4P 4EE Published in the USA by

Chapman and Hall in association with Methuen, Inc.

733 Third Avenue, New York NY 10017

© 1981 Chapman and Hall Softcover reprint of the hardcover 1st edition 1981

Typeset in Great Britain by Scarborough Typesetting Services and printed at The University Press, Cambridge

ISBN-13: 978-94-009-5829-6 e-ISBN-13: 978-94-009-5827-2 DOl: 10.1007/978-94-009-5827-2

All rights reserved. No part of this book may be reprinted, or reproduced or utilized in any form or by any electronic, mechanical

or other means, now known or hereafter invented, including photocopying and recording, or in any information storage and retrieval system,

without permission in writing from the publisher.

British Library Cataloguing in Publication Data

The American cockroach.

1. Cockroaches 1. Belt, William J. II. Adiyodi, K. G. 595.7'22 QL505.6

Contents

Contributors xv Preface XVll

1. INTRODUCTION 1 Louis M. Roth

1.1 Distribution 1 1.2 Life cycle 2 1.3 Ecology 3 1.4 Biotic associations and medical importance 7 1.5 Economic and biological importance 13

2. INTEGUMENT 15 Richard R. Mills

2.1 Introduction 15 2.2 Structure of the integument 15

2.2.1 Macromolecular structure 16 2.2.2 Chemical composition of the cuticle 18 2.3.3 Supermolecular structure of the cuticle 19

2.3 Integument during ecdysis 20 2.3.1 Post-ecdysial changes in the cuticle 24 2.3.2 Bursicon-mediated control of cuticle sclerotization 26 2.3.3 Accumulative control mechanisms associated with ecdysis 29

2.4 Stabilization of the ootheca 29

3. CIRCULATORY SYSTEM 33 P. Michael Fox

3.1 Introduction 33 3.2 Heart and circulation 33 3.3 Haemolymph volume 36 3.4 Haemocytes 38

VI Contents

3.5 Constituents of haemolymph 40 3.5.1 Ionic composition 40 3.5.2 Haemolymph sugars: trehalose and glucose 41 3.5.3 Haemolymph lipids 44 3.5.4 Haemolymph proteins 46

4. NUTRITION AND DIGESTION 57 D. E. Bt"gnell

4.1 Introduction 57 4.2 Morphology of the alimentary canal and salivary glands 57

4.2.1 General organization 57 4.2.2 Microscopy 60 4.2.3 The peritrophic membrane 66 4.2.4 Innervation 67

4.3 Nutrition 70 4.3.1 Natural and synthetic diets 71 4.3.2 Specific requirements 72 4.3.3 Long-term regulation of intake 74

4.4 Enzymology 75 4.4.1 pH and redox potentials 75 4.4.2 Digestive enzymes 76 4.4.3 Control of secretion 78

4.5 Physiology of digestion 80 4.5.1 Gut movements 80 4.5.2 Absorption of inorganic ions and water 82 4.5.3 Absorption of organic materials 84

4.6 Microbiology and pathology of the gut 86

5. RESPIRATION 87 P. L. Miller

5.1 Introduction 87 5.2 Rates of gaseous exchange 87 5.3 Morphology of the tracheal system 88

5.3.1 The tracheal plan 88 5.3.2 Fine structure 94 5.3.3 Non-respiratory functions of the tracheal system 94 5.3.4 Spiracle structure 94 5.3.5 Spiracle innervation 97

5.4 Spiracle activity 100 5.4.1 Independent spiracle action 101 5.4.2 Segmental control 101 5.4.3 Intersegmental control 102

5.5 Ventilation mechanisms 102 5.5.1 The organization of pumping movements 102

5.6

6.

6.1

6.2

6.3

6.4

6.5

6.6

7.

7.1 7.2 7.3

Contents vii

5.5.2 Ventilation in quiescent insects 5.5.3 Ventilation in active and in stressed insects 5.5.4 Auxiliary ventilation and autoventilation 5.5.5 Spiracle activity coupled to ventilation 5.5.6 Non-respiratory functions of spiracle coupling 5.5.7 The origin and control of the ventilatory rhythm 5.5.8 Sensory co-ordination of ventilation Diffusive-convective gas exchange in quiescent insects 5.6.1 Saturniidpupae 5.6.2 Periplaneta americana 5.6.3 The endogenous patterning of intermittent ventilation 5.6.4 One-muscle spiracles and diffusive-convective gas

exchange

OSMOREGULATION AND EXCRETION Donald E. Mullt'ns Introduction 6.1.1 General comments and reference to previous treat­

ments of osmoregulation and excretion in cockroaches and other insects

6. 1.2 Basic concepts in osmoregulation and excretion Water relations 6.2.1 Water content 6.2.2 Water loss 6.2.3 Tolerance to stress Components of water and ion metabolism 6.3.1 Sources 6.3.2 Pools and structures involved in osmoregulation and

excretion Excretory products 6.4.1 Nitrogenous excretory products 6.4.2 Miscellaneous materials Regulation and kinetics of osmoregulation 6.5.1 Regulation of ionic composition 6.5.2 Hormonal influences and kinetics of ion transport 6.5.3 Energetics of excretion Conclusions

FAT BODY AND METABOLISM Roger G. H. Downer Introduction Morphology Histology and ultrastructure 7.3.1 Trophocytes

102 103 105 105 107 109 111 112 112 112 115

116

117

117

117 118 119 119 121 122 126 126

127 137 137 140 141 141 143 147 148

151

151 151 152 153

V111 Contents

7.3.2 Urate cells 153 7.3.3 Mycetocytes 153

7.4 Bacteroids 155 7.4.1 General description 155 7.4.2 Functional significance 156 7.4.3 Culture of bacteroids 158

7.5 Composition of fat body 158 7.5.1 Organic constituents 158 7.5.2 Inorganic constituents 161

7.6 Intermediary metabolism 162 7.6.1 Synthesis of glycogen and trehalose 162 7.6.2 Gluconeogenesis 163 7.6.3 Synthesis of lipids 163 7.6.4 Protein synthesis 165 7.6.5 Uric acid metabolism 166 7.6.6 Amino acid metabolism 167 7.6.7 Glycogenolysis 167 7.6.8 Glycolysis and the pentose cycle 168 7.6.9 Tricarboxylic acid cycle 169 7.6.10 Respiratory chain and oxidative phosphorylation 169 7.6.11 Lipolysis 169 7.6.12 Cyclic nucleotide metabolism 170 7.6. 13 Other metabolic activities 171 7.6.14 Physiological factors influencing fat body metabolism 172

7.7 Conclusions 173

8. NERVOUS SYSTEM 175 Rudolph Pipa and Fred Delcomyn

8.1 Introduction 175 8.2 Structural organization of central and peripheral pathways 175

8.2.1 General anatomical features 176 8.2.2 The brain (supraoesophageal ganglion) 177 8.2.3 Stomodaeal nervous system (SNS) 186 8.2.4 Retrocerebral neuro-endocrine complex (RNC) 187 8.2.5 Ventral nerve cord (VNC) 188

8.3 The extraneuronal compartment 196 8.3.1 Structural components 196 8.3.2 Ionic balance and the 'blood-brain' barrier 198

8.4 Electrophysiology 199 8.4.1 Cable properties and resting potential 199 8.4.2 Active properties and action potential 200 8.4.3 Excitability 200

8.5 Synaptic transmission 202 8.5.1 Electrical and chemical transmission 202

8.5 .2 Graded transmission 8.5.3 Transmitter substances

8.6 Toxicology 8.6.1 The effects of insecticides on the nervous system 8.6.2 Autotoxicity

8.7 Functional organization 8.7.1 Reflexes and their central control 8.7.2 Intersegmental co-ordination 8.7.3 The giant fibre system 8.7.4 Neural basis of rhythmic behaviour

8.8 Learning

9. SENSE ORGANS Gunter Seelinger and Thomas R. Tobin

9.1 Introduction 9.2 Visual system

9.2.1 Strucmre of the compound eye 9.2.2 Light-dark adaptation and visual acuity 9.2.3 Colour vision and polarized light sensitivity 9.2.4 Central projections: the lamina ganglionaris 9.2.5 Ocelli

9.3 Mechanoreceptive sensory systems 9.3. 1 Cereal thread hair system 9.3.2 Proprioreceptors of the leg 9.3.3 Subgenualorgans

9.4 Antennal sensory system 9.4.1 Strucmre and classification of antennal sensilla 9.4.2 Olfaction 9.4.3 Pheromone reception 9.4.4 Thermoreception 9.4.5 Hygroreception

9.5 Chemoreceptors on the maxillary palpus 9.6 Conclusions

10. RHYTHMS Donald J. Sutherland

10.1 Concepts and terminology 10.2 Circadian rhythms of individuals

10.2.1 Locomotion 10.2.2 Feeding 10.2.3 Drinking 10.2.4 Susceptibility to chemical agents

10.3 Circadian rhythms of populations

Contents ix

203 203 205 206 208 208 208 209 210 212 214

217

217 219 219 220 221 222 223 223 223 227 233 234 234 240 242 243 244 244 244

247

247 248 248 260 263 264 266

x Contents

10.4 Circadian rhythms of physiological systems 267 10.4.1 Respiration 267 10.4.2 Circulation 268 10.4.3 Digestion 269 10.4.4 Integument 269 10.4.5 Endocrine 270 10.4.6 Nerve and muscle 270 10.4.7 Reproduction 271

10.5 Location of photoreceptors and circadian pacemakers 272 10.6 Rhythms other than circadian 273 10.7 Conclusions 273

11. MUSCLES AND MUSCULAR ACTIVITY 275 Fred Delcomyn

11.1 Introduction 275 11.2 Organization and innervation 275

11.2.1 Gross structure and innervation 276 11.2.2 Fine structure 279 11.2.3 Neuromuscular junctions 284

11.3 Biochemistry 284 11.4 Electrophysiology 287

11.4.1 Ionic basis of electrical responses 287 11.4.2 Electrical properties 288 11.4.3 Electrical responses to neural stimulation 290

11.5 Neuromuscular transmission and its chemical basis 293 11.5.1 Transmission at excitatory neuromuscular junctions 294 11.5.2 Transmission at inhibitory junctions 296 11.5.3 Transmission in visceral muscles 296 11.5.4 Octopamine and neuromodulation 297 11.5.5 Effects of toxins 298

11.6 Mechanical properties 298 11.6.1 Skeletal muscle 298 11.6.2 Visceral muscle 300

11.7 Functional use of muscle 301 11.7.1 Muscle activity during walking 301 11. 7.2 Muscle activity and muscle properties 302

12. NEUROSECRETIONS AND HORMONES 305 Stephen S. Tobe and Barbara Stay

12.1 Introduction 305 12.2 Neurosecretory cells (NSC) 305

12.2.1 Brain 306 12.2.2 Biogenic amines in the brain 309 12.2.3 Functions of the neurosecretory cells of the brain 310

Contents Xl

12.2.4 Control of NSC of brain 311 12.2.5 Suboesophageal and ventral ganglia; Perisympathetic

organs; other NSC terminals 313 12.3 Corpora cardiaca (CC) 315

12.3.1 General structure 315 12.3.2 Morphology and ultrastructure of the CC 315 12.3.3 Neurohormones of the CC 319

12.4 Neurohormones of the ventral nerve cord 322 12.4.1 Proctolin and hindgut-stimulating neurohormones 322 12.4.2 Bursicon 324 12.4.3 Antidiuretic hormone 325

12.5 Corpora allata (CA) 325 12.5.1 Fine structure of the CA 325 12.5.2 Innervation 327 12.5.3 Juvenile hormones 328 12.5.4 Regulation of the CA 333 12.5.5 Regulation of JH titre 334 12.5.6 Actions ofJH 336

12.6 Prothoracic glands (PG) 336 12.6.1 Tracheation and innervation 337 12.6.2 Fine structure 337 12.6.3 Growth and regression of the PG 338 12.6.4 Control of regression of the PG in adult 338 12.6.5 Function of the PG 339 12.6.6 Cyclic activity of PG 339 12.6.7 Actions of ecdysone 339 12.6.8 Titres of ecdysteroids 339 12.6.9 Alternate sources of moulting hormone 340 12.6.10 Activation of the PG 341

12.7 Ovary as an endocrine organ 341

13. REPRODUCTION 343 William J. Bell and K. G. Adiyodi

13.1 Introduction 343 13.2 Female reproductive system 343

13.2.1 Morphology of the ovary 343 13.2.2 Oogenesis and vitellogenesis 346 13.2.3 Oocyte resorption 356 13.2.4 Transmission of bacteroids 356 13.2.5 Ovulation and oviposition 357

13.3 Male reproductive system 357 13.3.1 Morphology of the testis and sperm ducts 358 13.3.2 Spermatogenesis 360 13.3.3 Sperm storage 362

XlI Contents

13.3.4 Sperm motility 364 13.3.5 Accessory sex glands and their functions 365 13.3.6 Mechanisms controlling sexual maturation and

reproduction in the male 369

14. PHEROMONES AND BEHAVIOUR 371 William]. Bell

14.1 Introduction 371 14.2 Orientation 371

14.2.1 Positional orientation 371 14.2.2 Object orientation 372

14.3 Courtship 385 14.3.1 Analysis of counship behaviour 385 14.3.2 Bioassay of female sex pheromone 387

14.4 Agonism 390 14.5 Aggregation 394 14.6 Learning 395 14.7 Conclusion 397

15. EMBRYONIC AND POST-EMBRYONIC DEVELOPMENT 399 Robert R. Provine

15.1 Introduction 399 15.2 Embryogenesis 399

15.2.1 Determination and regulation 401 15.2.2 Induction 402

15.3 The ootheca 403 15.4 Culture of intact embryos ex-ovo 408 15.5 Embryonic behaviour development 409 15.6 Eclosion and hatching 411 15.7 Tissue culture of the embryonic nervous system 415 15.8 Conclusion 422

16. REGENERATION 425 J. G. Kunkel

16.1 Introduction 425 16.2 Tissues with regenerative potential 426

16.2.1 Epidermal structures 426 16.2.2 Internal tissues 426 16.2.3 Regenerative fields 427

16.3 Phenomenology of limb regeneration 427 16.3.1 Faithfulness of regeneration 427 16.3.2 Moulting delay 430 16.3.3 Synchronization of moulting 432 16.3.4 The regenerative process 433

16.4 Regulation of regeneration 16.4.1 Role of nerves 16.4.2 Role of hormones

16.5 Unified model 16.5.1 Systems involved 16.5.2 Interactions of the systems

16.6 Conclusion

References Species Index Subject Index

Contents XUl

439 439 440 441 441 441 443

445 523 525

Contributors

K. G. Adiyodi, Department of Zoology and Vatsyayana Centre of Invertebrate Reproduction, Calicut University, PO Kerala 673635, India.

William J. Bell, Department of Entomology and Department of Physiology and Cell Biology, University of Kansas, Lawrence, Kansas 66045, USA.

D. E. Bignell,· University of Exeter, Department of Biological Sciences, Devon EX44PS, UK.

Fred Delcomyn, Department of Entomology and Program in Neural and Behavioral Biology, University of Illinois, Urbana, Illinois 61801, USA.

Roger G. H. Downer, Department of Biology, University of Waterloo, Waterloo, Ontario N2L 3GL, Canada.

P. Michael Fox, Department of Biological Sciences, State University of New York, Brockport, New York 14420, USA.

J. G. Kunkel, Department of Zoology, University of Massachusetts, Amherst, Massachusetts 01003, USA.

P. L. Miller, Department of Zoology, South Parks Road, Oxford OXI 3PS, UK. Richard R. Mills, Department of Biology, Virginia Commonwealth University,

Richmond, Virginia 23284, USA. Donald E. Mullins, Virginia Polytechnic Institute and State University, Depart­

ment of Entomology, Blacksburg, Virginia 24061, USA. Rudolph Pipa, Department of Entomology and Parasitology, University of

California, Berkeley, California 94720, USA. Robert R. Provine, Department of Psychology, University of Maryland, Baltimore

County, Catonsville, Maryland 21228, USA. Louis M. Roth, US Army Natick Research and Development Command, Natick,

Massachusetts 01760, USA. Gunter Seelinger, Institute of Zoology, University of Regensburg , D-8400 Regens­

burg, Federal Republic of Germany. Barbara Stay, Department of Zoology, University ofIowa, Iowa City, Iowa 52242,

USA .

• Present address. Department of Zoology, Westfield College, Hampstead, London NW3 7ST, UK.

XVl Contributors

Donald J. Sutherland, Department of Entomology and Economic Zoology, Rutgers University, New Brunswick, New Jersey 08903, USA.

Stephen S. Tobe, Department of Zoology, University of Toronto, Toronto, Ontario M5S IAI, Canada.

Thomas R. Tobin, Department of Entomology, University of Kansas, Lawrence, Kansas 66045, USA.

Preface

This volume deals mainly with the biology of the American cockroach, Periplaneta americana (1.). Contributors were urged to emphasize recent findings, including unpublished data when possible, a goal that would not have been feasible if it were not for the two previously published books on the basic biology of cockroaches, The Biology o/the Cockroach (1968) by D. M. Guthrie and A. R. Tindall and The Cockroach, Volume 1 (1968) by P. B. Cornwell. Those topics not included in The American Cockroach, such as external morphology, are well covered in the two preceding books. In addition, these books provided a broad background upon which contributors to The American Cockroach have been able to build with recent trends, new and established concepts and integration.

Although this book deals primarily with the American cockroach, many chapters offer a comparative approach in sections where the more recent and exciting research has been accomplished on other species. Most contributors place the cockroach in perspective with regard to its appropriateness or inappropriateness for various types of biological investigations. Many questions are realistically left unanswered when no acceptable or obvious solution is apparent; an invitation to new researchers to consider the cockroach as an experimental subject.

W.]. Belt, K. G. Adiyodi