The Study of Animal Behaviour

The Study of Animal Behaviour

The Study of Animal Behaviour FELICITY HUNTINGFORD Department oj Zoology University ojglasgotlj, UK LONDON NEW YORK Chapman and Hall

Firstpublished 1984 by Chapman and Hall Ltd 11 New Fetter Lane, London EC4P 4EE Published in the USA by Chapman and Hall 733 ThirdAvenue, New YorkNY 10017 1984 Felicity Huntingford Photoset by Enset Ltd. Midsomer Norton, Bath, Avon and printed in Great Britain by J. w. Arrowsmith Ltd., Bristol ISBN-13: 978-0-412-22330-3 e-isbn-13: 978-94-009-5536-3 DOl: 10.1007/978-94-009-5536-3 This title is available in both hardbound and paperback editions. The paperback edition is sold subject to the condition that it shall not, by way of trade or otherwise, be lent, re-sold, hired out, or otherwise circulated without thepublisher's prior consent in any form of binding or cover other than that in which it is published and without a similar condition including this condition being imposed on the subsequent purchaser. All rights reserved. No part of this book may be reprinted, or reproduced or utilized in any form or by any electronic, mechanical or other means, now known or hereafter invented, including photocopying and rewrding, or in any information storage and retrieval system, without permission in writingfrom the publisher. British Library Cataloguing in Publication Data Huntingford, Felicity A. The study of animal behaviour. 1. Animal behavior I. Title 591.51 QL751 Library of Congress Cataloging in Publication Data Huntingford, Felicity A. (Felicity Ann) The study of animal behaviour. Bibliography: p. Includes index. 1. Animal behavior. I. Title. QL751.H757 1984 591.51 83-19002

To Tim and Anne, without whom this book would not have been written, and to Joan and Jessica, without whom it might have been written sooner

Contents Preface Acknowledgements List of plates Chapter 1 Introduction 1.1 The ethological approach to the study of behaviour 1.2 A brief outline of classical ethological theory 1.3 The modem study of animal behaviour 1.4 An outline of the book Chapter 2 The description and measurement of behaviour 2.1 Describing behaviour by its function 2.2 Describing behaviour by its form 2.2.1 Behaviour described as a continuous process 2.2.2 Behaviour described as a series of discrete events 2.3 Describing and measuring the relationship between an animal and its environment 2.3.1 Describing the way a single animal uses space 2.3.2 Describing the relationship between an animal and neighbouring conspecifics 2.4 "What is the point of all this sophisticated analysis? Chapter 3 The study of the causes of behavioural change 3.1 "What constitutes a causal explanation of behaviour? 3.2 The different kinds of causal explanation 3.3 Motivational models 3.3.1 Descriptive and explanatory models 3.3.2 General, theory-based and specific, data-based models 3.3.3 Deterministic and probabilistic models 3.3.4 Assessing models xiv xv xvi 1 1 4 8 10 12 12 13 13 15 25 25 28 44 47 47 47 49 50 51 51 51 Contents vii

3.4 Studying external influences on behaviour 54 3.4.1 Prey catching in toads; behavioural studies 55 3.4.2 Attack in Haplochromis burtoni 56 3.4.3 Incubation in herring gulls 59 3.4.4 Prey catching in toads; physiological studies 62 3.4.5 The role of external stimuli in the control of behaviour 64 3.5 Studying internal influences on behaviour 66 3.5.1 Identifyin.g groups of causally related acts 66 3.5.2 The role of internal factors in the control of behaviour 75 3.6 What is the nature of the mechanisms which cause behavioural change? 76 3.6.1 A probabilistic model 76 3.6.2 A deterministic model 77 3.6.3 Modelling motivation as a hierarchy of decisions 79 3.6.4 Control theory models of motivation 80 3.6.5 Space-state models 88 3.7 Studying the physiological bases of behavioural change 97 3.7.1 Physiological explanations of complex behaviour 99 3.7.2 Alteration in behavioural theory as a result of physiological research 100 3.7.3 Identifying fruitful topics for physiological study by behavioural analysis 100 3.7.4 Ethological concepts and techniques can improve the quality of physiological research 100 3.7.5 Ethological ideas can help in the interpretation of physiological results 103 Chapter 4 The development of behaviour 104 4.1 Problems with the instinct-learning dichotomy 104 4.1.1 Instincts are defined by exclusion 104 4.1.2 Interpreting deprivation experiments is not simple 105 4.1.3 Learning is not the only way the environment influences development of behaviour 106 4.1.4 The instinct -learning dichotomy confounds three distinct consequences of behavioural development 106 4.2 Why is the term innate still used? 108 4.3 Describing the ontogeny of behaviour 109 4.3.1 The emergence of recognizable behaviour patterns in young animals 109 4.3.2 The time of appearance of behaviour patterns during development 111 Vlll Contents

4.3.3 The development of motivational systems 112 4.3.4 Physiological changes accompanying behavioural development 116 4.4 Characterizing the factors which influence the development of behaviour 118 4.4.1 Deductions from descriptive studies 118 4.4.2 Experimental studies of behavioural development 122 4.4.3 Experimental studies of the development of song in passerines 124 4.4.4 A quantitative model of the development of social preferences in birds 131 4.5 Classifying the factors which influence the development of behaviour 134 4.6 Some general features of behavioural development 135 4.6.1 Sensitive periods 135 4.6.2 Constraints on learning 136 4.6.3 Functional aspects of behavioural development 136 Chapter 5 The adaptive significance of behaviour 138 5.1 Sources of evidence about the adaptive significance of behaviour 139 5.1.1 Deduction from the theory of natural selection 139 5.1.2 The context in which behaviour is shown 139 5.1.3 The short-term consequences of behaviour 139 5.1.4 Comparisons between species and populations 139 5.1.5 Measuring the fitness of individuals which differ in their behaviour 141 5.1.6 Experimental manipulation of the consequences of behaviour 144 5.1.7 Deductions from the genetic architecture of behaviour 146 5.1. 8 Models of the adaptive significance of behaviour 147 5.2 Difficulties in studying the adaptive significance of behaviour 152 5.2.1 Multiple benefits 152 5.2.2 Costs, benefits and optimality models 153 5.2.3 Frequency dependent costs and benefits; games theory 156 5.3 The state of the art 159 5.4 The adaptive significance of the way animals pattern their behaviour in time 160 5.4.1 Rhythms ofbella!iollr _ 160 5.4.2 The adaptive significance of behavioural rhythmicity 162 5.5 The adaptive significance of the way animals use space 166 5.5.1 Dispersal patterns 166 5.5.2 Deciding where to live 167 5.5.3 What to do where; optimal foraging theory 169 5.5.4 Problems with optimal foraging theory 180 Contents ix

5.5.5 Constraints on use of space resulting from the presence of conspecifics 186 5.5.6 Territorial behaviour 188 5.6 The adaptive significance of an animal's aggressive responses 193 5.6.1 Games theory and the hawk-dove model 194 5.6.2 Weaknesses of the hawk-dove model 195 5.6.3 Games theory models in sexually reproducing species 196 5.6.4 Conflicts between doves; the War of Attrition model 197 5.6.5 Games with progressive escalation 198 5.6.6 Games with asymmetries between opponents 198 5.6.7 Games in which information is acquired during a fight 203 5.6.8 Gamel> with non-random encounters 203 5.6.9 The contribution of games theory to our understanding of the adaptive significance of the way animals fight 204 5.7 The adaptive significance of an animal's breeding habits; mating systems 205 5.7.1 Life history parameters 206 5.7.2 Questions about sex 206 5.7.3 Mating systems 208 5.8 Adaptive significance of behaviour accompanying mating 217 5.8.1 Identifying the correct species 217 5.8.2 Preventing mating with conspecifics of the wrong sex 218 5.8.3 Synchronizing the behaviour of potential mates 218 5.8.4 The impact of intra-sexual competition for mates 218 5.8.5 The impact of selectiveness in potential mates 221 5.8.6 Alternative mating strategies 229 5.8.7 Darwin, natural selection and sexual selection 233 5.8.8 Conflicts of interest between the sexes 235 5.9 The adaptive significance of parental care 237 5.10 The adaptive significance of living in groups 243 5.10.1 Studies of the adaptive significance of group life 243 5.1 0.2 The benefits resulting from group life 247 5.1 OJ The complex costs and benefits of group life; Caraco's model (1979) 249 5.11 Behaviour which cannot be explained by classic natural selection theory 253 5.11.1 An outline of the problem 253 5.11.2 Animals may ultimately benefit from their 'altruistic' behaviour 256 5.11J Group selection 257 x Contents

5.11.4 Kin selection 259 5.11.5 Parental manipulation 268 5.11.6 Has altruism been explained? 270 5.12 Overview; sociobiology and behavioural ecology 270 5.12.1 Weaknesses in the sociobiological approach to behaviour 271 5.12.2 Reasons why behavioural differences may not be adaptive 272 Chapter 6 The phylogeny of behaviour 276 6.1 Sources of evidence about the phylogeny of behaviour 276 6.1.1 The fossil record 276 6.1.2 Ontogeny 278 6.1.3 The behaviour of interspecific hybrids 278 6.1.4 Comparative studies 279 6.2 Some representative behavioural phylogenies 283 6.2.1 Tongue movements in reptiles 283 6.2.2 Predatory behaviour in gastropods 283 6.2.3 Aggressive interactions in fish 283 6.2.4 Hymenopteran social systems 285 6.3 Deriving general principles of behavioural evolution 288 6.3.1 Sound production in crickets 288 6.3.2 Courtship in peacocks 288 Chapter 7 The role of behaviour in the evolutionary process 290 7.1 The behaviour of other animals as a major selective force 290 7.1.1 The behaviour of conspecifics 290 7.1.2 The behaviour ofheterospecifics 291 7.2 Behaviour dictates the selection pressures to which an animal is exposed 293 7.3 The impact of behaviour on population structure 295 7.3.1 Behavioural influences on gene flow between populations 295 7.3.2 Behavioural influences on population size 298 7.3.3 Behavioural influences on panmixis 299 Chapter 8 Behavioural genetics 300 8.1 The objectives of research into the inheritance of behaviour 300 8.2 Potential contributions of genetics to the study of animal behaviour 301 8.2.1 As an additional research tool in the analysis of behaviour 301 8.2.2 As a source of essential information about behaviour 302 8.3 Quantitative genetics 303 8.4 Techniques for identifying the genetic origin of a known behavioural difference 306 Contents xi

8.4.1 Crosses between behavioural variants 306 8.4.2 Selective breeding from extremes of a behavioural continuum 313 8.5 Screening known genetic variants for behavioural differences 316 8.5.1 Known single gene mutations which influence behaviour 317 8.5.2 Visible differences in chromosome structure with behavioural effects 317 8.5.3 Comparing naturally occurring, isolated populations 317 8.5.4 Correlating degree of relatedness and behavioural similarity 318 8.5.5 Inbred strains 318 8.5.6 Itecombinantstrains 321 8.6 Characterizing the precise behavioural effects of genetic differences 322 8.7 The mechanisms whereby genes influence behaviour 326 8.7.1 Effects on the structures necessary for performing the behaviour 326 8.7.2 Effects on muscles or neuromuscular junctions 327 8.7.3 Effects on the sense organs 327 8.7.4 Effects on the CNS 327 8.7.5 Effects on the endocrine system 329 8.7.6 Effects on some totally unknown mechanism 329 8.8 Genetic mosaics 330 8.9 Animal behaviour and behavioural genetics 333 Chapter 9 Applied ethology 336 9.1 Clarification of terms; what is applied ethology? 336 9.2 Ways in which ethological research can be applied to practical problems 337 9.2.1 Direct application of the results of ethological research 337 9.2.2 Using the ideas and concepts of ethology 338 9.2.3 Using ethological techniques 338 9.3 Pest control 338 9.4 Increasing the productivity of commercially important species 341 9.4.1 Identifying suitable species for exploitation 342 9.4.2 Selection for desired behavioural attributes 342 9.4.3 Controlling dispersal and movement 342 9.4.4 Promoting survival 343 9.4.5 Promoting growth 344 9.4.6 Promoting successful reproduction 348 9.5 Animal welfare 350 9.5.1 Identifying suffering in animals 350 9.5.2 Alleviating animal suffering 353 9.6 Conservation 354 xii Contents

9.7 Human behaviour 356 9.7.1 Applying ethological techniques to human behaviour 356 9.7.2 Ethological concepts as a source of hypotheses about human behaviour 359 9.7.3 Making direct use of the facts collected by ethologists 362 9.7.4 Sociobiology and human behaviour 366 References Author index Species index Subject index 368 395 402 407 Contents Xlll

Preface The aim of this book is to identify the main areas of active discussion about, and research into, the biology of animal behaviour, to describe and assess ways in which these can be studied and using selected examples, to illustrate the kinds of results which are emerging. It is not intended to provide an exhaustive review of all we know about animal behaviour, although the examples have been chosen to cover as many as possible of the things that animals do. XlV Preface

Acknowledgements I would like to thank C. Swann, M.L.N. Murthy and the Superbrain for typing the manuscript; Linda Partridge, Pat Monaghan, Douglas Fraser and Richard Wilson for constructive criticism of earlier drafts; Alan Crowden for help in planning and producing the book and, particularly, Tim Huntingford for help and encouragement at all stages of its production. Acknowledgements are gratefully made to Jim Tulley fot producing plates 1, 2, 3, 7 and 12 and to Michael Hansell for the remainder. Acknowledgements xv

List of plates Plate 1 Non-random spacing in animals; a colony of breeding gannets 30 Plate 2 Behaviour of gulls at the nest; relief of an incubating kittiwake by its partner 58 Plate 3 Development of behavioural sequences; certain elements of play in cats become incorporated into predatory sequences 113 Plate 4 Foraging bees 175 Plate 5 Sexual advertisement? A male frog calling at a breeding pond 222 Plate 6 Parental investment by the female; a mother spider monkey carrying her infant 238 Plate 7 Group living and vigilance; a flock of grazing pink-footed geese 246 Plate 8 Living in groups can improve feeding efficiency; social facilitation in pink-footed geese 248 Plate 9 Sterile castes (of termites), a problem for the conventional theory of natural selection 266 Plate 10 Factors other than kinship may favour communal nesting in hymenoptera; a hornet (Vespa tropica) destroying a larva of the wasp Parischnogaster mellyi 269 Plate 11 Possible stages in the evolution of complex social organization in the hymenoptera. (a) A single female Parischnogaster jacobsoni at her nest; (b) a small group of Liostenogastervaripiaa at a communal nest 286 Plate 12 Differential choice of habitat by closely related species; the voles Clethrionomys brittanicus (a) and Microtus agrestis (b) in their natural environments 297 xvi List of plates