Table Of ContentAN 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
