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AN INTRODUCTION TO ANIMAL BEHAVIOUR Sixth Edition Wolves excitedly greet each other as members of the pack come together; a bumble bee uses its long tongue to reach the nectar at the base of a foxglove flower; a peregrine falcon stoops at high speed to strike a pigeon flying below; young cheetahs rest quietly together, very close to sleep. Now in full colour, this revised and updated edition of Manning and Dawkins’ classic text provides a beautifully written introduction to the fundamentals of animal behaviour. Tinbergen’s four questions of causation, evolution, development and function form the fundamental framework of the text, illustrated with fascinating examples of complex behavioural mechanisms. The authors provide accounts of all levels of behaviour from the nerve cell to that of the population. The strengths of An Introduction to Animal Behaviour as a textbook include its clear explanations and concise, readable text, and the enthusiasm of the authors for their subject. AUBREY MANNING, OBE FRSE was Professor of Natural History at the University of Edinburgh. His main research and teaching interests were based around the development and evolution of animal behaviour. He completed his DPhil under Niko Tinbergen and is now Emeritus Professor. He received the Zoological Society of London Silver Medal in 2003 for public understanding of science. MARIAN STAMP DAWKINS is Professor of Animal Behaviour at the University of Oxford where she heads the Animal Behaviour Research Group. Her research interests lie around animal perceptual worlds, with particular emphasis on animal suffering. She has authored, co-authored and edited eight books dealing with subjects ranging from basic behaviour to animal suffering and consciousness. AN INTRODUCTION TO ANIMAL BEHAVIOUR Sixth Edition Aubrey Manning University of Edinburgh Marian Stamp Dawkins University of Oxford CA MBRI DG E UNI V ERS ITY PRESS Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, Sa˜o Paulo, Delhi, Mexico City Cambridge University Press The Edinburgh Building, Cambridge CB2 8RU, UK Published in the United States of America by Cambridge University Press, New York www.cambridge.org Information on this title: www.cambridge.org/9781107000162 # Aubrey Manning and Marian Stamp Dawkins 2012 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 2012 Printed in the United Kingdom at the University Press, Cambridge A catalogue record for this publication is available from the British Library Library of Congress Cataloging-in-Publication Data Manning, Aubrey. An introduction to animal behaviour / Aubrey Manning, Marian Stamp Dawkins. – 6th ed. p. cm. Includes bibliographical references and index. ISBN 978-1-107-00016-2 (Hardback) – ISBN 978-0-521-16514-3 (Paperback) 1. Animal behavior. I. Dawkins, Marian Stamp. II. Title. QL751.M22 2012 591.5–dc23 2011027496 ISBN 978-1-107-00016-2 Hardback ISBN 978-0-521-16514-3 Paperback Additional resources for this publication at www.cambridge.org/9781107000162 Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. CONTENTS Preface page ix 1 Introduction 1 Questions about animal behaviour 5 The escaping cockroach 7 The courtship of the sage grouse 11 Units of the nervous system 16 Reflexes and more complex behaviour 20 Diversity and unity in the study of behaviour 30 Summary 31 2 The development of behaviour 33 Young animals grow up 34 Instinct and learning in their biological setting 40 The characteristics of instinct and learning 45 Genetics and behaviour 49 Development and changes to the nervous system 57 Hormones and early development 62 Early experience and the diversity of parental behaviour 68 Play 78 Imprinting 84 Bird song development 94 Conclusions 106 Summary 106 3 Stimuli and communication 109 What stimuli are and how they act 111 Diverse sensory capacities 114 v The problem of pattern recognition 126 Sign stimuli (key features) 128 ‘Supernormal’ stimuli 130 Neuroethological basis of sign stimuli 135 Other solutions for pattern recognition: generalized feature detection 139 Communication 144 What is communication? 145 Animal signals as effective stimuli 150 Honesty and deception in animal signalling 159 The honeybee dance 164 The calls of vervet monkeys 173 Summary 177 4 Decision-making and motivation 179 Decision-making on different time scales 182 Decision-making and ‘motivation’ 193 Measuring motivation 193 Is motivation specific or general? 199 Goals as decision points 202 Homeostasis and negative feedback 205 Competition between motivations 209 Inhibition/disinhibition 211 Decision-making with incomplete information: the role of signals 213 Conflict and ‘abnormal’ behaviour 217 The physiology of decision-making 220 Hormones and sequences of behaviour 227 Conflict and physiological stress 232 Decision-making, motivation and animal welfare 233 Conclusions 236 Summary 237 5 Learning and memory 239 Learning as part of adaptation 239 Sensitization and habituation 242 Associative learning 246 Specialized types of learning ability 257 What do animals actually learn? 262 Are there higher forms of learning in animals? 264 The comparative study of learning 268 Social learning and culture 272 The nature of animal minds 276 vi Contents The nature of memory 294 Summary 298 6 Evolution 301 The adaptiveness of behaviour 302 Genes and behavioural evolution 310 Kin selection and inclusive fitness 316 Evolutionarily stable strategies 328 Sex and sexual selection 336 Species isolation and species selection 345 Tinbergen’s fourth question: the phylogeny of behaviour 348 Summary 353 7 Social organization 355 The individual in the crowd 355 Advantages of grouping 358 Diverse social groups 364 Eusociality: division into castes 364 Territory in the social organization of vertebrates 369 Mating systems and social organization 373 Dominance in social systems 378 Diverse mammalian social behaviour 381 Primate social organization 388 Summary 403 References 405 Figure credits 435 Index 442 Contents vii PREFACE It is 14 years since the last edition and the science or sciences of animal behaviour have progressed enormously. Topics which justified only a brief mention in an introductory text then, for example sperm competition as a factor in mating systems, have prospered to require textbooks of their own. How then to approach a new edition which cannot be allowed to become significantly larger. It is our conviction that an introduction to the whole field, or at least a substantial part of it, remains as important as ever. Discussing new areas of research is best done from a firm basis of the basic concepts and for us these are still embodied in Niko Tinbergen’s 1963 ‘Four Questions for Ethology’ – function, evolution, causation and development. So the plan of our book remains essentially that of the other editions. There has been some extensive rewriting and we have tried to give good coverage to those areas where there have been important advances, notably in the evolution of behaviour and its development. We continue to give extensive references so that readers can easily get into the literature of areas that catch their interest. There is a great deal of new literature to be explored but we have never cited new work unless it really adds something. Often concepts are best illustrated by some of the now classical papers. This edition benefits enormously from the encouragement we have had from Cambridge University Press to illustrate more widely and, in particular, to use colour photographs. Animals behaving provide stunning images and we are delighted with many of the new figures here. It remains to acknowledge the great help and support we have had from Martin Griffiths – it was he who first persuaded us to undertake a new edition. His team at CUP have helped us at every stage and it has been a pleasure to work with them. Aubrey Manning Marian Stamp Dawkins ix CHAPTER ONE Introduction CONTENTS We introduce the study of animal behaviour as a subject of great diversity (many different species of animals going about their lives in a great variety of ways) but unified by four questions that can be asked about any behaviour and at any level from ‘whole animal’ to neuron. • Questions about animal behaviour • The escaping cockroach • The courtship of the sage grouse • Units of the nervous system • Reflexes and complex behaviour • Diversity and unity in the study of behaviour Wolves excitedly greet each other as members of the pack come together; a bumble bee uses its long tongue to reach the nectar at the base of a foxglove flower; a peregrine falcon stoops at high speed to strike a pigeon flying below; young cheetahs rest quietly together, very close to sleep (Fig. 1.1). The study of animal behaviour is about all these things and much more. It is about the chase of the hunter and the flight of the hunted. It is about the spinning of webs, the digging of burrows and the building of nests. It is about incubating eggs and suckling young. It is about the migration of a hundred thousand animals and the flick of a tail of one. It is about remaining motionless and concealed as well as about leaping and flying. Behaviour involves the static postures and active movements, all the noises and smells and the changes of colour and shape that characterize animal life. 1 Animal behaviour is a very popular subject, not just with biologists but with the general public – so much so that it has even come to occupy a lot of prime time on television, the surest measure of real popularity! Since our earliest origins, human beings have always been fascinated by our fellow creatures. Apart from this intrinsic interest and the fact, which we hope to demonstrate, that the subject presents us with questions as challenging as any in science, the study of animal behaviour is also of great practical importance. The conservation of wild animals in their natural habitats and the welfare of those other species we have domesticated for our use are both topics which command a lot of public attention. Experimental studies with animals are now controlled by law in many countries, and rightly so. In the past, we have gained valuable information about behaviour from experiments, for example deafening young birds or isolating a young monkey from its mother, which might now be deemed unacceptable. Nevertheless, we shall describe some such results as part of this book. Not to do so would be perverse, since they have advanced our understanding and by this understanding we are better able to design observations and experiments which are not invasive or cruel in any way. Animal behaviour workers are very conscious of their responsibilities in this regard and go to some lengths to minimize any kind of disturbance to the lives of their subjects. The Association for the Study of Animal Behaviour in the United Kingdom and the Animal Behavior Society of the USA collaborated to publish a collection of papers, Ethics in Research on Animal Behaviour, which considers such problems, not only for laboratory Figure 1.1 Young cheetahs recline sleepily. Inactivity is as much a characteristic of behaviour as activity. 2 Introduction studies but also for fieldwork (ASAB/ABS, 2006). Even observing animals from a distance can disturb them and so needs to be done with great care. We are now able to learn a great deal about the behaviour of animals by tagging them for recognition or fitting them with tracking devices. Although the animals may then be released back into the wild, catching them may cause stress and the tracking or marking devices may even alter their behaviour. This means that the way in which we design any study of animal behaviour – experimental or observational – has moral, social and economic implica- tions. The importance of animal welfare is being increasingly recognized around the world as more and more countries now have legislation, codes of practice or other guidance as to how animals should be treated. The study of animal behaviour has a particular contribution to make here, since understanding the behaviour of animals and how it has been evolved under natural selection can help us to improve welfare. Legislation will be effective only if it is based on good information about how animals live and how they respond to their environment. For example, the captive breeding of cheetahs (Acinonyx jubatus) is likely to be one important tactic for the long-term survival of this wonderful animal. Zoos had kept them for many years but their breeding success was pitifully low until we obtained the results of fieldwork in Africa (see Caro, 1994). This showed that keeping males and females together – the standard zoo practice – was doomed to failure. Female cheetahs live and hunt alone, completely separately from males, except for the brief days of their oestrus. Once this aspect of the natural situation was reproduced in captivity, cheetahs proved quite easy to breed and several zoos – the cheetahs in Fig. 1.1 are at London’s Whipsnade Wildlife Park – now have good numbers which could be the basis for re-introductions to the wild should this prove necessary. We opened this chapter with a glimpse at the range of very diverse phenomena we are dealing with. Where in all this diversity do we start? What do people who study animal behaviour actually do and what do they want to find out? There are two main approaches, the physiological and the ‘whole animal’. Behav- ioural physiology is the study of how the body works, that is how the nerves, muscles and sense organs are coordinated to produce complex behaviour such as singing in a cricket or a bird. The ‘whole animal’ approach investigates the behaviour of the intact animal and the factors that affect it, for instance, what it is in the environment of the cricket or bird that prompts them to sing at a particular time or why they sing at all. ‘Whole animal’ questions of this latter type can be studied both by looking at wild animals in their natural environments and also by observing captive or domestic animals living under more controlled conditions: it depends on the exact question involved. Physiological investigations often require bringing animals into a laboratory environment because they will involve ‘probing beneath the skin’, as it were. For example, if we want to get at the mechanisms that give rise to the behaviour of singing, or those which organize an animal’s responses to visual stimuli from predators. In practice there is considerable overlap between the approaches. It is now possible to collect urine samples from animals in the wild – only tiny amounts are needed – and Introduction 3