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 Cover photo credit: The male Eastern Tiger Swallowtail, Papilio glaucus, shown here is one of the most recognizable butterflies in North America; females of this species are dimorphic, appearing in both yellow and black forms. Like many other butterflies, swallowtails are attracted to the aromatic flower clusters of Lantana for nectar, but do not lay eggs on its somewhat toxic foliage. The authors took this photograph in their garden. 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. v vi Preface to the Second Edition 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 vii viii Contents 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