Perspectives on Animal Behavior

This page intentionally left blank

Perspectives on Animal Behavior

This page intentionally left blank

Perspectives on Animal Behavior

Third Edition

Judith Goodenough

Biology Department / University of Massachusetts, Amherst

Betty McGuire

Department of Ecology and Evolutionary Biology / Cornell University, Ithaca

Elizabeth Jakob

Psychology Department / University of Massachusetts, Amherst

John Wiley & Sons, Inc.

VICE PRESIDENT AND EXECUTIVE PUBLISHER Kaye Pace
SENIOR ACQUISITIONS EDITOR Kevin Witt
EDITORIAL PROGRAM ASSISTANT Alissa Etrheim
EDITORIAL ASSISTANT Jenna Paleski
PRODUCTION SERVICES MANAGER Dorothy Sinclair
SENIOR PRODUCTION EDITOR Janet Foxman
EXECUTIVE MARKETING MANAGER Clay Stone
CREATIVE DIRECTOR Harry Nolan
SENIOR DESIGNER Kevin Murphy
PHOTO EDITOR Sheena Goldstein
SENIOR ILLUSTRATION EDITOR Anna Melhorn
SENIOR MEDIA EDITOR Linda Muriello
PRODUCTION SERVICES Cécile Billioti de Gage/ Preparé
COVER DESIGN M77 Design
COVER PHOTO Richard Packwood/Getty Images, Inc.

This book was set in 10/12 Janson by Preparé and printed and bound
by Courier/Kendallville. The cover was printed by Courier/Kendallville.

This book is printed on acid-free paper.
8

Copyright © 2010, 2001, 1993 John Wiley & Sons, Inc. 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, scanning or
otherwise, except as permitted under Sections 107 or 108 of the 1976 United States
Copyright Act, without either the prior written permission of the Publisher, or authorization
through payment of the appropriate per-copy fee to the Copyright Clearance Center, Inc.,
222 Rosewood Drive, Danvers, MA 01923, website www.copyright.com. Requests to the
Publisher for permission should be addressed to the Permissions Department, John Wiley &
Sons, Inc., 111 River Street, Hoboken, NJ 07030-5774, (201) 748-6011, fax (201) 748-6008,
website www.wiley.com/go/permissions.

To order books or for customer service, please call 1-800-CALL WILEY (225-5945).

Library of Congress Cataloging-in-Publication Data
Goodenough, Judith.

Perspectives on animal behavior / Judith Goodenough, Betty
McGuire, Elizabeth Jakob.—3rd ed.

p. cm.
Includes bibliographical references (p. ).
ISBN 978–0–470–04517–6 (cloth)
1. Animal behavior. I. McGuire, Betty. II. Jakob, Elizabeth M.
III. Title.

QL751.G59 2010 2009013360
591.5—dc22

Printed in the United States of America

10 9 8 7 6 5 4 3 2 1

To my husband, Stephen Goodenough,
my daughters Aimee and Heather,
and my mother, Betty Levrat.
J. G.

In loving memory of James Patrick McGuire.
To Willy, Kate, and Owen Bemis,

and to Dora, Kevin, and Cathy McGuire.
B. M.

To Adam Porter and Margaret Dringoli, with love and gratitude.
E. J.

This page intentionally left blank

Preface

Outside the window, male ruby-throated humming- underpinnings, outward to its environment, and back in
birds newly returned from wintering in Central time to its evolutionary origins. Thus, animal behavior
America are brightening this early May day in the draws together fields of study that might often seem,
northeastern United States. The remarkable annual especially to a student early in his or her academic
migration of these tiny birds is a behavioral story in its career, to have little to do with one another. Our hope
own right, complete with a long, foodless crossing of is that readers of this book will see that the facts learned
the Gulf of Mexico to return to breeding areas they left in different courses are connected after all.
here more than six months before. But today it is the
behavior of the males that is the most immediate–they The authors of this third edition share a deep
are claiming or in some cases reclaiming feeding terri- interest in animal behavior, from the standpoints of
tories through dramatic aerial displays and battles. In a teaching, writing, and research. Yet each brings to this
week or so the females will arrive and the interactions project a very different perspective. Judith
will further intensify, as the breeding season gets under Goodenough, from the Department of Biology at the
way. Watching and understanding these behaviors University of Massachusetts Amherst, has led the
offers ways to engage nature in new and deeper ways, charge from the very first edition of this text. Judith has
and it places our own lives in the context of the other studied biological rhythms in creatures from planaria
animals that share the planet with us. to finches to deer mice (not to mention in the green
alga Chlamydomonas). Betty McGuire, from the
This brief foray into the easily observed lives of Department of Ecology and Evolutionary Biology at
hummingbirds illustrates a simple point: animal behav- Cornell University, who wrote eight chapters for the
ior is engaging to watch, as evidenced by the popularity first edition of the book but stepped down from the
of nature shows on both small and big screens. In fact, second edition because of other obligations, returns to
those of us fortunate enough to offer a course in animal this third edition. Betty’s research focuses on parental
behavior are often told by our colleagues how lucky we behavior, reproduction, and ecology of small mammals,
are to teach a subject that people of all backgrounds and she occasionally dabbles in work with larger
find fascinating. There is something very appealing in domestic animals such as dogs and horses. In addition
learning about the often bizarre lives going on around to Perspectives in Animal Behavior, Judith and Betty have
us, sometimes literally under our noses. coauthored Human Biology: Personal, Environmental, and
Social Concerns and Biology of Humans: Concepts,
Besides satisfying our natural curiosity, the study of Applications, and Issues. Elizabeth Jakob, from the
animal behavior is truly interdisciplinary. To deeply Department of Psychology at the University of
understand an animal’s behavior, we must look both Massachusetts Amherst, joins the team of authors. Beth
inward to its genetic, morphological, and physiological

vii

viii Preface

studies the behavior of spiders, asking questions about CHANGES AND UPDATES TO
their learning, perception, and interactions with con- THE THIRD EDITION
specifics and with other species. She has carried out
field projects in California, Mexico, Massachusetts, and We added new features to this edition to promote crit-
Maine, and she also does laboratory experiments when ical thinking, active learning, and the development of
the questions or the long Massachusetts winters vocabulary. We retained certain features from previous
demand it. She coauthored the fifth edition of Animal editions, such as the outlines at the start of each chapter
Behavior: Mechanisms, Ecology, Evolution and co-edited and the summary at the end, to help students organize
the laboratory manual Learning the Skills of Research: material and identify key concepts.
Laboratory and Field Exercises in Animal Behavior.
Collectively, the three of us have taught courses rang- NEW STOP AND THINK QUESTIONS
ing from large lectures for nonmajors to upper division
courses in animal behavior, vertebrate biology, and Each chapter has at least one Stop and Think Question
evolution. designed to encourage students to pause from reading
the text, think about the information they have just read,
Our goals and basic approach remain the same as in and apply it to a new situation. Many of these questions
the first two editions: to help students understand the focus on experimental design, methodology, or ethics.
history, mechanisms, development, function, and evo-
lution of behavior. To this end we introduce the major NEW BOLD TERMS AND GLOSSARY
approaches to the study of animal behavior and show
how these diverse approaches can be integrated to pro- Key terms in each chapter are now set in bold type
vide a more complete understanding of any particular when first formally introduced. These terms and others
behavior. Because courses in animal behavior are offered of lesser importance are included in the new glossary at
in biology, psychology, and animal science departments, the end of the book.
we include basic background material-for example, in
genetics, neurophysiology, and endocrinology–to ensure INCREASED EMPHASIS ON ALTERNATIVE
that each chapter can stand alone and that each con- HYPOTHESES
tains information accessible to students with different
backgrounds. Within each chapter, the examples we To increase our coverage of the ways in which scientists
develop provide a balance between classic and recent design and carry out research in animal behavior, we
studies. Throughout the text we use clear and engaging added many new in-depth examples to illustrate the
writing to explain potentially complex topics such as importance of developing and testing alternative
behavioral genomics and mathematical models of hypotheses. These examples will help students under-
behavior. stand how research is conducted and allow them to bet-
ter design their own experiments and to evaluate the
In organization, this third edition begins in much primary literature of animal behavior.
the same way as previous editions, with an introduc-
tory chapter on hypothesis testing, followed by Part 1 INCREASED COVERAGE OF SEVERAL KEY
on approaches to the study of animal behavior. These AREAS
early chapters present students with the questions
asked and methods used by scientists working in sub- In response to current events and reviewer comments,
fields of animal behavior such as behavioral genetics, we increased our coverage of the growing interactions
behavioral endocrinology, and behavioral ecology. Part between the fields of animal behavior and conservation
2 focuses on how behavior relates to the survival of biology. In particular, we include examples that demon-
individuals and includes chapters, for example, examin- strate how studies of behavior yield information critical
ing how animals find places to live, feed, and avoid to conservation efforts. We also address ethical issues in
being eaten. The chapters in Part 3 focus on interac- behavioral research, and on the flip side, we examine
tions between individuals, such as those between how behavioral research provides information essential
mates, parents and offspring, competitors, or collabo- to improving the lives of captive animals. This edition
rators. We also describe communication in detail also includes more examples from the fields of human
before moving on to exploring how it is used in con- behavior and applied animal behavior.
flict and cooperation.

Acknowledgments

Our editor, Kevin Witt, had confidence that three Ethan Cloftfelter, Amherst College
academics with very different schedules could work Fiona Cross, University of Canterbury
together to produce a current text with a single voice. Perri Eason, University of Louisville
We thank him for his encouragement and support. Sarah Huber, Randolph-Macon College
Many other dedicated people at John Wiley & Sons Brian Kelly, University of Massachusetts Amherst
helped get this book into your hands. Alissa Etrheim, Chris Maher, University of Southern Maine
our editorial program assistant, helped us put this book Sarah Partan, Hampshire College
together. She provided gentle reminders to keep us on Mark Petrie, University of Canterbury
schedule and always offered to help in any way possible. Jeff Podos, University of Massachusetts Amherst
We are particularly grateful for her help with permis- Denise Pope, Mount Holyoke College
sions. The text was improved by the skills of our copy Adam Porter, University of Massachusetts Amherst
editor, Betty Pessagno. Anna Melhorn, Senior Nancy Solomon, Miami University of Ohio
Illustration Editor, and Sheena Goldstein, our photo Theodore Stankowich, University of Massachusetts
editor, are largely responsible for the appearance of the Amherst
text. We also thank Will Sillin for his beautiful illustra- Zoran Tadic, University of Zagreb
tions that begin each chapter and each of the three Christina Veino, University of Massachusetts
parts of the book. Elaine Soares, our photo researcher, Amherst
worked diligently to find the perfect photographs for Paige Warren, University of Massachusetts Amherst
our needs. Cécile Billioti de Gage/Preparé headed pro- Gordon Wyse, University of Massachusetts
duction of our book. She helped set priorities and suc- Amherst
cessfully moved the project along even at the busiest
times of the academic year. We are now happy to pass We are also grateful to the many authors who were
the project to the capable hands of Lucy Parkinson, our generous enough to check over our portrayal of their
marketing director. Each person is a professional, a work. Any remaining errors are, of course, ours.
pleasure to work with, and a team player.
FROM JUDITH GOODENOUGH
We thank the reviewers who provided essential feed-
back that helped shape this new edition: I would like to thank many of my friends and col-
leagues at UMass for lending their expertise to various
Mitchell Baker, Queens College aspects of this book. Zane Barlow’s comments on
Zane Barlow, University of Massachusetts Amherst genetics greatly improved the chapter. As always,
Willy Bemis, Cornell University Gordon Wyse provided valuable suggestions on the
Renae Brodie, Mount Holyoke College nervous system. Adam Porter helped smooth the writ-
Bruce Byers, University of Massachusetts Amherst

ix

x Acknowledgments

ing of the most difficult sections. My e-mail friend refuge at the Jersey shore where I could escape the
from Croatia, Zoran Tadic, Faculty of Science, deadlines and e-mail (not to mention the weather in
University of Zagreb, provided useful comments and a Ithaca), and relax and reconnect for a few days. My
fresh perspective on many chapters. Although she did father, James McGuire, died during the writing of this
not help with writing, Margaret Ludlam helped me edition. He was an avid birder and a dedicated volun-
cope when things got tense, as they often did. She is teer at his local animal shelter, and I know that he
always cheerful and calm. Most of all, I would like to would have enjoyed our new text. Finally, I thank
thank my family who have always been my cheering Lowell Getz, close friend and colleague of almost 25
squad, and who have encouraged and supported me at years, for listening patiently and always being there. We
every stage of this revision. My husband Steve bore the will get those manuscripts done, Lowell, I promise!
brunt of my obsession. After months of my spending
many more hours with the computer than with him, FROM BETH JAKOB
Steve merely quipped that he was getting rather fond
of the back of my head and continued to do what was I thank my husband, Adam Porter, who was incredibly
necessary to keep the household running smoothly. supportive throughout this process, was always ready
He’s the funniest person I know, and his wit kept me to read something and offer his frank opinion and
sane. After 38 years of marriage, he still keeps me on detailed edits, and saved our credit rating by taking
my toes by introducing me as his first wife. My daugh- over paying the bills when I was too distracted to
ters, Aimee and Heather, still the joy of my life, remind notice them. I began work on my section of the book
me that the people you love must always come first. during my sabbatical leave, and I thank the faculty,
They’ll find time to spend with me when they know I staff, and students of my host institution at the
need a break. Their courage and confidence in reach- University of Canterbury, Christchurch, New Zealand
ing for their dreams encourages me to keep stretching for their help and friendship, Robert Jackson for his
toward mine—the most immediate of which is the sponsorship, and the Fulbright Foundation for sup-
completion of this revision. My mother, Betty Levrat, port. I am grateful for the patience of my graduate stu-
instilled in me a love of learning and was always willing dents and collaborators whose manuscripts and paper-
to do whatever needed to be done to free time for my work languished during the more intense periods of
writing. book preparation. Penny Jaques, Betsy Dumont, Joe
Elkinton, and my other colleagues in the Organismic
FROM BETTY MCGUIRE and Evolutionary Biology Program kept me sane and
at least somewhat on track when I foolishly agreed to
I thank my husband, Willy Bemis, for his continuous be Graduate Program Director when this book was
encouragement throughout this project and willingness underway. I am grateful to additional friends and fam-
to read (and edit) everything I passed his way. My ily for forgiving my incessant conversation, deep sighs,
daughter Kate let us use some of her wonderful photo- and continuous e-mails about the book and for
graphs in the third edition–at 16 she already has a keen reminding me that there are other things beyond my
eye and understanding of animal behavior. I thank my computer screen, particularly Doreen Jakob, Alexis
son, Owen, who always reminds me, by his near contin- Jakob, Carolyn Truini, Jack Dringoli, Margaret
uous recitation of animal facts, how fascinating animals Dringoli, Perri Eason, Marta Hersek, Chris Maher,
are to all who watch them. My mother, Dora McGuire, Maggie Hodge, and Nancy Reynolds. Now it’s finally
and siblings, Kevin and Cathy McGuire, provided time to get back outside!

Contents

Chapter 1 • Introduction 1 Chapter 3 • Genetic Analysis of Behavior 27

Four Questions About Animal Behavior 2 Basics of Gene Action 28
Animal Behavior as an Interdisciplinary Study 2 Goals of Behavioral Genetics 31
Methods of Behavioral Genetics 31
The Interplay of Questions: A Case Study 3
Inbreeding 31
Hypothesis Testing 5 Artificial Selection 33
Inducing Mutations and Screening for Change in
Part 1 • Approaches to the Study
of Animal Behavior Behavior 35
Finding Natural Variants and Looking for Genetic
Chapter 2 • History of the Study of Animal
Behavior 11 Differences 36
Hybridization 37
The Beginnings 11
Intellectual Continuity in the Animal World 11 The Foraging Gene as an Example of Behavioral
Darwin's Evolutionary Framework 12 Genetics in Action 38

Classical Ethology 13 Candidate Genes 38
The Approach: Evolutionary, Comparative, Linking a Protein to a Trait 40
Descriptive, Field-Oriented 13 Locating all the Genes Associated with a Trait 41
Classical Ethological Concepts 15 Microarray Analysis 41

Comparative Psychology 17 Important Principles of Behavioral Genetics 42
The Approach: Physiological, Developmental, One Gene Usually Affects Several Traits 42
Quantitative, Laboratory-Oriented 17 Genes Work in Interacting Networks 44
Early Concepts of Comparative Psychology 17
The Roots of Physiological Psychology 20 Behavioral Variation and Genes 45
Environmental Regulation of Gene Expression 47
Sociobiology and Behavioral Ecology 20
More Recent Trends 22 Dominance Relationships in Cichlid Fish 47
Song Learning in Male Songbirds 48
Field Studies 22 The Importance of Genetic Background to Behavioral
Cellular and Molecular Basis of Behavior 22
Behavioral Biology 23 Genetics 50
Applied Animal Behavior 23 Networks of Genes are Responsive to the

Environment 51

Epigenetics and Behavioral Genetics 52
Complex Relationships Among Genes 54
A Broader Perspective 54

xi

xii Contents

Chapter 4 • Natural Selection Predators and Prey: The Neuroethology of Life-and-
and Behavior 57 Death Struggles 109

Natural Selection 58 Processing in the Central Nervous System 113
Common Misunderstandings About Natural Brain Changes Underlying Behavioral Change 113
Selection 60 Social Behavior Network 120
Genetic Variation 61
Responding—Motor Systems 122
Variation is Common 61 Neural Control in Motor Systems 122
The Raw Material of Genetic Variation 61 Locust Flight 122

Variation and the Response to Natural Chapter 7 • Physiological Analysis of
Selection 62 Behavior—The Endocrine
System 127
The Maintenance of Variation 63
Gene Flow and Genetic Drift 63 The Endocrine System 129 130
Correlated Traits 65 Endocrine Glands and Hormones 129
Changing Environmental Conditions 65 Hormonal Versus Neural Communication 129
Frequency-Dependent Selection 67 Types of Hormones and Their Modes of Action
Negative-Assortative Mating 68
Evolutionarily Stable Strategies: Fitness and the How Hormones Influence Behavior 132
Behavior of Others 68 Effects on Sensation and Perception 132
Effects on Development and Activity of the Central
Testing Hypotheses About Natural Selection Nervous System 133
and Adaptation 70 Effects on Muscles 133

The Experimental Approach 72 Methods of Studying Hormone–Behavior
The Comparative Approach 73 Relationships 135
Monitoring Selection in the Field 75
Modeling the Costs and Benefits of Traits 75 Interventional Studies 135
Correlational Studies 137
Chapter 5 • Learning and Cognition 77

Definition of Learning 78 Organizational and Activational Effects of
Types of Learning 78 Hormones 139

Habituation 78 Defining the Dichotomy 139
Classical Conditioning 80 Sex Differences in the Behavior of Norway
Operant Conditioning 82
Latent Learning 84 Rats 139
Social Learning 85 Individual Differences in the Behavior of Male Tree

Species Differences in Learning: Lizards 141
Comparative Studies 87 Questioning the Dichotomy 141

The Ability to Learn as a Heritable Trait 87 The Dynamic Relationship Between Hormones
Evolution and the Variation in Learning and Behavior 142

Across Species 88 A Reciprocal Relationship 142
Hormonal Suppression of Behavior 142
Other Evidence of Cognitive Abilities
in Animals 91 97 Interactions Between Hormones, Behavior, and
the Environment 142
Tool Use 92
Detours 94 Adjusting to the Harshness and Predictability of the
Understanding Numbers and Other Physical Environment 143

Abstract Concepts 95 Adjusting to Onlookers in the Social
Self-Recognition and Perspective Taking Environment 145

Chapter 6 • Physiological Analysis—Nerve A Detailed Look at the Hormonal Basis of
Cells and Behavior 99 Selected Behaviors 146

Concepts from Cellular Neurobiology 100 Helping at the Nest 146
Types of Neurons and Their Jobs 100 Scent-Marking 147
The Message of a Neuron 101 Migrating 148
Ions, Membrane Permeability, and Behavior 104
Chapter 8 • The Development
Behavioral Change and Synaptic Transmission 104 of Behavior 151
The Structure of the Synapse 104
Integration 106 Influences on Behavioral Development 152
Development of the Nervous System 152
Specializations for Perception of Biologically Development of Nonneural Structures 155
Relevant Stimuli—Sensory Processing 107 Hormonal Milieu 155
Physical Characteristics of the Environment 157
Processing of Sensory Information for Sound Experience Through Play 158
Localization 108

Contents xiii

The Concept of Sensitive Periods 159 Magnetic Cues 214
Changing Terminology—From Critical Periods to Cues from the Earth’s Magnetic Field 214
Sensitive Periods 159 Directional Information from the Earth’s
Timing of Sensitive Periods 160 Magnetic Field: A Magnetic Compass 217
Multiple Sensitive Periods 161 Positional Information from the Earth’s
Some Examples of Sensitive Periods in Behavioral Magnetic Field: A Magnetic Map? 218
Development 161 Magnetoreception 222

Pulling It All Together—The Development of Chemical Cues 224
Bird Song 171 Olfaction and Salmon Homing 224
Olfaction and Pigeon Homing 226
Genetic, Hormonal, and Neural Control of Song 172
Role of Learning in Song Development 174 Electrical Cues and Electrolocation 229
Sensitive Periods in Song Learning 176
Own-Species Bias in Song Learning 178 Chapter 11 • The Ecology and Evolution
Social Factors and Song Development 178 of Spatial Distribution 233
A Diversity of Song Learning Strategies 179
Remaining at Home Versus Leaving 234
Developmental Homeostasis 180 Costs and Benefits of Natal Philopatry 234
Rehabilitation of Chimpanzees After Long-Term Costs and Benefits of Natal Dispersal 235
Isolation 180 Sex Biases in Natal Dispersal 238
Natal Dispersal and Conservation Biology 240

Part 2 • Survival Habitat Selection 241
Indicators of Habitat Quality 241
Chapter 9 • Biological Clocks 185 Search Tactics 243
Effects of Natal Experience 243
Defining Properties of Clock-Controlled Habitat Selection and Conservation
Rhythms 186 Biology 244

Persistence in Constant Conditions 186 Migration 245
Entrainment by Environmental Cycles 187 Costs of Migration 246
Temperature Compensation 188 Benefits of Migration 248
Migration and Conservation Biology
Rhythmic Behavior 189 251
Daily Rhythms 189
Lunar Day Rhythms 189 Chapter 12 • Foraging Behavior 253
Semilunar Rhythms 189
Monthly Rhythms 190 Obtaining Food 253
Annual Rhythms 191 Suspension Feeding 254
Omnivory 254
The Clock Versus the Hands of the Clock 192 Herbivory 254 259
Advantages of Clock-Controlled Behavior 192 Carnivory 256
Adaptations for Detecting Prey
Anticipation of Environmental Change 192
Synchronization of a Behavior with an Event Optimal Foraging 264
Diet Selection: A Simple Model 265
That Cannot Be Sensed Directly 193 Deciding When to Leave a Patch: The Marginal
Continuous Measurement of Time 194 Value Theorem 267
Adding Complexity and Realism 268
Adaptiveness of Biological Clocks 194 The Utility of Models 274
Organization of Circadian Systems 194

Multiple Clocks 195
Coordination of Circadian Timing 195

Human Implications of Circadian Rhythms 200 Chapter 13 • Antipredator Behavior 275
Jet Lag 200
Human Health 200 Camouflage 277 277
Coloration Matching the Visual Background
Chapter 10 • Mechanisms of Orientation Disruptive Coloration 280
and Navigation 203 Countershading 282
Transparency 283
Levels of Navigational Ability 204 Masquerade 284
Piloting 204 Other Functions of Color 284
Compass Orientation 204
True Navigation 206 Polymorphism 285
Warning Coloration 287
Multiplicity of Orientation Cues 206 Batesian Mimicry 289
Visual Cues 206 Diverting Coloration, Structures,
and Behavior 290
Landmarks 206
Sun Compass 207 False Heads 290
Star Compass 211 Autotomy 291
Polarized Light and Orientation 212 Feigning Injury or Death 292

xiv Contents

Intimidation and Fighting Back 294 Chemical Senses 361
Enhancement of Body Size and Display Touch 364
of Weaponry 294 Electrical Fields 365
Eyespots 294
Chemical Repellents 296 Multimodal Communication 366
Functions of Communication 367
Pronouncement of Vigilance 297
Group Defense 298 Species Recognition 368
Mate Attraction 369
Alarm Signals 298 Courtship and Mating 369
Improved Detection 299 Maintaining Social Bonds 372
Dilution Effect 299 Alarm 372
Selfish Herd 300 Aggregation 373
Confusion Effect 301 Agonistic Encounters 374
Mobbing 301 Communication about Resources:

Maintenance of Antipredator Behavior 302 A Case Study 374

Chapter 17 • The Evolution of
Communication 381

Part 3 • Interactions Between The Changing Views of Communication 381
Individuals Sharing Information 381
Manipulating Others 382

Chapter 14 • Reproductive Behavior 305 Signals and Honesty 382
When are Honest Signals Likely? 382
Sexual Selection: Historical and Theoretical When are Dishonest Signals Likely? 386 386
Background 306 Can Honest and Dishonest Signals Coexist?

Explanations for Sex Differences in Reproductive The Evolutionary Origins of Signals 387
Behavior 306 Ritualization 387
Receiver-Bias Mechanisms 390
Revisiting the Ideas of Bateman 308

Intrasexual Selection—Competition for Mates 309 Selective Forces That Shape Signals 391
Adaptations That Help a Male Secure Copulations 309 Characteristics of the Sender 391
Adaptations That Favor the Use of a Male’s Sperm 313 Characteristics of the Environment 392
Sexual Interference: Decreasing the Reproductive Characteristics of the Receiver 395
Success of Rival Males 318

Intersexual Selection—Mate Choice 320 Language and Apes 396
Criteria by Which Females Choose Mates 320 What is Language? 396
Origin and Maintenance of Mate-Choice Ape Language Studies 397
Preferences 327
Cryptic Female Choice 329 Communication and Animal Cognition 401

Sexual Conflict 330 Chapter 18 • Conflict 405

Chapter 15 • Parental Care and Mating Aggression and Conflict 406
Systems 333 Why Do Animals Fight? 406

Parental Care 334 An Evolutionary View of Conflict 406
Conflicts Among Family Members Over Parental The Evolution of Fighting Behavior 406
Investment 334 Using Game Theory to Understand
Some Factors That Influence the Allocation the Evolution of Conflict 406
of Parental Resources 336 Asymmetries in Contests 410
Overall Patterns of Parental Care 339
Dispensing with Parental Conflict Among Group Members 413
Care—Brood Parasitism 343 How Dominance is Determined 413
The Benefits of Being Dominant 413
Mating Systems 345 The Benefits of Being Subordinate 414
Classifying Mating Systems
Monogamy 346 345 Conflict Over Space 415
Polygyny 349 Home Ranges, Core Areas, and Territories 415
Polyandry 353 The Ideal Free Distribution and Space Use 415
The Economics of Holding a Territory 416
Chapter 16 • Communication: Channels and The Economics of Territory Size 416
Functions 355 Strategies for Reducing the Cost
of Territorial Defense 417

The Definition of Communication 356 A Proximate View of Conflict 419
Channels for Communication 356 Aggression and Testosterone 419
Stress, Aggression, and Dominance 420
Vision 356
Audition 358
Substrate Vibrations 361

Contents xv

Chapter 19 • Group Living, Altruism, and Examples of Cooperation Among Animals 434
Cooperation 423 Alarm Calls 434
Cooperation in Acquiring a Mate 436
Living in Groups: From Aggregations to Cooperative Breeding and Helping 439
Structured Societies 423 Eusociality 445

Benefits of Group Living 424 Glossary 451
Costs of Living in Groups 426 References 461
Balancing Costs and Benefits 427 Photo Credits 513
Permissions 517
The Puzzle of Altruism 427 428 Index 523
Individual Selection and “Altruism”
Kin Selection 428
Reciprocal Altruism 432
Manipulation 434

This page intentionally left blank

1

Introduction

Four Questions About Animal Behavior In one way or another, people have been studying ani-
mal behavior for thousands of years. The most skillful
Animal Behavior as an Interdisciplinary Study hunters and fishermen are usually those who can make
predictions about the behavior of their prey (Figure 1.1).
The Interplay of Questions: A Case Study It is important to know that when salmon are spawning,
they will not respond to a fisherman’s bait; that many
Hypothesis Testing rodents escape toward the dark, whereas most birds
escape toward the light; and that many kinds of animals
A New Caledonian crow picks up a twig, bends it into a will fight, some ferociously, if they are trapped.
hook with her foot, pokes it into a hole, and pulls out an
insect. A male wolf spider does a rhythmic courtship The study of animal behavior may have occupied the
dance, waving his tufted legs as he approaches an atten- fringes of human consciousness for centuries for just such
tive female. An albatross spreads its massive wings, lifts a practical reason. Later, when animals were domesti-
off into the ocean breezes, and does not touch land again cated and put to work, it was necessary to learn new
for two years. Two male rattlesnakes entwine themselves things about them. Horses could be trained for riding or
in a wrestling match, settling their dispute without for pulling wagons or tools. Dogs could be trained to
resorting to a venomous bite. And an emperor penguin, track prey or to protect individual humans; cats could not.
huddled on the ice in the endless blizzards of an
Antarctic winter, forgoes food for months while incu- In time, the study of animal behavior took on new
bating the egg delicately balanced on his feet. dimensions. The goals, as well as the techniques,
changed. Animals are no longer studied simply so that
The behavior of animals is featured on endless we can exploit them more efficiently, although this may
nature shows and even the occasional big-screen block- still be one reason for our attention. Now, however, we
buster for a reason—we find fascinating these glimpses have become aware that increased knowledge of the
into the worlds of the other creatures on our planet. behavior of specific species in their natural habitats may
How does the world appear to them? Do they think and help us save some endangered groups from extinction.
feel like we do? How did such strange behaviors come In addition, information on their normal behavior may
to exist? help us ensure their welfare, not just in the wild, but also
in laboratories or zoos (Blumstein et al. 2004; Sutherland
At this point in human history, we have the luxury et al. 1998; Swaisgood 2007). We may be interested in
of studying animal behavior for curiosity’s sake. In the
past, our interest in it was based on more practical needs.

1

2 Chapter 1 / Introduction

FIGURE 1.1 People have been studying animal behavior focus on function (survival value) and evolution. It has
for centuries, sometimes for very practical reasons. also been suggested that consideration of the mecha-
Knowledge of the behavior of game species may make it nisms of behavior should, at least in some cases, include
easier to put food on the table. both cognitive and emotional mental processes (Emery
and Clayton 2005).
behavior as an example of a broader intellectual concern,
such as evolutionary theory. Or we may be interested in To better appreciate the types of questions we may
studying animal behavior because it may serve as a model ask about animal behavior, consider a familiar phenom-
to help us understand human behavior. And, as we said enon: the seasonal migration of songbirds between
before, sometimes we are fortunate enough to be able to northern and southern latitudes. As new birds appear
study animal behavior simply because our curiosity daily at backyard feeders in early spring, we may each
prompts us to ask questions about some of the organisms become curious about migration, but depending on our
with which we share the earth. personal interests, each of us may ask different questions.
How do they “know” it is time? How do they find their
FOUR QUESTIONS way? Such questions focus on the mechanisms that
ABOUT ANIMAL BEHAVIOR underlie the behavior. Must those making this journey
for the first time learn the route from experienced trav-
As casual observations of animal behavior crystallized elers? Do they inherit a directional tendency from their
into a field of scientific study, Niko Tinbergen (1963) parents? Questions such as these concern development.
identified four types of questions that should be asked Why do they do it? What do they gain that outweighs
about behavior: What are the mechanisms that cause it? the risks and demands of such a journey? These are ques-
How does it develop? What is its survival value? How tions about the survival value, or adaptiveness of migra-
did it evolve? Tinbergen believed that ethology—the tion. Finally, how did it all begin? Were the advancing
biological study of behavior—should “give equal atten- glaciers responsible? Were the migratory paths modified
tion to each of them and to their integration.” during the thousands of years each species has been
Tinbergen’s four questions are sometimes condensed migrating? These questions center on the evolution of
into two categories: “how” questions, which focus on the behavior. So we see that when we ask why an animal
causation and development, and “why” questions, which behaves in a certain way, some of us may be asking about
immediate causes (the machinery underlying the
response) and others may be asking about the evolu-
tionary causes.

No one type of question is better than the others.
Answers to all types are necessary as we weave the fab-
ric of our understanding. These are not competing
avenues of investigation. Rather, they are complemen-
tary. Each may feed back on the others, deepening our
understanding and broadening our avenues of investi-
gation (Armstrong 1991; Halpin 1991; Stamps 1991).

ANIMAL BEHAVIOR AS
AN INTERDISCIPLINARY STUDY

Marion Stamp Dawkins (1989) has drawn an analogy
between Tinbergen’s (1963) four aspects of investigation
of behavior and the four legs of an animal. An animal
that lacks one of its legs can only hobble along.
Similarly, progress in the study of animal behavior is
hampered by a lack of information in any one of these
areas of study. This is not to imply that each investiga-
tor must ask all types of questions. Often we find that
individuals are more excited by one type of question than
by others. However, each investigator will be more suc-
cessful in finding the answer to the question of personal
interest if he or she is armed with information and tech-
niques from all four areas of study.

Animal Behavior as an Interdisciplinary Study 3

THE INTERPLAY OF QUESTIONS: the dominant pair raise their offspring. They baby-sit,
A CASE STUDY attack predators, drive away intruding mongoose groups,
To illustrate the richness of a multidimensional and warn others of a predator’s approach. If a subordi-
approach, let’s consider the dwarf mongoose (Helogale nate female does give birth, she will nurse the young of
parvula)—an appealing and active animal that has some the top-ranking female along with her own, even
very unusual behavior. Dwarf mongooses are the small- though she has fewer young than the dominant female.
est African carnivores (meat eaters), weighing only The efforts of these helpers allow the breeders to raise
300–340 g (11–12 ounces) and only about 43 cm (16 in.) more offspring than they could without help: in fact,
long, half of which is tail (Figure 1.2). unaided breeding pairs are almost never able to raise
their offspring to independence.
What makes dwarf mongooses so unusual is that
they live in social groups. Mongoose packs have around In Chapter 4 we will explore in detail how natural
9 adults and yearlings (Creel and Waser 1994; Rood selection works, but even without more in-depth back-
1990), but may contain up to 40 individuals. Because we ground you can easily imagine why the observation that
are such social creatures ourselves, sociality may not mongooses give up some of their own chances to have
strike us as particularly unusual, but in fact it is quite offspring in favor of helping others is intriguing to ani-
rare. Most carnivores, in fact, are solitary and find each mal behaviorists. This raises a host of “how” and “why”
other only when it is time to mate. questions that involve both the mechanism and the evo-
lution of behavior. Let’s begin by examining some ques-
Dwarf mongooses don’t simply live as close neigh- tions about evolution.
bors, but they take social behavior to an extreme: most
of the breeding is done by a dominant female (reviewed Evolutionary Questions
in Creel 2005). Over 70% of the pregnancies in one About Dwarf Mongoose Behavior
long-term study area were by dominant females. The
top-ranking female also gets priority access to food and When we study the evolution of behavior, we can take sev-
initiates any movements that the pack undertakes. The eral different approaches. First, we can ask about the cur-
rest of the pack falls into a dominance hierarchy, each rent costs and benefits of a behavior. Evolution, as we will
with their own place in the chain of command. see later in the book, is all about reproductive success, so
an evolutionary approach to asking questions about mon-
In spite of the fact that subordinate animals low in goose behavior concerns how behavior affects the pro-
the hierarchy rarely get to personally breed, they help duction of offspring. We can also look deeper into history,
and study how a behavior first originated in mongoose
FIGURE 1.2 The dwarf mongoose lives in groups in ancestors.
which the members cooperate in raising the young.
The dominant male and female are often the only First let’s think about why dwarf mongooses might
group members that breed. Reproduction by other currently benefit from living in groups. If you have been
group members is usually suppressed. However, other lucky enough to watch dwarf mongooses in the wild or
high-ranking individuals are sometimes allowed to in a zoo, one of the behaviors you will notice is their con-
breed. The variability of reproductive suppression stant vigilance—they stand on their tiptoes and peer
raises many “why” questions. The answers illustrate alertly around. Their seeming paranoia is justified: dwarf
the interaction of physiological, behavioral, and evolu- mongooses are small and thus an appetizing prey for
tionary mechanisms. many other carnivores. This leads us to a hypothesis for
why dwarf mongooses live in groups: to reduce the risk
of predation. And in fact, researchers have found that by
living in groups, dwarf mongooses benefit by each other’s
vigilance and by sheer safety in numbers (if a predator
is going to grab a single mongoose and run off, it’s bet-
ter to be in a group than all alone). More than half of
mongooses that venture off on their own are eaten.

Are there costs to being in a group? Certainly. As we
discuss in Chapter 19, being in a group means facing
competition for all sorts of resources. For dwarf mon-
gooses, however, sharing one particularly important
resource is not a problem—food. Dwarf mongooses feed
primarily on arthropods—crickets, grasshoppers, ter-
mites, spiders, and scorpions—and there are plenty to go
around. So, one of the biggest potential problems with
being in a group isn’t too important for dwarf mongooses.

4 Chapter 1 / Introduction

So, there are plenty of advantages to being in a group behavior. For example, we can ask a simple question:
for dwarf mongooses. But what about those subordinates which characteristics make an animal likely to be dom-
that don’t get to reproduce much, if at all, in a group? Do inant? In one study, the dominant female was without
the costs of losing the chance to reproduce outweigh the exception the oldest in a pack. Within an age class,
benefits of being in a group? Let’s approach this question heavy mongooses were more likely to be dominant
in a way animal behaviorists often do: let’s carefully out- (Creel 2005).
line the choices available to a subordinate mongoose. One
option is to leave the original pack with a few other sub- We can also ask more complex and interesting ques-
ordinates and together form a new pack, where it may tions about the interactions among mongooses in a pack.
rank higher in the hierarchy. Or it can go off and try to Up until now, you may have the impression that subor-
join an already existing pack—the chances of a new immi- dinate mongooses quietly give up their reproductive
grant getting an opportunity to breed are fairly good, capabilities, but in fact reproduction is a point of con-
especially if the incoming mongoose manages to drive off tention. Dominant mongooses can reproductively sup-
the resident breeders (Rood 1990). However, the prob- press subordinates (Creel et al. 1992, 1995).
lem with either of these choices is that half of dispersers
die in the process, generally getting eaten by predators. In general, reproductive suppression can be accom-
plished through either chemical or behavioral means. In
Alternatively, a subordinate can stay in the pack and the first way, chemicals released by dominant individu-
hope for an improvement in its social rank, either by als, perhaps in urine or feces, suppress reproductive
slowly gaining status over its lifetime or by benefiting development or function in subordinates. In the second
from a tragedy that befalls the dominant mongoose. In way, dominant individuals behave aggressively toward
addition, subordinates do have some chance at breeding subordinates who attempt to breed. Sometimes both
themselves. In one study, 12% of subordinate mongooses chemicals and aggressive behavior play a role.
became pregnant, and DNA fingerprinting revealed that
15% of the offspring in a pack had subordinate mothers Reproductive suppression in male and female dwarf
and 25% had subordinate fathers (Keane et al. 1994). mongooses involves different mechanisms (Creel et al.
The chances of subordinates getting to reproduce are 1992). In males, reproductive suppression of subordi-
especially good when extra food is around, as researchers nates is accomplished entirely through behavioral means.
have shown by providing food supplements. (Creel and The dominant male attacks other males to keep them
Waser 1997). Finally, even dwarf mongooses that don’t from mating with fertile females. Levels of androgens
breed can help their genes pass on to the next genera- (male hormones) of subordinate and dominant males are
tion by helping to raise their relatives. Thus, for any indistinguishable. In females, suppression can occur
given mongoose, the current costs and benefits of its dif- through hormonal as well as behavioral controls. The
ferent options may vary, and indeed different individu- ability to breed depends on the female’s peak level of the
als make different choices. hormone estrogen. Low-ranking subordinates have low
estrogen levels compared to the breeder. However, high
Using a different set of techniques, we can also ranking, older subordinates have estrogen levels similar
investigate the evolutionary origins of dwarf mongoose to that of the breeder, and have a better chance of breed-
social behavior. As we will see in many other examples ing if they disperse. As a result, the top-ranking female
later in this book, to study evolutionary origins usually must ease her behavioral suppression of the older
involves the construction of a phylogeny, sort of a fam- females to keep them as helpers.
ily tree of a taxonomic group. Usually we are not fortu-
nate enough to have a good fossil record, so we have to Why might both kinds of reproductive suppres-
use other techniques. Veron et al. (2004) used both gene sion evolve for females but not for males? The answer
sequences and behavioral traits of the 37 species of mon- may lie in the certainty of parentage and the ultimate
gooses that are alive today in order to construct a phy- means of suppressing reproduction by subordinates—
logeny. Their work suggests that the ancestor of infanticide. The top female is likely to be able to iden-
modern-day mongooses was solitary, lived in a forest, tify her own offspring by odor cues learned at the time
and ate vertebrates. When the environment changed of birth. However, the young of a single litter can have
during the Pliocene, some mongoose lineages switched different fathers, so a male cannot easily determine
to eating insects. Insectivory made sociality more likely which of them are his. If resources become too scarce
because competition for food was reduced. to support the young of a subordinate, a dominant can
kill them. Because a female can recognize her own
Proximate Questions young, she can selectively kill those of subordinates. A
About Dwarf Mongoose Behavior dominant male practicing the same infanticidal policy
would risk killing some of his own offspring. So, a top-
Besides questions about current costs and benefits and ranking female will allow reproduction of subordinate
the evolutionary history of mongoose social behavior, females who are most likely to leave and breed else-
we can also ask about the mechanisms that underlie the where because she can veto that decision later if need
be. Thus, the variation in reproductive suppression in

Hypothesis Testing 5

dwarf mongooses results from an interplay between FIGURE 1.3 Male burrowing owls scatter mammal
the mechanisms that control it and evolution. manure around the entrance of their nest. There are
at least four alternative hypotheses for this behavior:
The dwarf mongoose studies illustrate the extent to attracting mates, signaling that the nest burrow is occu-
which proximate and ultimate questions about behavior pied, camouflaging the scents of an active owl nest, and
are intertwined. In the pages that follow, we will consider attracting prey. A different set of predictions accompa-
aspects of the behavior of other species in light of all four nies each hypothesis, and each prediction can be tested.
of Tinbergen’s questions. First, we will introduce some
of the approaches to the study of animal behavior—
genetics, evolution, ecology, learning, neurobiology,
endocrinology, and development. We will discuss some
of the basic principles and techniques used in each
approach. Then, in the chapters that follow, we will con-
sider specific types of behavior, including orientation,
foraging, antipredator defense, mating, parental care,
and other social behavior, and see how the various per-
spectives may act synergistically to broaden our under-
standing of animal behavior. Before we begin, however,
we should take a moment to consider how scientists pose
questions about animal behavior and then go about
answering them.

HYPOTHESIS TESTING The observation of manure scattered around the
nest entrance prompts the question, “What is the func-
The study of animal behavior usually begins with an tion of manure around the nest opening?” Matthew
observation that prompts a question, which is followed Smith and Courtney Conway (2007) developed and
by forming hypotheses (logical guesses) about a possi- tested several hypotheses to answer this question.
ble answer. It is necessary to be able to test each hypo-
thesis. Generally, the hypothesis leads to a prediction, Mate attraction The first hypothesis was that males
which will support the hypothesis if it holds true when scatter manure to attract females. Perhaps females
tested. Depending on the hypothesis, the test may use the manure to assess a male’s quality, much like
involve further observations, comparisons of behavior female bowerbirds use the objects in a male’s bower
among species, or experimental manipulation. to assess his quality. Only males scatter manure,
which is consistent with the hypothesis that the
Different hypotheses can sometimes lead to identi- manure attracts females.
cal predictions, and then both hypotheses are supported
or refuted, depending on the outcome of the test. In this Sign that burrow is occupied Suitable nest sites
event, it is necessary to make other predictions that will are limited, and resident males defend their site vig-
allow us to reject one of the hypotheses. orously. Perhaps the manure signals to other males
that the burrow is occupied. Nonresident males
There may also be alternate hypotheses to explain could then avoid the costs of fighting by looking
a particular behavior. If so, each hypothesis could lead elsewhere for a burrow.
to different predictions, and each prediction would be
tested by observations and experiments. Olfactory camouflage Common predators of bur-
rowing owls include coyotes, badgers, and skunks,
Studies of an unusual nesting practice of burrowing which are predators that use odors to locate prey.
owls provide an example of an observation leading to By masking the scents of an active owl nest, the
several hypotheses for the function of the behavior. manure may reduce the risk of predators detecting
Burrowing owls (Athene cunicularis) live and nest in desert the owls within.
grasslands in Canada, the western United States, and
some parts of South America (Figure 1.3). The male pre- Prey attraction Burrowing owls eat what is avail-
pares the underground nest burrow by digging and able: mice, voles, toads, small birds, insects, spiders,
scraping out dirt or by taking over a burrow of another and centipedes. Indeed, small arthropods make up
small mammal, such as a prairie dog or kangaroo rat. a large part of their diet. Perhaps the manure attracts
The unusual part of nest building is that the male lines small arthropods to the owl nest, creating a home-
the tunnel leading to the nest cup with 3 to 7 cm of delivery service for owl nestlings.
mammal manure and then scatters manure around the
entrance to the nest. As you can see in Table 1.1, a different set of predic-
tions accompanies each of these hypotheses, and each

TABLE 1.1 Hypotheses, Predictions, and Tests of the Function of Ma

Prediction Hypothesis Hypothesis Hypothesis Hypothesis
1: Mate 2: Burrow 3: Olfactory 4: Prey
attraction occupied Camouflage attraction

1. Stage of nesting Before pair Soon after Just before All stages
cycle when manure is
collected should be: formation arrival incubation

2. Presence of manure Yes/no Yes No No

at traditional nest before

owls return from

migration discourages

nesting by other owls

3. Increased Yes/no Yes No No

perception of

competition

increases manure

scattering

6

4. More surviving young No No No Yes
at nests with manure

5. Fewer predatory attacks No No Yes No
in natural nests with
manure

6. Fewer predatory attacks No No Yes No
in artificial nests with
manure

7. Greater arthropod No No No Yes

biomass in nests with

manure

anure Scattering by Burrowing Owls

Test Result Conclusion

Estimated date of pair Scattering began after Contradicts mate-
attraction, burrow-
bond formation and dates pair bond formation occupied, and olfactory
camouflage hypotheses
of manure scattering Pattern in direction of
burrow-occupied
Scatter manure around 58% of nests with manure hypothesis but results
entrance of some burrows; became nests; 78% of are not statistically
remove manure from nests with removed significant
some burrows of previous manure became nests Pattern in direction of
years prediction of burrow-
occupied prediction but
Experimental group = Resident male more likely results are not statistically
presented with mount of to attack an owl mount significant
burrowing owl and tape than starling mount;
of its primary call; control Increased scattering Supports prey-attraction
group = presented with after presentation of owl hypothesis
mount of European mount than of European Contradicts olfactory-
starling of its primary call; starling camouflage hypothesis
Measure amount of Contradicts olfactory-
manure spread camouflage hypothesis

Count number of Manure at entrance of nest Contradicts olfactory-
surviving offspring in made no difference in the camouflage hypothesis
manure-supplemented and number of surviving young
manure-removed nests Supports prey-attraction
hypothesis
Select active nests and add Probability of predatory

or remove manure attacks was not altered

by treatment

Probability of predatory
attacks was not altered
by treatment

Compare biomass of Pitfall traps with manure
arthropods at nest sites collected more arthropod
with and without manure biomass than did pitfall
and pitfall traps with and traps without manure
without manure

Hypothesis Testing 7

prediction can be tested. For example, each hypothesis played for ten minutes or until the resident male attacked
makes a different prediction about the timing of manure the mount. Before the first presentation of calls, all scat-
scattering. If the manure attracts a mate, then one would tered material was removed from around the burrow
predict that manure should be present before pair bond- entrance. After the third presentation, all scattered mate-
ing occurs. However, if the manure signals that the bur- rial was again collected and weighed. As predicted by the
row is occupied, then one would predict that manure burrow-occupied hypothesis, resident males were more
should be scattered soon after the owls return from migra- likely to attack a mount of a burrowing owl, which would
tion, well before pair bonding. On the other hand, if be perceived as a threat, than they would a European
manure masks the odor of the owl nest to lower the risk starling mount. Furthermore, after three presentations
of predation, then one would predict that manure scat- of a burrowing owl mount, resident males scattered more
tering occurred later, just before incubation. If the func- manure than they did after three presentations of a
tion of manure is to attract arthropod prey, then one European starling mount. However, once again, these
would predict that scattering should increase after pair results are in the right direction but are not statistically
formation and be most common when nestlings are pre- significant. Recall that the third prediction, that manure
sent in the nest. scattering will begin soon after arrival at the nesting site,
was not met; manure scattering actually occurred several
The obvious test of these predictions is to find out weeks after arrival.
when manure scattering takes place. The usual course of
events is that single males arrive at the nesting grounds The olfactory-camouflage hypothesis predicts that
first, followed by previously mated pairs, and finally sin- the amount of manure scattered around the burrow
gle females. Pair bonding occurs when the females entrance will influence the risk of predation. Smith and
arrive. The female incubates seven to ten eggs for 28 to Conway tested this prediction on active natural nests and
30 days until they hatch. She continues to sit on the on artificial nests. They randomly selected 26 active nest
brood for another week or two. During this entire time, sites and added or removed manure from the nest
the male brings food to the nest. For about the next six entrances every two to four days. The artificial nests
weeks, both adults feed the young until they can hunt for were created by baiting unoccupied burrows with
themselves. chicken eggs and assigning each to one of four treat-
ments: horse manure and signs of owls, such as feathers
Smith and Conway (2007) observed burrows every and pellets; coyote scat plus signs of owls; no manure or
two to four days to determine the number of adults and scat but signs of owls; no manure or scat or signs of owls.
juveniles present, when manure scattering took place, If the manure at the nest entrance functions to hide the
and whether any owls were killed by predators. In 87% scent of an active owl nest, then one would predict less
of the 46 observed burrows, manure scattering occurred predation on natural or artificial burrows with manure
after pair bond formation, which is inconsistent with the or scat around the entrance. This prediction was not sup-
mate-attraction and burrow-occupied hypotheses and ported; there was no difference in the probability of pre-
best fits the prey-attraction hypothesis. dation between nests with manure and those without
manure.
The burrow-occupied hypothesis predicts that a
nonresident male would be less likely to enter a bur- The first prediction of the prey-attraction hypo-
row if manure was scattered at the entrance. To test this thesis is that manure attracts small arthropod species that
prediction, Smith and Conway added or removed burrowing owls typically eat. To test this prediction,
manure from burrows that had been used in the previ- Smith and Conway created 75 sampling areas, each con-
ous two years. They visited the nests twice a week to taining two treatment sites—one with manure and a con-
see which nests were used. Whereas 78% of the nests trol without manure. Each sampling area also contained
from which manure had been removed became nests, three pitfall traps to collect any small arthropods that
only 58% of the burrows with added manure became were attracted to and approached the treatment site. As
nests. This result is not statistically significant, but is predicted, the average biomass (dry weight) of arthro-
in the direction that would be predicted by the hypoth- pods collected was higher at manure sites.
esis that the manure functions as an indicator that the
burrow is occupied, suggesting that it is biologically If more small arthropods are attracted to nests with
meaningful. more manure, it follows that a second prediction of the
prey-attraction hypothesis is that manure increases the
A second prediction of the burrow-occupied survival rate of nestlings by attracting arthropods to sup-
hypothesis is that the amount of manure scattered would plement the food brought to the nest by the parents. The
increase with perceived competition. Smith and Conway data do not support this prediction. There was no sig-
tested this prediction by presenting each resident male nificant difference in the number of young surviving in
with a mount of a burrowing owl accompanied by a nests with or without manure. Furthermore, there were
recording of its primary call and, separately, a mount of slightly more survivors in nests without manure, which
a European starling accompanied by a recording of its is in the opposite direction of the prediction.
primary call. On three separate occasions, the calls were

8 Chapter 1 / Introduction

These studies point out the usefulness of testing their nesting behavior in general and about the function
alternate hypotheses and alternate predictions from a of manure scattering in particular may provide insight
single hypothesis. The data do not support the hypoth- into whether or how the disappearance of large grazing
esis that scattered manure functions to attract a mate. mammals from prairies has caused the owl population to
Other data, though not statistically significant, suggest decline (Smith and Conway 2007). A study performed in
that manure may function as a sign that a burrow is occu- Oklahoma revealed that the declining population of bur-
pied: burrows with manure were 36% less likely to rowing owls is related to the elimination of prairie dogs
become nests than burrows without manure, and the (Cynomys ludovicianus). In this region of the country, most
perception of competition increased manure scattering burrowing owls made nests in abandoned prairie dog
by resident males. Although the timing of manure scat- burrows. Unfortunately, prairie dogs are not welcomed
tering fits the olfactory-camouflage hypothesis, the fail- guests on many ranches because they eat some of the
ure of manure to increase survival of the young does not. available food and because their burrow holes may pose
The hypothesis that the function of manure scattering a risk to livestock. As prairie dogs disappear, so do their
is to attract prey to the nest burrows is supported by both burrows. Fewer prairie dog burrows mean fewer nesting
the timing of manure scattering and the increased burrows for burrowing owls, so their numbers are also
amount of prey biomass trapped near nests with manure declining. To increase the number of burrowing owls, it
compared to nests without manure. However, the num- would seem that the prairie dog population must also be
ber of young surviving in nests was not increased by the maintained (Butts and Lewis 1982).
presence of manure, which does not at first appear to be
consistent with the prey-attraction hypothesis. But per- In the pages that follow, we will explore various per-
haps attracting prey to the nest allows juveniles to learn spectives on animal behavior, sometimes stopping to
to handle prey near the safety of the burrow, or perhaps consider how the information might be used to serve
attracting prey to the nest means that the parents can animal welfare or conservation. We will also see many
make fewer foraging trips. examples of hypothesis testing. Keep these general pro-
cedures in mind as you read them. Instead of passively
STOP AND THINK accepting the given explanation for a particular behav-
ior, be critical of the evidence. Try to think of alternate
Some males use materials such as feathers, grass, or dried hypotheses for the behaviors described. Make predic-
moss to scatter at the nest entrance. Which hypothesis or tions and design your own tests of those predictions.
hypotheses would be consistent with this observation?
SUMMARY
STOP AND THINK
Animal behavior is studied for many reasons, both prac-
There are other possible hypotheses for the function of tical and intellectual. A full understanding of animal
manure scattering at the nest entrance by male burrow- behavior requires answers to four types of questions,
ing owls. Mammal manure is abundant in areas where those about (1) immediate mechanisms, (2) development,
burrowing owls nest, so perhaps manure is good nest- (3) survival value, and (4) evolution. Our progress in
building material, and some gets dropped around the understanding the behavior of animals will be enhanced
entrance by sloppy males. Perhaps manure serves as insu- by considering all four types of questions.
lation or absorbs water to prevent flooding in the nest.
How would you test these hypotheses? Can you think of The study of animal behavior usually begins with an
others? How would you test them? observation that prompts a question. The next step is to
think of tentative explanations, called hypotheses, to
Populations of burrowing owls are declining so pre- answer that question. Each hypothesis should produce
cipitously that they are listed as endangered in some testable predictions. The tests of those predictions sup-
states and as threatened in others. Learning more about port or refute the hypothesis.

PART ONE

Approaches to the Study
of Animal Behavior

9

This page intentionally left blank

2

History of the Study
of Animal Behavior

The Beginnings THE BEGINNINGS
Intellectual Continuity in the Animal World
Darwin’s Evolutionary Framework INTELLECTUAL CONTINUITY
IN THE ANIMAL WORLD
Classical Ethology
The Approach: Evolutionary, Comparative, Descriptive, It is difficult, perhaps impossible, to pinpoint the precise
Field-Oriented beginnings of the study of animal behavior. Rather than
Classical Ethological Concepts attempting this feat, we will simply consider some of the
highlights in the development of the discipline. One
Comparative Psychology idea, that of intellectual continuity among animals, was
The Approach: Physiological, Developmental, important in shaping some of the earliest views of ani-
Quantitative, Laboratory-Oriented mal behavior. Although the idea of intellectual continu-
Early Concepts of Comparative Psychology ity was summarized in 1855 by Herbert Spencer in his
The Roots of Physiological Psychology book Principles of Psychology (Spencer 1855), its roots can
be traced back much further in history, to the ideas of
Sociobiology and Behavioral Ecology the ancient Greek philosophers. The concept focused on
More Recent Trends continuity in mental states between “lower” and
“higher” animals and was based on a picture of evolu-
Field Studies tion similar to Aristotle’s scala naturae, the great chain of
Cellular and Molecular Basis of Behavior being. In the scala naturae, the evolution of species was
Behavioral Biology viewed as linear and continuous. This classification sys-
Applied Animal Behavior tem was hierarchical, with animals ranked according to
their degree of relationship, the highest point of evolu-
To understand a field of study today, we must know tion being humans (Hodos and Campbell 1969). At the
something about its past. In this chapter, we consider the bottom of the scale were creatures such as sponges; then
history of the study of animal behavior. Our focus is on further up the scale were insects, fish, amphibians,
the development of key concepts in the field.

11

12 Chapter 2 / History of the Study of Animal Behavior

reptiles, birds, nonhuman mammals, and finally humans. based variation in their behavior, morphology, physiol-
Because evolution was seen as a linear process, with each ogy, and so on. Evolutionary change occurs as the her-
higher species evolving from a lower one until, finally, itable traits of successful individuals (i.e., those that
humans emerged, it was thought that the animal mind survive and reproduce) are spread throughout the pop-
and the human mind were simply points on a continuum. ulation, whereas those traits of less successful individu-
als are lost.
DARWIN’S EVOLUTIONARY
FRAMEWORK In two later books, The Descent of Man, and Selection
A few years after the publication of Spencer’s book, in Relation to Sex (1871) and Expression of the Emotions in
Charles Darwin (Figure 2.1) published his thoughts on Man and Animals (1873), Darwin applied his evolution-
evolution by natural selection in On the Origin of Species ary theory to behavior. In these volumes he recorded his
(1859). Although Darwin’s focus in this book was not on careful and thorough observations on animal behavior,
animal behavior, his ideas provided a conceptual frame- but his records were anecdotal and often anthropomor-
work within which the field of animal behavior could phic. This was not, however, sloppy science. In the tra-
develop. Discussed in more detail in Chapter 4, these dition of his day, he believed that careful observations
ideas can be briefly summarized as follows: were useless unless they were connected to a general the-
1. Within a species, there is usually variation among ory. Darwin’s general theory was evolution by natural
selection. Because humans evolved from other animals,
individuals. he considered the minds of humans and animals to be
2. Some of this variation is inherited, and is passed on similar in kind and to differ only in complexity. As a
reflection of this belief, he described the behavior of ani-
from mother to offspring. mals by using terms that denote human emotions and
3. Most of the offspring produced by animals do not feelings: Ants despaired, and dogs expressed pleasure,
shame, and love. Darwin’s opinion was influential, and
survive to reproduce. Some individuals survive it is not surprising that others interested in animal behav-
longer and produce more offspring than others, ior followed his lead. Both ethologists and comparative
because of their particular inherited characteristics. psychologists trace the beginnings of their respective
Natural selection is the differential survival and fields to the ideas of Darwin.
reproduction of individuals that results from genetically
For about a decade after the publication of Expression
FIGURE 2.1 Charles Darwin. His ideas on evolution by of the Emotions in Man and Animals (1873), descriptions
natural selection provided an evolutionary framework of animal behavior usually took the form of stories about
for the study of animal behavior. the accomplishments of individual animals that were
believed to think and experience emotions as humans do.
For example, based on his subjective interpretation of
what he observed, George J. Romanes, a protégé of
Darwin, constructed a table of emotions that charted the
evolution of the mind and listed the emotions in order
of their historical or evolutionary appearance (Figure
2.2). In his books, Animal Intelligence (1882), Mental
Evolution in Animals (1884), and Mental Evolution in Man
(1889), Romanes examined the implications of
Darwinian thinking about the continuity of species for
the behavior of nonhuman and human animals.

In addition to Romanes, several other scientists
made notable contributions to the study of animal
behavior at the turn of the twentieth century. Jacques
Loeb (1918) believed that all patterns of behavior were
simply “forced movements” or tropisms, physiochemi-
cal reactions toward or away from stimuli. Herbert
Spencer Jennings, perhaps best known for his book
Behavior of the Lower Organisms (1906), disagreed with
Loeb’s ideas and instead emphasized the variability and
modifiability of behavior. Of course, there were many
other pioneers in the study of animal behavior, but we
will move on to the turmoil that developed in the disci-
pline during the twentieth century.

Classical Ethology 13

Emotion Animals in which where variables could be controlled. Finally, ethologists
emotion first appears were interested in differences between the species,
whereas comparative psychologists searched for general
Shame, deceit Apes, dogs “laws” of behavior.

Revenge, anger Monkeys, elephants Of course there were many exceptions to this char-
acterization. Some ethologists made remarkable discov-
Grief, hate, cruelty Emotional development Carnivores, rodents eries indoors in their homes and laboratories and
explored the influence of experience on behavioral devel-
Pride, resentment Birds opment (Barlow 1989), and some comparative psychol-
ogists studied a wide range of species and patterns of
Sympathy Ants, bees, wasps behavior and conducted their studies in the field
(Dewsbury 1989). Indeed, within each field there were
Affection Crustaceans individuals interested in all four questions of animal
behavior. Although traditionally ethology and compar-
Jealousy, anger Fish ative psychology have been portrayed as very different
approaches, some accounts of the history of animal
Pugnacity, industry, curiosity Insects, spiders behavior have tended to downplay the differences
between them (e.g., Dewsbury 1984).
Sexual feelings Molluscs
CLASSICAL ETHOLOGY
Surprise, fear Larvae of insects,
segmented worms THE APPROACH: EVOLUTIONARY,
COMPARATIVE, DESCRIPTIVE, FIELD-
FIGURE 2.2 The ideas of George J. Romanes on the ORIENTED
evolutionary appearance of emotions in animals.
(Modified from Romanes 1889.) “Why is that animal doing that?” is perhaps the funda-
mental question of ethology, the approach to the study
As interest in animal behavior grew, differences in of behavior founded largely by Konrad Lorenz, Niko
opinion developed. These differences eventually led to Tinbergen, and Karl von Frisch, European zoologists
the development of two major approaches to the study who shared the Nobel Prize in medicine and psychol-
of animal behavior, ethology and comparative psychol- ogy in 1973 (Figure 2.3). Traditionally, ethology con-
ogy, centered in Europe and the United States, respec- centrated on the evolutionary basis of animal behavior.
tively. The split that developed between the two Because natural selection can act only on traits that are
approaches seemed at times quite severe. Indeed, one genetically determined, it seems a logical outcome of the
must wonder why two groups of scientists, each striving ethologists’ basic interest in the evolution of behavior to
for a greater understanding of the marvels of animal focus on those behavior patterns that are inherited. An
behavior, could have stood worlds apart. The European emphasis on phylogeny (the evolutionary history of a
ethologists and the American comparative psychologists species) is particularly characteristic of the work of
were separated by more than the Atlantic Ocean. In fact, Konrad Lorenz.
the basic questions they asked about animal behavior
were different. (Recall from Chapter 1 that the four The studies of ethologists often involve comparisons
questions outlined by Niko Tinbergen in 1963 con- among closely related species. In the words of Lorenz
cerned the mechanism, function, development, and evo- (1958), “Every time a biologist seeks to know why an
lution of behavior.) Whereas the ethologists focused organism looks and acts as it does, he must resort to the
their attention on the evolution and function of behav- comparative method.” Here Lorenz was referring to the
ior, the comparative psychologists concentrated on the method employed by comparative anatomists when they
mechanism and development of behavior. Because they ask the same question about morphology. If comparative
asked different questions, the types of behavior they anatomists were to ask why a whale’s flipper is structured
studied and even their experimental organisms differed. as it is, they might compare the skeleton of the flipper
Whereas ethologists, by and large, studied innate behav- with that of the forelimb of other vertebrates. They
ior in birds, fish, and insects, comparative psychologists, could then see that the typical vertebrate forelimb has
particularly those of the behaviorist school (see discus- been specialized for the aquatic life of this mammal.
sion later in chapter), emphasized learned behavior in Similarly, if one were to wonder why a male fly of the
mammals such as the Norway rat. Furthermore, to species Hilara sartor spins an elaborate silken balloon to
determine the normal function of a behavior, ethologists
often attempted to observe the animal in its natural habi-
tat or in environments designed to simulate that habi-
tat. On the other hand, comparative psychologists
believed that learning was best studied in the laboratory,

14 Chapter 2 / History of the Study of Animal Behavior

present to a female before mating (Figure 2.4), the sig- place food inside cocoons; others enclose something
nificance of the behavior would become apparent after meaningless, such as a daisy petal. Finally, the males of
comparing it with the mating behavior of the other H. sartor present the females with an empty gauze case
species of flies in the family Empididae. Let us consider that turns off the predatory behavior of the female,
the gift-giving behavior of H. sartor in more detail to thereby allowing them to mate (Kessel 1955). Long-
illustrate the ethologist’s comparative method. tailed dance fly males (Rhamphonyia sulcata) usually offer
a female a genuine nuptial gift. Natasha LeBas and Leon
Among the empidid flies are species that display
almost every imaginable evolutionary step in the pro-
gression toward the balloon display. By observing the
manner in which the male empidid fly approaches the
female for mating, one sees that at the heart of the prob-
lem is the fact that the male may be a meal, rather than
a mate, for the predacious female. In one species, Empis
trigramma, the male approaches the female while she is
eating. Because her mouth is already full, his well-timed
approach increases his chances of surviving the
encounter. In another species, E. poplitea, the male cap-
tures a prey, perhaps a fly, and gives it to the female, pro-
viding her with a meal before attempting to copulate.
Males of the species H. quadrivittata gift-wrap the meal
in a silky cocoon before offering it to the female. In
another species, H. thoracica, the cocoon, or case, is large
and elaborate, but the food inside is small and of little
value. In yet another species, H. maura, only some males

FIGURE 2.3 Konrad Lorenz (above), Niko Tinbergen
(top right), and Karl von Frisch (right), three ethologists
who shared the Nobel Prize in 1973.

Classical Ethology 15

Female Male
Female
Male

FIGURE 2.4 Male flies of the species Hilara sartor present females with an empty silken bal-
loon before mating. The evolution and function of this behavior can be understood by com-
paring the behavior of closely related species, that is, by using the comparative method
characteristic of the ethological approach. (Drawn from descriptions in Kessel 1955.)

Hockham (2005) altered the gift by filling it with a large these patterns of movement to be just as reliable as mor-
prey, small prey, or a worthless nonedible token. phological characters in defining a particular group.
Although females did copulate longer with males offer-
ing the largest prey, the females copulated for the same The stereotyped patterns of behavior that intrigued
amount of time with males bearing small prey and those ethologists such as Whitman, Heinroth, and Craig were
bearing token gifts. Thus, male cheaters can invade the named fixed action patterns by Lorenz. By definition, a
population. Without a comparison of the behavior with fixed action pattern (FAP) is a motor response that is
that of other species, an observer would be hard pressed initiated by some environmental stimulus but that can
to explain why males offer silken balloons to females. continue to completion without the influence of exter-
nal stimuli. For example, Lorenz and Tinbergen (1938)
In addition to utilizing the comparative method, showed that a female greylag goose (Anser anser) will
ethologists often work in the field rather than in the lab- retrieve an egg that has rolled just outside her nest by
oratory. After all, they reason, it is in the natural setting reaching beyond it with her bill and rolling it toward her
that the normal context in which the behavior is dis- with the underside of the bill (Figure 2.5). If the egg is
played is apparent. From this setting, the function of the experimentally removed once the rolling behavior has
behavior may be deduced, and knowledge of the func- begun, the goose will continue the retrieval response
tion may allow us to understand why the behavior has until the now imaginary egg is safely returned to the
been shaped to its present form by natural selection. nest. We have emphasized the fact that once initiated,
Tinbergen and his students conducted much of their FAPs continue to completion. There is little consensus,
research in the field. Lorenz and his followers, on the however, on their defining attributes. Other character-
other hand, studied captive animals, but they often istics that have been used to describe them include the
attempted to simulate in captivity some characteristics of following: (1) the sequence of component acts of an FAP
the animal’s natural habitat (Barlow 1991). As we will see is unalterable, (2) an FAP is not learned, (3) it may be
in Chapter 16, von Frisch’s carefully designed field triggered under inappropriate circumstances, and (4) it
experiments reveal that scout honeybees communicate is performed by all appropriate members of a species
the distance and direction of a rich food source to (Dewsbury 1978).
recruits by “dancing” within the hive.
The concept of a fixed action pattern was questioned
CLASSICAL ETHOLOGICAL CONCEPTS in the years following Lorenz’s first introduction of the
term. George Barlow (1968) suggested that, in reality,
The Fixed Action Pattern most patterns of behavior are not as stereotyped as the
notion of the FAP suggests, and furthermore, most can-
At the turn of the twentieth century, Charles Otis not easily be separated into fixed and orientation com-
Whitman of the University of Chicago and Oskar ponents. He suggested the alternative term modal action
Heinroth of the Berlin Aquarium were pioneering the pattern (MAP). In specific cases, however, the term fixed
field of ethology (Lorenz 1981). Both scientists were action pattern may be appropriate. Finley and colleagues
interested in the behavior of birds, and each indepen- (1983) examined the courtship displays of mallard ducks
dently concluded that the displays of different species are (Anas platyrhyncos) and concluded that the patterns of
often exceptionally constant. In fact, they considered behavior were indeed as highly stereotyped as suggested
by the notion of FAP. We will continue to use the

16 Chapter 2 / History of the Study of Animal Behavior

FIGURE 2.5 The egg retrieval response of the greylag goose. The chin-tucking move-
ments used by the female as she rolls the egg back to the nest are highly stereotyped
and are an example of a fixed action pattern. The side-to-side movements that correct
for any deviations in the path of the egg are called the taxis component of the
response. If the egg is removed, the female will continue to roll an imaginary egg back
to the nest. One defining characteristic of a fixed action pattern is that it will continue
to completion even in the absence of guiding stimuli. (Drawn from a photograph in
Lorenz and Tinbergen 1938.)

traditional term here, keeping in mind that there is some The final product is an intricate pattern which etholo-
debate over the appropriateness of its use. gists call a chain of reactions. Here, each component
FAP brings the animal into the situation that evokes the
Sign Stimuli and Releasers as Triggers next FAP.

A fixed action pattern is obviously produced in response One of the earliest analyses of a chain of reactions
to something in the environment. Let’s consider the was conducted by N. Tinbergen (1951) on the courtship
nature of the stimulus that might trigger the behavior. ritual of the three-spined stickleback. This complex
Ethologists called such a stimulus a sign stimulus. If the sequence of behaviors culminates in the synchronization
sign stimulus is emitted by a member of the same species, of gamete release, an event of obvious adaptive value in
it is called a social releaser or, simply, a releaser. species with external fertilization. Each female behavior
Releasers are important in communication among ani- is triggered by the preceding male behavior, which in
mals, as we will see in Chapter 18. Although releasers are turn was triggered by the preceding female behavior
technically a type of sign stimulus, the terms are often (Figure 2.6).
used interchangeably.
A male stickleback in reproductive condition may
Sign stimuli may be only a small part of any envi- sometimes attack a female entering his territory. If the
ronmental situation. For example, a male European robin female does not flee and instead begins to display the
(Erithacus rubecula) will attack another male robin that appropriate head-up posture in which she hangs
enters its territory. Experiments have shown, however, obliquely in the water, exposing her egg-swollen
that a tuft of red feathers is attacked as vigorously as an abdomen, the male will begin his courtship with a zigzag
intruding male (Lack 1943). The attack is not stimulated dance. He repeatedly alternates a quick movement
by the sight of another bird but only by the sight of red toward her with a sideways turn away. This dance
feathers. Of course, in the world of male robins, red releases the approach behavior of the female. Her move-
feathers usually appear on the breast of a competitor. ment induces the male to turn and swim rapidly toward
the nest, an action that entices the female to follow. At
Sign stimuli, simple cues that may be indicative of the nest, he lies on his side and makes a series of rapid
very complex situations, get through to the animal’s ner- thrusts with his snout into the entrance while raising his
vous system, where they release patterns of behavior that dorsal spines toward his mate. This behavior is the
may consist, in large part, of fixed action patterns. For releaser for the female to enter the nest. The presence
example, the attack of the male European robin may be of the female in the nest is the releaser for the male to
composed of FAPs that involve pecking, clutching, and begin to rhythmically prod the base of her tail with his
wing fluttering. The end result is that when an intrud- snout, causing the female to release her eggs. She then
ing male robin appears, it is immediately identified and swims out of the nest, making room for the male to enter
effectively attacked. and fertilize the eggs. At the completion of this ritual,
the male chases the female away and continues to defend
Chain of Reactions his territory against other males until another female can
be enticed into the courtship routine. The male mates
So far we have considered only relatively simple behav- with three to five females and then cares for the devel-
iors, but a great deal of complexity can be added to the oping eggs by guarding them from predators and fan-
behavioral repertoire by building sequences of FAPs. ning water over them for aeration. We see, then, that this

Comparative Psychology 17

2 1 vated than the other (Morris 1958). Such flexibility
Male swims Female appears, begins to make sense when the function for which the
ritual evolved is considered. For the stickleback,
zigzag to gives head-up courtship is important to time the release of the
female display gametes, and thus males and females seem to adjust their
activities so that they are physiologically ready for
3 gamete release at the same time. Despite some flexibil-
Female swims, ity, however, the component behaviors do not occur ran-
domly. In the display, a particular behavior is more likely
head up, to be followed by certain actions than by others.
toward male
COMPARATIVE PSYCHOLOGY
4
Male swims THE APPROACH: PHYSIOLOGICAL,
toward nest DEVELOPMENTAL, QUANTITATIVE,
LABORATORY-ORIENTED
5
Female follows The comparative psychologists’ emphasis on labora-
tory studies of observable, quantifiable patterns of
6 behavior distinguished them from the European ethol-
Male shows nest ogists during the first half of the twentieth century.
Recall that, at this time, many ethologists preferred to
7 study animal behavior under natural conditions. This
Female enters nest meant that they went into the field and observed behav-
ior. The problem was that in the field, the unexpected is
8 expected; one cannot control all the variables. The com-
Male tremble-thrusts parative psychologists argued that good, experimental
science cannot be done under such uncontrolled condi-
9 tions. The ethologists were further criticized because,
Female spawns although they described changes in behavior, they often
neglected to quantify their results and rarely analyzed the
10 data with statistical procedures. Given the psychologists’
Female leaves penchant for laboratory studies that produce quantifiable
results, it is not too surprising that much of their early
11 research focused on learning and the physiological basis
Male enters of behavior. Again, however, we wish to emphasize that
and fertilizes although learning and physiology were popular areas of
study among comparative psychologists, the evolution
FIGURE 2.6 Courtship behavior in the three-spined and function of behavior were also examined by some
stickleback. (From N. Tinbergen, 1989.) of comparative psychology’s practitioners. We will now
consider some of the major conceptual developments in
complex sequence is largely a chain of FAPs, each trig- the field of comparative psychology.
gered by its own sign stimulus, or releaser.
EARLY CONCEPTS OF COMPARATIVE
The chain of reactions is not as rigid as the above PSYCHOLOGY
description of courtship in the three-spined stickleback
implies. There are actually many deviations in the pre- Morgan’s Canon
cise order of the events in the ritual, and some actions
must be repeated several times if one partner is less moti- Recall from our previous discussion of the ideas and
writings of Darwin and Romanes that the early descrip-
tions of animal behavior were often subjective, anthro-
pomorphic accounts. C. Lloyd Morgan helped stop the
anecdotal tradition, thereby helping comparative psy-
chology to become the objective science it is today. He
argued that behavior must be explained in the simplest
way that is consistent with the evidence and without the

18 Chapter 2 / History of the Study of Animal Behavior

assumption that human emotions or mental abilities are a
involved. This idea was crystallized in Morgan’s Canon
(1894): “In no case may we interpret an action as the out- b
come of the exercise of a higher psychical faculty if it can
be interpreted as the outcome of the exercise of one 400
which stands lower in the psychological scale.” In other
words, when two explanations for a behavior appear Time (sec) 300
equally valid, the simpler is preferred. People were urged
to offer explanations of an animal’s behavior without 200
referring to the animal’s presumed feelings or thought
processes. 100

Learning and Reinforcement 0 10 15
10 20 30 40 50 60
We have already mentioned that many of the early com- Trials
parative psychologists focused their research efforts on
learning. The early days of these studies were exciting FIGURE 2.7 (a) A problem box. Thorndike invented
times indeed, and some of the most important work was many “problem boxes” to measure the learning ability
done by scientists in America. E. L. Thorndike (1898), of animals. An animal would be placed inside the box
for example, devised experimental techniques to study and would have to learn how to operate an escape
learning in the laboratory. He was a pioneer in research mechanism. (b) The time required for escape on succes-
on what was called trial-and-error learning, now usually sive trials was a measure of how quickly the animals
called operant conditioning. In operant conditioning, the mastered the task. (From Thorndike 1911.)
animal is required to perform a behavior to receive a
reward. In one series of experiments, Thorndike Pavlov rang a bell immediately before feeding a dog and
invented boxes that presented different problems to ani- found that, in time, the dog came to salivate at the sound
mals. For instance, one problem box was a crate with a of the bell alone (Pavlov 1927). We will discuss classical
trapdoor at the top through which an experimenter conditioning in more detail in Chapter 5.
might drop a cat to the inside of the box. A hungry cat
was left in the box until it accidentally operated a mech- At first, comparative psychologists used operant and
anism, perhaps pulling a loop or pressing a lever that classical conditioning techniques to study the learning
opened an escape door on the side of the box, allowing abilities of a wide variety of species. Thorndike, for
it access to food that had been placed nearby. The length example, examined learning in fish, chickens, cats, dogs,
of time it took for each escape provides an objective, and monkeys and noted striking similarities in the learn-
quantifiable measure of learning progress (Figure 2.7). ing processes of these animals. His results were there-
During repeated trials, the animal became more efficient fore consistent with the idea of intellectual continuity.
and required less time to hit the escape latch. Thorndike concluded that although animals might dif-
Thorndike’s studies led him to develop the Law of fer in what they learned or in how rapidly they learned
Effect, a cornerstone of operant conditioning. His basic it, the process of learning must be the same in all species.
notion was that responses that are rewarded, that is, fol- In his 1911 collection of papers, he summarized his idea
lowed by a “satisfying” state of affairs, will tend to be of intellectual continuity as follows (p. 294):
repeated (this idea was also described by C. Lloyd
Morgan and other investigators of animal behavior). [Intellect’s] general law is that when in a certain situa-
Thorndike began publishing studies on animal intellect tion an animal acts so that pleasure results, that act is
and behavior in the late 1800s, and in 1911 he published selected from all those performed and associated with
a collection of his writings in a book entitled Animal that situation, so that, when that situation recurs, the
Intelligence: Experimental Studies. act will be more likely to follow than it was before. . . .
The intellectual evolution of the race consists of an
Just a few years after Thorndike introduced the idea increase in the number, delicacy, complexity, perma-
of trial-and-error learning, Ivan Pavlov (Figure 2.8), a
Russian physiologist, described the conditioned reflex.
Pavlov noticed that a dog begins to salivate at the sight
of food, and he reasoned that the sight of food must have
come to signal the presence of food. (In science, the key
observations that trigger great ideas are often quite com-
monplace, as in this case. It is not what you observe; it
is what you make of it.) In his well-known experiment,

Comparative Psychology 19

FIGURE 2.8 Ivan Pavlov described a conditioned reflex B. F. Skinner, one of the most famous behaviorists,
in the dog. devised an apparatus that was similar to Thorndike’s
problem box but lacked the Houdini quality. Instead of
nence and speed of formation of such associations. In learning to operate a contrivance that provides a means
man his increase reaches such a point that an appar- of escape, a hungry animal placed in a “Skinner box”
ently new type of mind results, which conceals the real must manipulate a mechanism that provides a small food
continuity of the process. . . . Amongst the minds of reward (Figure 2.9). A rat may learn to press a lever, and
animals that of man leads, not as a demigod from a pigeon may learn to peck at a key. Patterns of behav-
another planet, but as a king from the same race. ior that are rewarded tend to be repeated, or to increase
in frequency, and so learning can be measured as the
Behaviorism number of responses over time. Skinner believed that the
control of behavior was a matter of reinforcement.
Another important event that steered comparative psy-
chology toward objectivity and laboratory analysis was Behaviorists began to see basic principles underly-
the birth of behaviorism, a school of psychology that ing learning that were common to all species. They
restricts the study of behavior to events that can be expected to find similarities in the learning process
seen—a description of the stimulus and the response it because at that time, the minds of all species were con-
elicits. Behaviorists sought to eliminate subjectivity from sidered similar in kind. Thus, according to the tradi-
their studies by concentrating their research efforts on tional view of learning held by the followers of
identifying the stimuli that elicit responses and the behaviorism, the minds of humans and animals were
rewards and punishments that maintain them. This was, similar in kind and differed only in complexity. In short,
indeed, a step toward better science. They designed there were general laws of learning that transcended all
experiments that would yield quantifiable data, invented species and problems. If this was true, then it was rea-
equipment to measure and record responses, and devel- sonable to study the laws of acquisition, extinction, delay
oped statistical techniques that could be used to analyze
behavioral data. The assumptions that an animal’s men- FIGURE 2.9 B. F. Skinner and his apparatus, the Skinner
tal capacity could not be measured directly, but its abil- box. Animals placed in the box learned to operate a
ity to solve a problem could, again focused attention on mechanism to obtain a food reward.
learning ability as a popular research subject. A learned
response could be described objectively, and experiments
could be conducted under the controlled conditions of
the laboratory.

20 Chapter 2 / History of the Study of Animal Behavior

of reinforcement, or any other aspect of the learning basis of learning in the rat. He also examined the role of
process in a simple and convenient animal, such as the the brain in emotion and in vision.
domesticated form of the Norway rat (Rattus norvegicus),
and the results could then be broadly applied to other The comparative psychologist Frank Beach began
species. his career by using brain surgery to determine the effects
of lesions on the maternal behavior of the rat, but he
STOP AND THINK later went on to study the effects of hormones on behav-
ior. He analyzed the roles of nerves, hormones, and
Cancer is a disease that gives off odors. Assume that you experience in the sexual behavior of fishes, amphibians,
are a researcher interested in knowing whether dogs can reptiles, birds, and mammals. We will discuss some of his
detect bladder cancer. What experiment would you work in the field of behavioral endocrinology in more
design? detail in Chapter 7.

THE ROOTS OF PHYSIOLOGICAL Recognizing that animal behavior is concerned with
PSYCHOLOGY the activities of groups of animals, as well as of individ-
uals, some comparative psychologists studied social
Although learning was a dominant focus of research dur- behavior. Robert Yerkes, for example, established a
ing the middle of the twentieth century, it was not the research facility (later named the Yerkes Laboratory of
only research interest of comparative psychologists. Primate Biology) at Orange Park, Florida, to study a
Another research topic was the physiological basis of wide range of behavior in primates. Some researchers
behavior. Part of the psychological foundation of behav- also began to see that although it is often easier to make
ior is, of course, the nervous system. The comparative measurements in the laboratory, it is not impossible to
psychologists’ interest in the neurological mechanisms of get good measurements in the field. C. R. Carpenter
behavior can be traced back to Pierre Flourens, a pro- studied a variety of primate species, each in its natural
tégé of Baron Cuvier, a famous scientist of nineteenth- setting: howler monkeys in Panama, spider monkeys in
century France who stressed the importance of Central America, and gibbons in Thailand, to name a
laboratory research (Jaynes 1969). Flourens earned his few. T. C. Schneirla used both field observation and lab-
reputation for his studies of the relationship between oratory experimentation to investigate the social behav-
behavior and brain structure. For example, he did exper- ior in army ants. In doing so, he applied the rigorous
iments in which parts of the brain were removed, such methodology of laboratory researchers to his field stud-
as the cerebral hemispheres from a pigeon, to look for ies. Such pioneering studies began to help weave the two
the effect on the animal’s behavior. independent sciences of ethology and comparative psy-
chology together.
Karl Lashley was one comparative psychologist who
maintained an interest in physiology, as well as a com- SOCIOBIOLOGY AND
parative base of study, during the years when learning by BEHAVIORAL ECOLOGY
the laboratory rat dominated the field. His attempts to
localize learning in the cerebral cortex resulted in the The field of animal behavior has grown enormously. In
rejection of some hypotheses that were widely accepted the 1960s and early 1970s, for example, field researchers
at the time. For example, based on Pavlov’s ideas, it was such as John Crook (1964; 1970) and John Eisenberg and
assumed that learning depended on the growth or colleagues (1972) suggested that ecological context was
strengthening of neural connections between one part of sometimes a better correlate of social behavior than was
the cerebral cortex and another. To test this idea, Lashley phylogeny (remember that ethologists often focused on
(1950) trained rats on a variety of mazes and discrimi- phylogenetic analyses of behavior). Another dramatic
nation tests and then tried to disrupt the memory by development was the birth of a new discipline that focused
making a cut into the cerebral cortex in a different place on the application of evolutionary theory to social
in each animal. After destroying varying amounts of behavior. This new discipline was called sociobiology.
brain tissue, he would then retest the animals to see if Another discipline, behavioral ecology examines the
their behavior changed. In general, he found that when ways in which animals interact with their environment to
it came to complex problem solving, the entire cerebral learn how behavior contributes to the animal’s reproduc-
cortex was involved, and any particular area was just as tive success and survival. In either case, the key element
important as any other. He also experimentally addressed of this approach is the idea that behavior should, on aver-
questions such as whether the learned response age, maximize fitness of individuals. Thus, behavioral
depended on a fixed pattern of muscle movements. ecologists attempt to identify the payoffs and costs that
Contrary to expectations, he found that they do not. But play a role in the evolution of behavior (Owens 2006).
Lashley was not solely concerned with the neurological
There has been some question concerning the
uniqueness of the approach of sociobiology. Some sci-

Sociobiology and Behavioral Ecology 21

entists, for example, question whether sociobiology is However, it was not until 1975, when E. O. Wilson pub-
really a new discipline or simply part of contemporary lished his landmark text, Sociobiology, that the true impact
ethology (e.g., Dawkins 1989). In contrast, others of sociobiological ideas was felt. The text, an engaging
believe that at least early on, ethology and sociobiology integration of ideas from fields such as ethology, ecol-
could be separated in several ways (Barlow 1989). For ogy, and population biology, gained almost instant noto-
example, whereas classical ethologists tended to derive riety from both within and outside the scientific
hypotheses from detailed observations (i.e., through community. Wilson defined sociobiology as the “sys-
induction), sociobiologists tended to be more deductive, tematic study of the biological basis of all social behav-
typically deriving hypotheses from larger theoretical ior” and proposed that a knowledge of demography (e.g.,
frameworks. Whereas classical ethologists were inter- information on population growth and age structure)
ested in species differences, sociobiologists began to and of the genetic structure of populations was essential
investigate individual differences, examining the costs in understanding the evolution of social behavior.
and benefits of a particular act. Having mentioned some
of the questions concerning the precise relationship Although sociobiological ideas had been developing
between sociobiology and other fields of animal behav- for several years before the publication of Wilson’s book,
ior, let us consider the relatively recent “history” of the text crystallized many of the relevant issues and soon
sociobiology. became the focal point for proponents and critics alike.
Criticism arose from both the scientific and political are-
During the late 1960s and early 1970s, most scien- nas. First, in attempting to establish sociobiology,
tists were quite comfortable with the idea that natural Wilson attacked fields such as ethology and comparative
selection acted primarily on individuals. Despite the exis- psychology and made the bold prediction that in due
tence of widespread agreement, however, some nagging time sociobiology would engulf these disciplines. He
issues that seemed inconsistent with selection at the level specifically predicted that ethology and comparative psy-
of the individual remained (Hinde 1982). For example, chology would be “cannibalized by neurophysiology and
how could one explain the evolution of sterile castes in sensory physiology from one end and sociobiology and
species of ants, bees, and wasps? How could the evolu- behavioral ecology from the other” (Wilson 1975).
tion of nonreproducing individuals be consistent with Another area of great concern, this time from the polit-
Darwinian selection? Similarly, how was one to explain ical arena, was the extension of sociobiological thinking,
the evolution of certain patterns of behavior, called altru- in the absence of sound evidence, to human social behav-
istic behavior, that seemed to benefit others but were ior (Cooper 1985). Opponents of sociobiology claimed
costly (with respect to survival and reproduction) to the that Wilson advocated biological determinism, the idea
performer? Why, for example, do some animals give that the present conditions of human societies are sim-
alarm calls when they spot a predator, when calling may ply the result of the biology of the human species and
actually increase their own chances of being detected? therefore cannot be altered. Although only the final
The answer to these questions came in 1964 when W. D. chapter of his text was devoted specifically to humans,
Hamilton published his seminal papers, “The Genetical heated debate over the social and political implications
Evolution of Social Behaviour, I, II.” Hamilton showed of sociobiological theories ensued (e.g., see the collec-
that evolutionary success (the contribution of genes to tion of papers in Caplan 1978).
subsequent generations) should be measured not only by
the number of surviving offspring produced by an indi- During the 1970s and early 1980s, research on
vidual but also by the effects of that individual’s actions sociobiological topics in animal behavior flourished.
on nondescendant kin (e.g., siblings, nieces, and George Barlow (1989) suggested, “The study of animal
nephews). He coined the term inclusive fitness to describe behavior had indeed begun to stagnate by 1975, and the
an individual’s collective genetic success—that is, a com- advent of sociobiology was just the kick in the pants the
bination of direct fitness (own reproduction) and indi- field needed to get moving again.” The field of animal
rect fitness (effects on reproduction by nondescendant behavior became revitalized because sociobiology pro-
kin). When quantifying an individual’s inclusive fitness, vided a framework that could be used to test hypotheses
we count—to varying degrees, depending on how about the adaptiveness or survival value of behavior. But
closely they are related—all the offspring, personal or of the “kick in the pants” was so strong that for a time
relatives, that are alive because of the actions of that indi- almost all research in animal behavior was done under
vidual. This concept of inclusive fitness paved the way the banner of sociobiology (Bateson and Klopfer 1989).
toward an understanding of the evolution of sterile castes Of all possible questions about animal behavior, one—
and altruistic acts (these topics are discussed in more its function, or survival value—had come to dominate
detail in Chapter 19). the field.

In the years following Hamilton’s (1964) paper, By the end of the 1980s, however, many researchers
many studies were conducted in which the idea of inclu- began to notice the imbalance in the study of animal
sive fitness was used to interpret social behavior. behavior. It became apparent that our understanding of
animal behavior would be fuller if both its immediate and

22 Chapter 2 / History of the Study of Animal Behavior

evolutionary causes are considered. As Marian Stamp depends on what other members of the population are
Dawkins (Dawkins 1989, p. 53) has said, doing. In such situations, it is often helpful to consider
whether an individual’s choice of action is an evolution-
Genes operate through making bodies do things. These arily stable strategy (ESS). An ESS is a strategy that,
bodies have to develop and they need machinery (sense when adopted by most members of the population,
organs, decision centers, and means of executing action) cannot be invaded by the spread of any rare alternative
to be able to pass their genes on to the next generation. strategy. The concept of ESS has been applied in stud-
To understand this process fully, we need a science that ies of mating systems, communication, conflict, and
is not only aware of the evolutionary ebb and flow of cooperation (Krebs and Davies 1997).
genotypes over evolutionary time, but can look at the
bridge between generations, at the bodies that grow and CELLULAR AND MOLECULAR BASIS
move and court and find food and pass their genetic OF BEHAVIOR
cargo on through time with the frailest and most mar-
velous of flesh-and-blood machinery. We are also making great strides in understanding the
mechanisms of behavior, largely because of tools and
MORE RECENT TRENDS techniques that were not available even a few years ago.
Today, sign stimuli may be interpreted as filtering at the
The study of animal behavior has seen some changes in level of sensory receptors or as feature detection neurons
the areas that are the focus of study. On the whole, how- that respond to specific features of a stimulus. We can
ever, it seems to have returned to research that consid- identify neurons in circuits that underlie FAPs. For
ers all of Tinbergen’s four questions. Michael Taborsky example, new recording techniques have made it possi-
(2006) points out that ethology has largely regained its ble to map the nervous systems of several invertebrates.
balance and addresses questions of mechanism as well as In some animals, specific neurons have been linked to
function. Let’s consider some of the recent changes of specific behaviors. For instance, in the grasshopper
focus in behavioral research. (Omocestrus viridulus) three different hind leg movements
(FAPs) are involved in producing the courtship sound
FIELD STUDIES signals. By using microinjection techniques and intra-
cellular recording, it has been shown that a specific type
Following the assumption that natural selection shaped of brain nerve cell is responsible for each of these three
behavior, we should expect that behavior observed in the FAPs. During courtship, these nerve cell types are acti-
field should increase the animal’s chance of survival. vated in a specific sequence (Hedwig and Heinrich
Many of the pioneering field studies were purely 1997). Fixed action patterns are now discussed in terms
descriptive, and some also included an explanation of of neural networks, command neurons, or central pat-
what was described. However, today’s field studies usu- tern generators. In the chapters that follow, we will con-
ally begin with a clearly stated hypothesis to be tested by sider many other examples of how physiology,
data collection and analysis. The hypothesis generally neurobiology, and molecular biology have enhanced the
relates either to the short-term function of the behavior study of behavior.
or to the long-term fitness (relative number of surviving
offspring) consequences of a behavior. Thus, the data During the last decade, some avenues of research
collected are often the outcome or consequence of a have focused on the cellular, or even the molecular,
behavior, such as the amount of food collected. underpinnings of animal behavior. One of the most
Researchers might then determine the fitness conse- exciting areas of research is behavioral genomics—study
quences of natural variation in the expression of that of the role of an organism’s genetic material in behav-
behavior within a population (Altmann and Altmann ior. An organism’s genome consists of all of its DNA.
2003). As we will discuss in later chapters of this book, One goal of genomics is to learn the sequence of all the
particularly in Chapters 4 and 12, today’s field studies of genes in an organism’s genome. Indeed, scientists have
animal behavior usually focus on the costs and benefits now determined the sequence of bases in the entire
of a particular behavior, with the common currency genomes of more than 100 organisms. This information
being reproductive success. Natural selection is often allows scientists to zero in on the sequence of a partic-
assumed to have shaped not just an efficient but also an ular gene. That sequence can then be compared to a
optimal form of behavior. For example, we would expect database of known gene sequences, which contains some
a starling to select the type of prey that will maximize genes whose function is known. If the location or
the amount of food (energy) that can be delivered to its sequence matches that of a gene whose function is
brood. Also, because an animal’s environment includes known, it may provide a clue as to the function of the
competitors, an individual’s best choice of action often gene of interest.

Genomics provides a way for researchers to consider
the activity of networks of genes, instead of looking at one

More Recent Trends 23

gene at a time. Gene sequences reveal which mRNAs to TABLE 2.1 Disciplines in Animal Behavior
look for if the gene is active. This is often accomplished
using DNA microarray analysis, which compares the Discipline Focus
activity of thousands of genes simultaneously. We will see
subsets of genes become active under different condi- Neuroethology The neurological study of behavior
tions. Genomics also tells us which proteins to look for Behavioral
if the gene is active. The next goal is to determine the endocrinology The study of the hormonal basis of
functions of the proteins that are produced. The biggest Neuroecology behavior
challenge will be to figure out how the environment and
genome work together to direct the structure and Cognitive ecology The study of adaptive variation in
behavior of an individual. As Gene Robinson (2005; p. cognition and the brain
257) declared, the time has come to “achieve a compre- Evolutionary
hensive understanding of social life in molecular terms: psychology An approach that views cognition as
how it evolved, how it is governed, and how it influences an adaptive trait shaped by natural
all aspects of genome structure, gene expression and Behavioral genetics selection
organismal development, physiology and behavior.” or genomics
Applied ethology An approach to psychology that
This reductionist approach to animal behavior (try- attempts to explain human mental and
ing to understand the behavior by understanding its psychological traits as adaptations
components) has allowed many exciting discoveries, but shaped by natural selection
by the early twenty-first century appeals were being
made to “return to the whole organism” (e.g., Bateson The study of the influence of genetic
2003, 2005). According to these appeals, if you want to information on behavior
know why an animals behaves a certain way, you must
look at the whole organism, not just neurons, genes, and The study of the behavior of domestic
molecules (Hogan 2005). animals or other animals kept in
captivity
BEHAVIORAL BIOLOGY
The integration of research focusing on Tinbergen’s
In recent years, the term behavioral biology has been four questions has led to the development of new sub-
coined to describe behavioral research that includes disciplines of animal behavior (Table 2.1). A fascinating
more than one of Tinbergen’s four questions (Taborsky subdiscipline is animal cognition or cognitive ethology.
2006). The themes of returning to studying behavior at Animal behavior is no longer viewed only as the result
the level of the whole organism and integrated studies of genetic programming or neural wiring or as the result
of the four questions are threaded through the papers of a simple stimulus–response reaction. Instead, an
celebrating the fortieth anniversary of Tinbergen’s clas- animal’s mental capabilities are seen as a product of nat-
sic paper on the four questions1. Michael Ryan (2005) ural selection. The field of study began with Donald
argues that an approach to animal behavior that integrates Griffin’s controversial book, The Question of Animal
Tinbergen’s four questions—cause, development, sur- Awareness (1976). Griffin later (2001) named the field
vival value, and evolution—is needed to provide a com- cognitive ethology. It is an interdisciplinary area of
plete and correct understanding of behavior. More is research that brings Tinbergen’s four questions to bear
learned by integrating the aims and methods associated on the study of animals’ mental experiences. Three areas
with each question than by studying each question in iso- of research, in particular, are making rapid progress: ani-
lation. Ryan illustrates this idea by explaining how mal communication, seed caching and recovery, and nav-
knowledge of the evolutionary history of calls of túngara igation and orientation (Balda et al. 1998). You will read
frogs (Physalaemus pustulosus) helped researchers under- more about these subjects in later chapters of this book.
stand the mechanism of male calling and female
response, as well as how it develops and increases fitness. APPLIED ANIMAL BEHAVIOR
And David Sherry (2005) suggests that knowledge of the
survival value or function of a behavior can assist Professional opportunities are growing in applied animal
research on the causes of the behavior. For example, behavior, the study of animal behavior with practical
knowing that the ability to sense the earth’s magnetic implications rather than just for the sake of accumulating
field serves an orientation function suggests the proper- knowledge. This subfield of applied animal behavior is
ties that a magnetoreceptor must have. itself divided into other disciplines. Many applied animal
behaviorists focus on captive animals. Some work with
1A collection of these papers can be found in Animal Biology companion animals, such as dogs and cats, training them
2005(4): 55. and solving behavioral problems. Others study the posi-
tive effects of the human–animal bond: pets, for example,
improve the mental health of many elderly. Still other
researchers work with laboratory, zoo, and farm animals.

Many applied animal behaviorists work to improve
the welfare of captive animals (Fraser and Weary 2005).

24 Chapter 2 / History of the Study of Animal Behavior

To understand the challenges of this discipline, consider Other applied animal behaviorists work with wild
the “Five Freedoms” for captive animals proposed by the animals. Among them are professionals who work in
Farm Animal Welfare Council in the United Kingdom: wildlife management (e.g., increasing the population of
(1) freedom from thirst, hunger, and malnutrition, (2) game species) and pest management. An increasingly
freedom from discomfort due to environment, (3) free- important field is conservation behavior, in which the
dom from pain, injury, and disease, (4) freedom to principles of animal behavior are used in efforts to con-
express the normal behavior of the species, and (5) free- serve biodiversity. As human populations spill over into
dom from fear and distress. Whether certain of these the habitats of animals, many populations of animals are
freedoms are provided is easy to determine. For instance, declining or disappearing. To halt or reverse these
we can see whether the animals have ready access to fresh losses, we need behavioral data about habitat prefer-
water and a healthy diet. It is generally possible to see ences, migratory routes, territory size, social organiza-
that an animal is injured or diseased and to provide rapid tion, food requirements, risk of predation, mating
diagnosis and treatment. It is more difficult to be sure habits, and more. These data are crucial for designing
that we are providing animals with the other freedoms. effective nature preserves. For example, studies of trop-
For instance, in order to ensure that animals have the ical birds revealed the paths of their migratory routes
freedom to express normal behavior we must know what up and down mountains, and conservationists subse-
normal behavior is. This may require new studies of cap- quently protected corridors of land that connected pre-
tive species (or their close relatives) in their natural habi- serves on the mountaintop and in the valleys.
tat. In order to ensure that animals are free from Conservation behaviorists also may breed animals in
discomfort, pain, fear, and distress, we must understand captivity for return to the wild. This requires knowledge
something about the mental state of other species. Table of the communication signals used in mating.
2.2 categorizes some of the ways that researchers assess Reintroduction of a captive-born animal to the natural
stress in animals. habitat requires training to recognize and avoid preda-
tors (see Chapter 5). Throughout the book, we will
STOP AND THINK mention the work of applied animal behaviorists.

Dust bathing is a natural behavior that chickens perform Today there is a sense of rejuvenation in the study
to keep their feathers in good condition and rid themselves of animal behavior, largely because many disciplines are
of mites. If you were charged with designing commercial now contributing to its study (van Staaden 1998). New
chicken cages with the welfare of chickens in mind, what techniques and interactions among disciplines allow us
experiment would you perform to determine the “impor- to ask and answer many questions about behavior that
tance” of the opportunity to dust bathe to chickens? could not be addressed previously.

TABLE 2.2 Three Conceptions of Animal Welfare and Typical Measures Used

to Provide Positive Evidence of Animal Welfare

Conception of animal welfare Typical measures

Biological function Increase in stress hormones (–)
Affective states Reduction in immune competence (–)
Natural living Incidence of disease and injury (–)
Survival rate (+)
Growth rate (+)
Reproductive success (+)

Behavioral signs of fear, pain, frustration, etc. (–)
Physiological changes thought to reflect fear, pain, etc. (–)
Behavioral signs of aversion or learned avoidance (–)
Behavioral indicators of comfort/contentment (+)
Performance of behavior (e.g., play) thought to be pleasurable (+)
Behavioral signs of approach/preference (+)

Performance of natural behavior (+)
Behavioral/physiological indicators of thwarted natural behavior (–)
Performance of abnormal behavior (–)

Source: D. Fraser and D. M. Weary. 2005. Applied animal behavior and animal welfare. In The Behavior of Animals:
Mechanisms, Function, and Evolution, edited by J. J. Bolhuis and L.-A. Giraldeau, Table 15.1, p. 364. Malden, MA:
Blackwell Publishing.

Summary 25

Study of the history of animal behavior will show us methodology for classical conditioning. Behaviorism is
that whether our primary interest is the mechanism or a school of psychology that proposes limiting the study
the function of behavior, our efforts will be most fruit- of behavior to actions that can be observed. B. F. Skinner,
ful if we keep a clear focus on behavior as the driving a prominent behaviorist, found that patterns of behav-
interest of research. ior that are rewarded tend to be repeated or to increase
in frequency, and he concluded that the control of behav-
SUMMARY ior was largely a matter of reinforcement.

Perhaps the most important concept in the study of ani- The physiological basis of behavior is another tra-
mal behavior is Darwin’s idea of evolution through nat- ditional subject investigated by comparative psycholo-
ural selection, which provides the evolutionary gists. Despite their emphasis on learning and physiology
framework necessary for the development of animal in the laboratory, some comparative psychologists stud-
behavior. ied the social behavior of animals in the field.

In the early 1900s, the two dominant approaches to In the 1960s, a new discipline emerged in the study
the study of animal behavior were ethology, centered in of animal behavior; this discipline, called sociobiology
Europe, and comparative psychology, headquartered in (or sometimes behavioral ecology), focused on the appli-
the United States. Ethologists focused primarily on the cation of evolutionary theory to social behavior. W. D.
function and evolution of behavior. Because the context Hamilton articulated one of its central concepts, that of
in which a behavior is displayed is sometimes a clue to inclusive fitness, in 1964. According to Hamilton, indi-
its function, ethologists often studied behavior under viduals behave in such a manner as to maximize their
field conditions. It followed from their interest in evo- inclusive fitness (i.e., their own survival and reproduc-
lution that ethologists used a comparative approach and tion plus that of their relatives) rather than acting sim-
studied primarily innate behaviors. ply to maximize their own fitness. Suddenly, certain
issues that seemed inconsistent with selection at the level
Early ethologists were interested in stereotyped pat- of the individual, such as the evolution of sterile castes
terns of behavior, considering them to be just as reliable in insects and altruistic behavior (behavior that benefits
as morphological characters in defining a particular others at the expense of the performer), were explain-
group. These stereotyped behaviors were called fixed able.
action patterns (FAPs). An FAP is triggered by a very
specific stimulus. That portion of the total stimulus that Approximately ten years after Hamilton’s paper,
releases the FAP is called the sign stimulus or releaser. E. O. Wilson crystallized sociobiological ideas in his
Because most behaviors are not so stereotyped as landmark text, Sociobiology. Sociobiology and an interest
implied by the notion of FAP, they have more recently in the survival value of behavior dominated the study of
been described as modal action patterns (MAPs). animal behavior for approximately a decade, but it soon
became apparent that a complete understanding of
In contrast to the early ethologists, comparative psy- behavior requires knowledge of both mechanism and
chologists emphasized laboratory studies of observable, function. As new technologies became available,
quantifiable patterns of behavior. In general, they asked researchers began to explore the mechanisms of behav-
questions that concerned the development or causation ior on a molecular or cellular level. Today, the study of
of behavior. Learning and the physiological bases of animal behavior has returned to a more balanced
behavior were the focus of much of their research. approach that considers mechanism and function.
Research is conducted in the laboratory, as well as in the
Many exciting advances were made in the study of field. Information gathered in this research is being
learning. Thorndike developed the techniques for study- applied to assist the welfare of captive animals and to
ing trial-and-error learning, and Pavlov provided the study conservation biology.

This page intentionally left blank

3

Genetic Analysis of Behavior

Basics of Gene Action Networks of Genes Are Responsive
to the Environment
Goals of Behavioral Genetics
Epigenetics and Behavioral Genetics
Methods of Behavioral Genetics
Complex Relationships Among Genes
Inbreeding
Artificial Selection A Broader Perspective
Inducing Mutations and Screening for Change
in Behavior Picture this: In front of you are two cages, each contain-
Finding Natural Variants and Looking ing a female rat and her litter of week-old pups. Your col-
for Genetic Differences league enters the room, and the door slams behind her.
Hybridization The pups in one cage jump in response to the sound,
The Foraging Gene as an Example of Behavioral while those in the other cage continue grooming or sleep-
Genetics in Action ing. Why do the pups behave so differently when they
hear loud sound? In this case, it is fair to blame the
Candidate Genes mother because, in addition to influencing the future
Linking a Protein to a Trait mothering style of the female pups, the quality of mater-
Locating All the Genes Associated with a Trait nal care affects the pups’ response to stress, both now and
Microarray Analysis in adulthood. The mother of the calm pups spends a great
Important Principles of Behavioral Genetics deal of time grooming and nursing her pups (Figure 3.1);
the mother of the skittish pups is neglectful.
One Gene Usually Affects Several Traits
Genes Work in Interacting Networks Although it might be tempting to explain these dif-
Behavioral Variation and Genes ferences in behavior as being due to differences in either
learning or genes, we will learn in this chapter that the
Environmental Regulation of Gene Expression relationships among genes, experience, and behavior are
not that simple. For example, we will see that the expe-
Dominance Relationships in Cichlid Fish riences during the first week of life alter the activity of
Song Learning in Male Songbirds two genes in a nearly permanent way and influence both
The Importance of Genetic Background
to Behavioral Genetics

27

28 Chapter 3 / Genetic Analysis of Behavior

FIGURE 3.1 The quality of maternal care that
rat pups receive determines how timid the
pups will be and the quality of maternal care
that the females will give to their own pups
later in life.

how the adult rats will respond to stress and how attentive changes in gene expression alter the nervous system and
the females will be to their own pups. Furthermore, this physiology, and behavior is modified (Robinson 2008).
change in gene activity is transmitted to the next gener- Thus, we see that the effect of genes on behavior can be
ation. So, is the behavior determined by gene activity? dynamic. When we see animals that differ from one
Yes. Is it determined by early experience? Yes. How is another in behavior, it seems almost impossible that we
this possible? We will answer that question later in this will be able to say precisely how they differ. Yet this is
chapter, after discussing some of the ways that genes can exactly what the thriving field of behavioral genetics is
influence behavior. Surprisingly, the answer suggests that giving us the ability to do, at least for some behaviors.
your behavior today may be influenced by your great-
grandmother’s lifestyle. BASICS OF GENE ACTION

The relationship between genes and behavior is What do genes really do, then? How do they work? As
often difficult to decipher, but we do know that there is you may already know, genes can direct the synthesis of
not a one-to-one correspondence between genes and proteins. Each protein is specified by a different gene,
behavior. Consider a very simple behavior: a fly extends or if the protein consists of more than one chain of
its proboscis (a tubular structure of mouthparts) when the amino acids, a gene specifies one of those chains. The
sense organs on its feet detect sugar. Think of all the parts protein may be structural and be used as a building block
of the fly that need to be in good working order for the of the organism, or it may be regulatory. A regulatory
fly to successfully perform this behavior: the physical protein may modify the activity of other genes. In other
structures (the sense organs on the feet, for example) words, genes can code for specific proteins, and the pro-
must be functional, as must the neural circuitry to carry teins affect the composition and organization of the ani-
the information from the sense organs to the fly’s brain, mal in ways that influence how it behaves. An animal’s
which must assess the information and send signals via sensory receptors detect stimuli and send information to
motor neurons to the muscles of the proboscis, which the nervous system, where it is further interpreted and
must be able to contract. Each of these pieces is essen- analyzed. The nervous system may then initiate a
tial to behavior, and their structure and function are influ- response by effectors (muscles and glands) that results in
enced by many genes. In addition, most steps are behavior. Genes direct the development of the structure
influenced by both the internal physiological state of the and function of receptors, nerves, muscles, and glands.
animal (Is it hungry? Has it already learned anything Alterations in genes may change the proteins they code
about the environment?) and the external environment. for, with the result that anatomy or physiology may be
altered in a manner that changes behavior. We will look
There are two ways that genes can affect behavior. at a few examples of the links between genes and behav-
In the example of fruit fly foraging just described, genes ior later in this chapter.
alter behavior through their effects on development of
the nervous system and physiology. We will see other To understand the relationship between genes and
examples of this relationship throughout the chapter. proteins, it is helpful to know a little biochemistry.
But we will also consider examples of behavior in which Genes are made up of DNA (deoxyribonucleic acid).
the environment, especially social interactions, trigger The structure of DNA is somewhat like a long ladder,
changes in the nervous system or physiology. These twisted about itself like a spiral staircase. The DNA lad-
changes then alter the pattern of gene expression; that
is, they turn some genes on and others off. In turn,

Basics of Gene Action 29

der is composed of two long strings of smaller molecules the accurate production of new DNA molecules, but
called nucleotides. Each nucleotide chain makes up one also for conversion of the information in the gene into
side of the ladder and half of each rung. A nucleotide a protein.
consists of a phosphate, a nitrogenous base, and a sugar
called deoxyribose. There are only four different nitro- The instructions for each protein are written as the
gen-containing bases in DNA: adenine (A), thymine sequence of bases in the DNA molecule. The first step
(T), cytosine (C), and guanine (G). Although DNA has is to transcribe the information in DNA into RNA
only four different nucleotides, a DNA molecule is very (ribonucleic acid), specifically messenger RNA (mRNA).
long and has thousands of nucleotides. When forming The DNA is unzipped for part of its length so that an
a rung of the ladder, adenine must pair with thymine mRNA molecule can be formed. This first mRNA strand
and cytosine must pair with guanine (Figure 3.2). The is modified or edited before it leaves the nucleus. Some
specificity of these base pairs is important, not only for of the regions of the mRNA strand that do not code for
a protein are then snipped out.

DNA molecule Transcription Translation
5'
3'
A T 5'

TA
GC

C

A•••T TA An enzyme G Glutamic
A•••T GC RNA polymerase A glu acid

AT
CG

A C•••G A3' T G
O A•••T T UA
T•••A G GC A
C G•••C C CG C thr Threonine
O G GC U
C•••G G GC
Sugar C•••G A AT A
(deoxyribose) A•••T T UA G ser Serine
T•••A G GC C
Phosphate C CG
G GC
Nucleotide AT

A G
U
C AU
A G
G A
AT
G•••C CG 5' val Valine

T•••A TA m RNA Part of
C•••G CG a protein
A•••T 3'
G AT
5' Part of
C mRNA
3' molecule

DNA

DNA RNA Protein

FIGURE 3.2 A diagrammatic representation of the biochemistry of gene expression. A gene is a
region of a DNA molecule that has the information needed to make a specific protein. A DNA
molecule is composed of nucleotides. A nucleotide, shown on the extreme left of the figures, is a
nitrogenous base, a sugar (deoxyribose), and a phosphate. In the ladderlike DNA molecule, the
two uprights are composed of alternating sugar and phosphate groups, and the rungs are paired
nitrogenous bases. The pairing of bases is specific: adenine with thymine and cytosine with gua-
nine. During transcription, the synthesis of mRNA, the sequence of bases on the DNA molecule
is converted to the complementary sequence of bases on the mRNA molecule. Each unit of
three bases on the mRNA molecule signifies a particular amino acid. The message of messenger
RNA is, therefore, its sequence of bases that determines the order and kinds of amino acids in
the protein product.

30 Chapter 3 / Genetic Analysis of Behavior

The mRNA has a structure similar to DNA except the membranes of nerve cells that allow potassium ions
for three differences: It is single-stranded, its sugar is to pass through. Potassium channels are critical to nor-
ribose, and the base uracil substitutes for thymine. mal nerve cell function, and so the mutation causes a
Because adenine must pair with uracil and cytosine must nerve cell defect and abnormal behavior (Kaplan and
pair with guanine, the sequence of bases on RNA is spec- Trout 1969).
ified by the sequence of bases on DNA. Because the
DNA molecule is so long, the four bases can be ordered A recurrent theme in behavioral genetics is that
in many ways. Therefore, with only four bases, DNA can behavior depends on which genes are expressed in which
encode the information needed for the synthesis of a tissues and when. Although all the cells of an animal’s
myriad of different proteins. body have the same genes, some of them are turned off
during development. When genes are turned off, they do
The next step is to translate the order of bases on not produce a protein. If these genes are then turned on,
the mRNA molecule into a protein. Proteins are long however, their proteins are produced, and in some cases,
chains of amino acids. Each different protein has a they will modify a structure or function in a way that will
unique order of amino acids. A group of three bases on alter behavior. Thus, an organism’s behavior may change
the mRNA molecule is translated, three bases at a time, as specific genes are turned on or off in specific tissues.
into a protein. The order of bases on DNA specifies the This applies even in the short term, as the animal expe-
sequence of bases in mRNA, which can be translated into riences new stimuli.
only one array of amino acids. Thus, the information in
the gene is its sequence of bases that codes for a specific The activity of specific genes is often influenced by
protein. The transfer of information can be summarized regulatory genes, of which there are many types. Certain
as follows: regulatory genes modify the activity of other genes
through the production of proteins called transcription
Sequence of bases in DNA S Sequence of bases in factors. Transcription factors and other products of reg-
mRNA S Sequence of amino acids in a protein. ulatory genes increase gene expression or decrease gene
expression, altering the amount of mRNA produced.
For most proteins, and ultimately the traits they Thus, gene regulation determines when and where a
influence, different forms exist because the underlying protein will be produced, as well as how much of that
DNA sequences are different. For example, coat color protein is produced. Mutations in regulatory genes often
in mice might be black or brown. In other words, this have a more widespread effect on the organism than do
gene for coat color can be expressed in two different structural genes because these genes produce proteins
ways; one resulting from intense black pigment granules, that regulate many other genes.
and the other from chocolate brown pigment granules.
These alternative forms of a gene are called alleles. Consider the mechanisms by which genes regulate
Sometimes, as in the eye color of fruit flies, there are courtship and mating in fruit flies. If you have ever left
many possible alleles. The wild type, or most common a ripe banana in your kitchen too long, you may know
eye color of fruit flies, is red, but other alleles of this gene that mating is something fruit flies do well, but you may
can result in white or vermilion (a brilliant red tinged not know that the choreography is complex. The dance
with orange) eyes. Furthermore, most of the animal begins with orientation, during which the male faces the
species used in genetic studies are diploid, meaning that female and taps her on the abdomen with his foreleg. If
an individual possesses two alleles of each gene, one from she wanders away, he follows her. Next, he begins to
each parent, and this influences how the gene is “sing” a courtship song by fluttering a single out-
expressed. If the two alleles of a gene are identical, the stretched wing. If the female does not show interest, he
individual is said to be homozygous for the trait. will repeat these actions. When the female seems recep-
However, an individual may inherit different alleles for tive, he extends his proboscis and licks the female’s gen-
a gene from its mother and father. Such an individual is italia. Next, he will try to copulate with her. If the
heterozygous for the gene. The genetic diversity attempt fails, he will wait a few moments before starting
among unrelated individuals results from the particular the ritual from the beginning (Hall 1994).
alleles that they possess and from whether or not they
are heterozygous. The regulatory gene fruitless (fru) affects nearly
every aspect of male courtship in fruit flies and provides
Structural genes produce proteins that become part an example of gene regulation at several levels—sensory
of a structure or that have a specific function within an processing, choice of behavior, and carrying out the
organism. Consider, for example, the Shaker gene in the behavior (Dickson 2008). Fru is but one gene in a hier-
fruit fly, Drosophila melanogaster. A particular mutation— archy of regulatory genes that influence the final behav-
that is, a specific change in the sequence of bases in the ior pattern. In such a hierarchy, the protein product of
DNA—in the Shaker gene results in flies that shake vio- one gene regulates the activity of another gene whose
lently under anesthesia. It turns out that the mutation protein product affects the activity of perhaps a third
changes a protein used in the formation of channels in gene and fourth gene, and so on. Recall that a newly
formed mRNA is edited or spliced before it is translated

Methods of Behavioral Genetics 31

into protein. Fru mRNA transcripts are edited differ- als. Then, typically by comparing relatives, we can deter-
ently in males and females, under the direction of a gene mine how much of the observed variation is due to
higher in the hierarchy (transformer or tra) that responds genetic differences among the individuals and how much
to the number of X chromosomes present. When only is caused by differences in their environments. The
one X chromosome is present, the male-specific versions heritability of a particular trait in a specific population
of these fru transcription factors are produced. In turn, is the ratio of the variation caused by genetic differences
these fru transcription factors regulate genes in certain to the total amount of variability in the trait in that pop-
neurons to build the correct neural circuitry for male ulation. Therefore, heritability can vary from 0 to 1. A
courtship and sex determination in fruit flies. The value of 0.5 indicates that 50% of the variability in the
female-specific mRNA transcripts of fru do not direct population studied is due to genetic differences. The
the development of the same circuitry (Baker et al. 2001; heritability of a complex trait such as behavior is rarely
Dulac 2005). more than 50% (Plomin et al. 2003).

Male-specific fru proteins alter the way that the Genomics, the study of an organism’s entire
neural circuit underlying sexual behavior functions to genome—all of its DNA—has had a major impact on
produce male courtship behavior. This difference is most behavioral genetics. The field took off during the 1990s
likely due to an identifiable subset of fru-expressing with the beginning of gene-sequencing projects designed
interneurons that are present only in males. In the to discover the sequence of nucleotides in entire genomes.
female, these neurons are programmed to die. The pres- The goal of functional genomics is to understand the
ence of the male-specific fru protein prevents the death function of genes and noncoding regions of the genome.
of these interneurons, which alters the way in which the It often begins with the wealth of information created by
neural circuit for sexual behavior functions in a male gene-sequencing projects, but functional genomics is pri-
(Kimura et al. 2005). marily interested in patterns of gene activity under dif-
ferent conditions or at different developmental stages.
Fru is expressed in only about 500 neurons, roughly Comparative genomics analyzes differences in the
1.5% of the neurons in the central nervous system. genomes of different species. Its goal is to understand how
However, fru is also expressed in nearly all of the sen- traits have evolved, as well as how they work physiologi-
sory neurons involved in courtship, especially olfactory cally. The next level of study is proteomics, which strives
sensory neurons. Thus, as you might expect, disruptions to study the full set of proteins coded for by an organism’s
of fru lead to changes in sexual behavior. Male fru genes and to understand how these proteins work
mutants are bisexual. A group of only male fru mutants together to produce and modify traits. As we will see, dif-
form courtship chains in which each male chases and ferent genes are expressed in different degrees and in dif-
courts the male in front, forming revolving circles of ferent tissues at different times during development and
courting flies. Expression of male-specific fru causes under different environmental conditions.
females to display male courtship behavior instead of
female behavior (Manoli et al. 2005). We see, then, that METHODS OF BEHAVIORAL
this single regulatory gene has profound influences on GENETICS
many aspects of mating behavior.
As we have seen, the observed variation in behavior
GOALS OF BEHAVIORAL among individuals results from differences in genes and
GENETICS in environments. Therefore, when we are interested in
exploring the influence of genes on behavior, it is impor-
When we observe an animal in nature, its actions are tant to rule out environmental effects by raising the
generally a result of many genes interacting with one animals in the same environment. If environmental con-
another and the environment. A goal of behavioral ditions are identical for all animals, then observed behav-
genetics, then, is to identify the gene, or more commonly ioral differences are due to genetic differences.
the genes, that underlie a behavior and to learn the func-
tions of these genes. Another goal of behavior genetics INBREEDING
is to decipher the interactions among genes and their
products and between genes and the environment to Inbred lines, one of the tools used by behavioral geneti-
understand why a particular behavior takes the form it cists, are laboratory colonies of individuals that have no,
does. In order to understand these interactions, it is often or virtually no, genetic diversity: they are homozygous for
useful to quantify the heritability of a behavior. nearly all their genes. Inbred strains are usually created
by mating close family members with one another for
Heritability is a statistical measure that suggests how many generations and are useful in behavioral genetics
strongly a behavior is influenced by genes. Because it is
a statistical measure, we must measure the differences in
the behavior of a sufficiently large number of individu-