Insect Behavior Robert W. Matthews · Janice R. Matthews

Insect Behavior

Second Edition

123 Robert W. Matthews Janice R. Matthews University of Georgia University of Georgia Dept. Entomology Dept. Entomology Athens GA 30602 Athens GA 30602 USA USA [email protected] [email protected]

ISBN 978-90-481-2388-9 e-ISBN 978-90-481-2389-6 DOI 10.1007/978-90-481-2389-6 Springer Dordrecht Heidelberg London New York

Library of Congress Control Number: 2009926821

© Springer Science+Business Media B.V. 2010 No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work.

Cover design: Boekhorst Design BV

Printed on acid-free paper

Springer is part of Springer Science+Business Media (www.springer.com) Preface to the Second Edition

This book is for all who are interested in the biological sciences. Like the course that originally inspired it, the text is designed for use at senior undergraduate level for college and university students, so we trust that it will find readership among those who have had some basic introduction to entomology and animal behavior. However, we also hope it will prove useful to newcomers who may be approaching behavioral study from other perspectives. This is our second edition, born anew after thirty years. Much has changed during that time, especially in the breadth and depth of a field that (like us) was fairly young back in 1978. New technologies are allowing scientists to shape—and answer— questions in ways that once could not even have been envisioned. Insect behavior research now has wings, and is poised to take off. However, at this juncture, we all must also take care not lose an awareness of our roots. Thus, as writers introducing this exciting field of study to the next generation of scientists and insect enthusiasts, we have tried to strike a balance between new ideas and old, and between modern developments and historical insights. Our objectives in writing this edition remain the same as they have always been. The first of these has been to help readers understand how a number of major behavioral systems function. Thus, this is not an encyclopedia, but an introduc- tion to fundamental concepts and processes as seen from a comparative evolutionary viewpoint. We have not documented numerous strings of examples merely for ‘com- pleteness of coverage’ but instead have tried to give a flavor of the diversity of ways in which insects approach similar life tasks. Because the Internet and excellent search engines have made access to information sources easy and nearly instan- taneous, we have not burdened readers with a cumbersome citations in the text; searching on key terms, aided when necessary by references associated with fig- ure credits at the book’s end, will provide entry into additional literature for those interested in further pursuing subjects we can but introduce. Our second objective has been to help readers gain insights into accessible ways in which behavioral research can be conducted. Whenever possible, we have included discussions of important experiments and investigations, rather than pre- senting a rhetoric of conclusions. Selected principles are interwoven with case stud- ies of specific situations, presenting actual examples in a manner compatible with the dynamic, open-ended field and laboratory experiences in which they have arisen.

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Like any writers of a general textbook, we recognize a deep obligation to many others—to those of whose work we write, to other authors whose ideas we use, to our own teachers who have shaped our perspectives and interests, and to our stu- dents, friends and colleagues with their many stimulating and invaluable suggestions and criticisms. We also thank the many scientists and journal editors who have freely granted permission for the use of published material. Many colleagues have generously provided us with photographs, which are acknowledged in the credits list; special thanks are due to Douglas W. Whitman for contributing numerous new images and to Robert E. Silberglied and Carl W. Rettenmeyer, both now deceased, whose pho- tographic talent continues to enhance this edition. We also are especially grateful to Joan W. Krispyn and Paul H. Matthews for numerous original drawings.

Athens, Georgia Robert W. Matthews Janice R. Matthews Contents

1 The History and Scope of Insect Behavior ...... 1 1.1 Introduction ...... 1 1.1.1 WhatIsInsectBehavior?...... 1 1.1.2 InsectBehavior’sBiologicalContext...... 3 1.1.3 Historical Foundations ...... 6 1.1.4 TheWatershedYears...... 9 1.1.5 TheRiseofEthology...... 13 1.2 Conceptual Frameworks ...... 15 1.2.1 EvolutionbyNaturalSelection...... 15 1.2.2 GeneticsandBehavior...... 17 1.2.3 The Comparative Approach ...... 24 1.2.4 Conceptual Pitfalls ...... 25 1.3 Phylogeny’s Role ...... 28 1.3.1 MicroevolutionandMacroevolution...... 28 1.3.2 Phylogenetic Systematics and Cladistics ...... 33 1.3.3 Behavior and Speciation ...... 36 1.4 Questions and Perspectives ...... 38 1.4.1 Proximate and Ultimate Analyses ...... 40 1.4.2 Types of Approach ...... 41 2 Programming and Integrating Behavior ...... 45 2.1 Introduction ...... 45 2.2 Nerve-BasedCoordination...... 46 2.2.1 TheInsectNervousSystem...... 47 2.2.2 Simple Reflexes and Repeated Motor Patterns . .... 50 2.2.3 EthologicalExplanations...... 56 2.3 LifeinaStimulus-RichWorld...... 59 2.3.1 Sensory Tuning and Filtering ...... 60 2.3.2 MemoryandLearning...... 68 2.3.3 Insect Intelligence ...... 81 2.4 Hormone-Based Coordination ...... 83 2.4.1 Clocks and Reiterative Rhythms ...... 86 2.4.2 GatedRhythms...... 88

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3 Spatial Adjustment ...... 93 3.1 Introduction ...... 93 3.2 Locomotion ...... 94 3.2.1 Terrestrial and Aquatic Locomotion ...... 96 3.2.2 Aerial Locomotion ...... 98 3.3 Orientation...... 100 3.3.1 Locomotory Responses ...... 101 3.3.2 Posture and Position ...... 103 3.3.3 OrientationtoRadiantEnergy...... 105 3.3.4 Magnetic Field Orientation ...... 108 3.3.5 Orientation to the Evidence of Others’ Presence .... 109 3.4 Thermoregulation...... 110 3.4.1 Dormancy and Thermotolerance ...... 110 3.4.2 RegulationofHeatGain...... 113 3.4.3 Heat Production ...... 114 3.5 Migration...... 116 3.5.1 Seasonal Migration ...... 117 3.5.2 Migration Under Ephemeral Conditions ...... 122 3.5.3 DispersalandNavigation...... 124 4 Foraging and Feeding ...... 131 4.1 Introduction ...... 131 4.1.1 Food Recognition and Acceptance ...... 134 4.1.2 Regulation of Feeding ...... 137 4.2 ForagingStrategies...... 140 4.2.1 Herbivory...... 141 4.2.2 Active Search ...... 141 4.2.3 Trapping and Ambush ...... 146 4.2.4 ParasitesandParasitoids...... 148 4.2.5 Theft and Kleptoparasitism ...... 152 4.2.6 InsectAgriculture...... 154 4.2.7 Nest Symbionts: Becoming a House Pet ...... 157 4.3 CoevolutionandtheArmsRace...... 164 4.3.1 Attack, Defense, and Counterattack ...... 165 4.3.2 Employing Mercenaries for Protection ...... 170 4.3.3 The Tommy Tucker Syndrome: Food in Return forServices...... 173 4.4 Feeding as a Communal Activity ...... 177 4.4.1 Simple Groups and Feeding Aggregations ...... 177 4.4.2 Social Feeding Behaviors ...... 181 5 Defense: A Survival Catalogue ...... 185 5.1 Introduction ...... 185 5.2 Defense Messages ...... 186 5.3 Passive Messages ...... 187 5.3.1 Crypsis:‘I’mNotHere!’...... 187 Contents ix

5.3.2 SystemicDefenses:‘I’mNoxious!’...... 194 5.3.3 Mimicry: ‘I’m Someone Else!’ ...... 197 5.3.4 Aposematic Defenses: ‘I’m Dangerous!’ ...... 202 5.4 Active Messages ...... 204 5.4.1 Attack: ‘I’m Turning the Tables!’ ...... 204 5.4.2 Startle: ‘I’m Not What You Thought!’ ...... 209 5.4.3 Group Actions: ‘We’re in This Together!’ ...... 213 6 Chemical Communication ...... 217 6.1 Introduction ...... 217 6.2 Mechanisms of Chemical Communication ...... 217 6.2.1 Odor Creation and Reception ...... 218 6.2.2 Communication Through Chemistry ...... 223 6.3 The Functions of Chemical Communication ...... 227 6.3.1 Finding and Choosing Mates ...... 228 6.3.2 Assembly,Aggregation,andRecruitment...... 231 6.3.3 AlarmandAlert...... 240 6.3.4 Host-Marking...... 242 6.3.5 Recognition ...... 246 6.4 The Information Content of Pheromones ...... 249 6.4.1 Physiological Adjustments: The Q/K Ratio...... 249 6.4.2 Pheromones as Language: Syntax and Lexicon . .... 251 6.4.3 Exploitation and Code-Breaking ...... 255 6.4.4 The Chemical Channel and Other Signal Modes .... 256 6.5 ChemicalCommunicationandInsectControl...... 258 7 Visual Communication ...... 261 7.1 Introduction ...... 261 7.2 Bioluminescence ...... 262 7.2.1 The Physiology of Insect Light Production ...... 263 7.2.2 Bioluminescence as a Communication Method . .... 264 7.3 Light Reception ...... 268 7.3.1 Receptors and Form Perception ...... 268 7.3.2 VisualAcuityandFlickerVision...... 272 7.3.3 PolarizedLightPerception...... 275 7.3.4 ColorVision...... 277 7.4 Functions of Visual Communication ...... 279 7.4.1 AggregationandDispersion...... 281 7.4.2 Alarm...... 283 7.4.3 Sexual Signals ...... 284 7.4.4 Multimodal Signaling ...... 288 8 Mechanocommunication ...... 291 8.1 Introduction ...... 291 8.2 Producing and Sending Signals ...... 292 8.2.1 Sound Creation ...... 293 x Contents

8.2.2 Distance and Substrate ...... 295 8.3 Receiving Signals ...... 296 8.3.1 Vibration...... 298 8.3.2 Hearing...... 303 8.3.3 Communication by Touch ...... 305 8.4 The Acoustic Channel ...... 307 8.4.1 Parameters of Insect Song ...... 307 8.4.2 Song Synchronies ...... 308 8.4.3 Active Acoustics ...... 311 8.4.4 Sound as a Communication Method ...... 313 8.5 Functions of Insect Communicative Sounds ...... 314 8.5.1 Protest,Alarm,andAggression...... 314 8.5.2 Aposematic Sounds and Acoustic Mimicry ...... 319 8.5.3 Sexual Signals ...... 321 8.5.4 Social Sounds ...... 327 9 Reproductive Behavior ...... 341 9.1 Introduction ...... 341 9.2 CourtshipandMating...... 342 9.2.1 ThePhysiologyofMatingBehavior...... 344 9.2.2 Reproduction Modes ...... 346 9.2.3 ComplexityandPlasticity...... 349 9.2.4 Pollination and Male Reproductive Behavior ...... 354 9.3 Courtship and Conflict ...... 359 9.3.1 Dimorphism, Sexual Selection, and Mate Choice . . . 361 9.3.2 Intrasexual Competition ...... 369 9.3.3 Territoriality and Dominance ...... 371 9.3.4 NuptialGifts...... 372 9.4 MatingSystemsandParentalInvestment...... 380 9.5 Oviposition Behavior ...... 382 9.5.1 SelectingaSiteorHost...... 383 9.5.2 Reproductive Rates and Energy Allocation ...... 387 10 Parental Behaviors and Social Life ...... 389 10.1 Introduction ...... 389 10.2 Social Organization ...... 390 10.2.1 Aggregations and Simple Groups ...... 390 10.2.2Parent-OffspringInteractions...... 394 10.2.3 Solitary and Communal Nesters ...... 400 10.3 The Insect Social Register ...... 407 10.3.1TheAnts...... 410 10.3.2TheEusocialWasps...... 416 10.3.3TheBees...... 420 10.3.4TheTermites...... 423 10.3.5 Lesser Known Candidates ...... 427 10.4 Implications and Correlates of Social Life ...... 428 Contents xi

10.4.1TheEcologyofParentalCare...... 430 10.4.2 Paradoxes of Insect Sociality ...... 434 10.4.3 Interspecific Social Interactions ...... 440 Credits ...... 445 Plates ...... 463 Index ...... 503 Case Studies

1.1 Foraging Onset in the Honey Bee, Apis mellifera ...... 42 2.1 Escape Behavior in the Cockroach, Periplaneta ...... 53 2.2 HowNoctuidMothsHearBats...... 63 2.3 Learning in the Parasitoid Wasp, Hyssopus ...... 77 2.4 Initiation of Adult Behavior in Saturniid Moths ...... 89 3.1 Migration in the Milkweed Bug, Oncopeltus ...... 118 4.1 Myrmecophily in the Rove Beetle, Atemeles ...... 159 4.2 Coevolution of Acacias and Their Ants, Pseudomyrmex ...... 171 4.3 Mutualism Between Fig Trees and the Wasp, Blastophaga ...... 175 4.4 Group Feeding and Cannibalism in the Willow Leaf Beetle, Plagiodera ...... 179 5.1 Melanism in the Peppered Moth, Biston betularia ...... 191 6.1 Identification of the Mate Attractant of the Silkworm Moth, Bombyx mori ...... 225 6.2 Aggregation in a Bark Beetle, Dendroctonus ...... 232 6.3 Host-searching by an Ichneumonid Wasp, Pleolophus ...... 243 7.1 Visual Communication in the Silver-Washed Fritillary, Argynnis paphia ...... 286 8.1 Vibrotaxis in the Thorn Bug, Umbonia crassicornis ...... 300 8.2 Aggressive Singing in Two Crickets, Acheta and Gryllus ...... 317 8.3 Sexual Attraction in the Mosquito, Aedes aegypti...... 324 8.4 Communicatory Interaction in the Honey Bee, Apis mellifera ...... 328 9.1 Courtship in the Crane Fly, Tipula oleracea ...... 351 9.2 Female Choices in the Stalk-Eyed Fly, Cyrtodiopsis ...... 365 9.3 Nuptial Gifting in the Arctiid Moth, Cosmosoma ...... 374 10.1 Reversed Sex Roles in the Giant Water Bug, Abedus ...... 398 10.2 Cyclical Foraging in Army Ants, Eciton ...... 413 10.3 Egg-Carrying in the Golden Egg Bug, Phyllomorpha ...... 428 10.4 Parental Care in the Stink Bug, Antiteuchus tripterus ...... 432

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