Social Behaviour in Animals

WITH SPECIAL REFERENCE TO VER TEBRA TES

N. TINBERGEN Formerly Reader in Animal Behaviour

in the University of Oxford

With a new foreword by C. P. Baerends

S CHAPMAN AND HALL

LONDON. NEW YORK. TOKYO. MELBOURNE. MADRAS

UK

USA

JAPAN

AUSTRALIA

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Chapman and Hall, 11 New Fetter Lane, London EC4P 4EE Chapman and Hall, 29 West 35th Street, New York NY10001 Chapman and Hall japan, Thomson Publishing japan, Hirakawacho Nemoto Building, 7F, 1-7-11 Hirakawa-cho, Chiyoda-ku, Tokyo 102 Chapman and Hall Australia, Thomas Nelson Australia, 480 La Trobe Street, PO Box 4725, Melbourne 3000 Chapman and Hall India, R. Sheshadri, 32 Second Main Road, CIT East, Madras 600 035

First edition 1953 Reprinted three times Second edition 1964 Reprinted 1965, 1969 First published in Science Paperbacks 1965 Reprinted 1966, 1968, 1969, 1971 and 1972 Facsimile reprint 1990

© 1953. 1964, 1965,:\". Tinbcrgen

ISBN 978-0-412-36920-9 ISBN 978-94-011-7686-6 (eBook) DOI 10.1007/978-94-011-7686-6

All rights reserved. No part of this publication may be reproduced or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, or stored in any retrieval system of any nature, without the written permission of the copyright holder and the publisher, application for which shall be made to the publisher.

British Library Cataloguing in Publication Data Tinbergen, Niko, 1907-

Social behaviour in animals : with special reference to vertebrates. - 2nd ed. 1. Animals. Social behaviour I. Title 591. 51

Library of Congress Cataloging-in-Publication Data Tinbergen, N., 1907-

Social behavior in animals, with special reference to vertebrates 1 N. Tinbergen ; with a new foreword by

G.P. Baerends. p. em.

Includes bibliographical references. 1. Social behavior in animals. 2. Vertebrates -Behavior.

I. Title. QL775.T5 1990 591.5'1 - dc20

89-77968 CIP

CONTENTS

CHAP.

I INTRODUCTION

Statement of the problems - The Herring Gull -The Three-spined Stickleback - The Grayling -Types of social co-operation

II MATING BEHAVIOUR

The functions of mating behaviour-Some instances of timing-Persuasion and appeasement-Orienta­tion-Reproductive isolation-Conclusion

P40a

I

22

III FAMILY AND GROUP LIFE 40 Introduction-Family life-Group behaviour

N flGHTING 57 Reproductive fighting-The functions of reproduc-tive fighting-The causes of fighting-The peck-order

V ANALYSIS OF SOCIAL CO-OPERATION 72

Recapitulation-The actor's behaviour-The be­haviour of the reactor-Review of releasers-Con­clusion

VI RELATIONS BETWEEN DIFFERENT SPEcms

The release of reactions-The avoidance of release

VII THE GROWTH OF SOCIAL ORGANIZATIONS

Differentiation and integration-The establishment of social ties-Further developments-Conclusion­Regulation

99

VIII EVOLUTIONARY ASPECTS OF SOCIAL ORGANIZATION 118

The comparative method-Comparison of social systems-Comparison of releasers-Conclusion

IX SOME HINTS FOR RESEARCH IN ANIMAL SOCIOLOGY 129

BIBLIOGRAPHY 140

INDEX 147

III

PREFACE

T HIS book is not intended as an exhaustive review of facts. Its aim is rather the presentation of a bio­

logical approach to the phenomena of social behaviour. This type of approach was revived by Lorenz's pioneer studies. It is characterized by emphasis on the need for renewed and careful observation of the huge variety of social phenomena occurring in nature; by emphasis on a balanced study of the three main biological problems­function, causation, evolution; by emphasis on an appro­priate sequence of description, qualitative analysis, quanti­tative analysis; and finally by emphasis on the need for continuous re-synthesis.

The character of this approach, combined with the limitations of space, have determined this book's contents. Limits of space led to the omission of a great deal of de scrip­tion. Thus, Deegener's voluminous work on fhe multitude of types of animal aggregations has not been discussed. Also, the highly specialized 'states' of social insects have not been treated in detail, since there are excellent books dealing exclusively with them.

The nature of the approach makes this book essentially different from other books on social behaviour. On the one hand, I have treated briefly some problems which have been much more elaborated by other authors. Thus Allee's works are mainly concerned with the various uses animals derive from crowding; there is little mention of the causes underlying social co-operation, and when dealing wiih these causes, attention is focused entirely on the pheno­menon of peck-order-an interesting, but minor aspect of social organization. Other workers seem to attach undue value to the influence of transmission of food from one individual to another; while this is admittedly a factor in

v

vi SOCIAL BEHAVIOUR IN ANIMALS

the development of some social relationships, it is again merely one element of a large complex of phenomena. Lastly, there is an enormous amount of scattered and often unrelated analytical evidence, acquired under such special laboratory conditions that it is at present impossible to say how it is related to the normal life of the species concerned.

On the other hand, I considered it of great importance to work out the formulation of the main problems, of their relation to each other and to more special, subordinated problems. This task, together with the necessary descrip­tions of many new facts found through 'naturalistic' study, and with the first qualitative steps of analysis, required much space. In addition, I wanted to formulate and emphasize some new theories which I consider important because of their great heuristic value. Thus the significance of intraspecific fighting, the causation of threat and court­ship behaviour, the functions of releasers, and other problems to which the new approach has made distinct contribution~, have been presented in some detail, and an attempt has been made to give them their proper place in the complex system of problems.

I have tried to present my thoughts in such a way that they can easily be followed by interested non-professionals. I t is my hope that by doing so I will stimulate research, for I am convinced that the amateur can still make great contributions to our young science.

I am much indebted to Dr. Michael Abercrombie and to Desmond Morris for valuable criticism and for revising the English text; to Dr. L. Tinbergen for drawing part of the illustrations, and to the Oxford University Press for permission to use a number of the illustrations from my book The Study of Instinct. My thanks are further due to Dr. Hugh Cott for permission to reproduce Fig. 61 and to Dr. Brian Roberts for permission to use his splendid penguin photograph used for the wrapper and on Plate 5.

TEXT ILLUSTRATIONS

Fig. Page

I. Male Herring Gull about to feed female 4 2. Upright threat posture of male Herring Gull 5 3. Herring Gull feeding chick 6 4. Herring Gull chick crouching 7 5. Boundary fight of two Three-spined Stickleback males

(after Ter Pelkwijk and Tinbergen, 1937) 9 6. Courtship sequence of Three-spined Stickleback (after Tin-

bergen, 1951) 10

7. Male Three-spined Stickleback guarding young 13 8. The Grayling: dorsal view; ventral view (after Tinbergen et

al., 1942) 15 9. The 'bow' of the Grayling (after Tinbergen et al., 1942) 16

10. Male Kestrel passing prey to female 18 I I. Blackbird feeding young 19 12. Young Tilapia natalensis returning to female 20 13. Swarming of oyster larvae (after Korringa, 1947) 25 14. Male Three-spined Stickleback courting a crude model of

female 27 15. Female Three-spined Stickleback following male model 28 16. Pre-coition display of European Avocets (after Makkink,

1936) 29 17. Pre-coition display of Herring Gulls (after Tinbergen, 1940) 30 18. Male Bitterling courting the female during spawning (after

Boeseman et al., 1938) 31 19. Saturnia pyri 33 20. Lapwing in flight 34 2 I. The function of song in the locust Ephippiger (after Duym and

Van Oyen, 1948) 35 22. Male Ten-spined Stickleback showing nest entrance to

female (after Sevenster, 1949) 38 23. Time spent fanning by male Three-spined Stickleback.

Fanning graph when eggs are replaced on 4th day 42 24. Young Cuckoo throwing out an egg of its foster parents

(after Heinroth and Heinroth, 1928) 43 25. Female Herring Gull proposing to male 46

Vll

Vlll SOC I ALB E H A V IOU R I NAN I MAL S

Fig. Page 26. Night Heron at rest; performing the 'appeasement cere-

mony' 47 27. Hemichromis bimaculatus: the relieved parent swims away in

a straight course (after Baerends and Baerends, 1948) 48 28. Ringed Plover with chicks 5 I 29. Two ways in which a male Redstart advertises its nest-hole

to a female (modified from Buxton, 1950) 52 30. Wagtails mobbing a Sparrow Hawk 55 31. Fighting Red Deer 57 32. Tail-fighting in fish (after Tinbergen, 1951) 58 33. Threat display of the English Robin (after Lack, 1943) 58 34. Frontal threat display in Cichlasoma meeki and Hemichromis

bimaculatus (after Tinbergen, 1951) 59 35. Male Antelope cervicapra marking a tree with the secretion of

the scent-gland located in front of the eye (after Hediger, ~ ~

36. Bitterling male with Mussel (after Boeseman et al., 1938) 60 37. Fighting male Chaffinches 6r 38a. A test on the dependence of attack on territory 63 38b. The same males in territory B 63 39. Bitterlings react to an empty Mussel (after Boeseman et at., ~ ~

40. Experiments on the release of fighting in male Three-spined Stickleback (after Tinbergen, 1951) 66

41. Threat posture of male Three-spined Stickleback (after Tin-bergen, 1951) 67

42. An experiment on fight-releasing stimuli in the Robin (after Lack, 1943) 67

43. Female and male American Flicker (after Noble, 1936) 68 44. Head of Shell Parrakeet (after Tinbergen, 1951) 69 45. Male Cuttlefish at rest and displaying (after L. Tinbergen,

~) ~ 46. Male Fence Lizard in display (after Noble, 1934) 70 47. Various displacement activities functioning as threat (after

Tinbergen, 1951, and Makkink, 1936) 76 48. Models of Herring Gull heads (after Tinbergen and Perdeck,

1950 ) 79 49. Models of Herring Gull heads (after Tinbergen and Perdeck,

1950) 80 50. Male Snipe 'bleating' 82

TEXT ILLUSTRATIONS lX

Fig. Page 5 I. Two ordinary scales and one scent-scale of the male Gray-

ling (after Tinbergen et al., 1942) 82 52. Mating Garden Snails (after'Meisenheimer, 1921) 83 53. Visual display phase of Common Newt (after Tinbergen and

Ter Pelkwijk, 1938) 84 54. Male Common Newt sending a water current to the female

(after Tinbergen and Ter Pelkwijk, 1938) 84 55. Flight line of a Hover Fly (Bombylius) (after Knoll, 1926) 88 56. Flight line of a Honey Bee (after Knoll, 1926) 89 57. Linaria vulgaris and its orange honey guide (after Knoll, 1926) 90 58. Artificial flowers with honey guide models (after Knoll, 1926) 90 59. Flight line of a Pine Hawk Moth 91

60. Longitudinal section of inflorescence of Arum macula tum (after Knoll, 1926) 92

61. Chaetodon capistratus and its 'eye spot' (after Cott, 1940 ) 94 62. The Digger wasp Ammophila adriaansei with prey (after

Baerends, 1941) 100 63. Termite 'king' and 'queen' 103

64. An ant worker and soldier 121

65. A termite worker and soldier 121

66. Male Fiddler Crab displaying (after Pearse from Verw/y, 1930) 122

67. Displacement preening in courting ducks 126

PLATES

Facing page

I. Male Three-spined Stickleback, adopting the threat posture (Plwto by N. Tinbergen) 20

2. The forward threat posture of the Black-headed Gull (Photo by N. Tinbergen) 30

Head-flagging of Black-headed Gulls (Photo by N. Tinbergen)

3. A male Grayling courting a female of the related species Hipparchia statylinus (Photo by N. Tinbergen) 36

Singing male Natterjack (Flashlight photo by N. Tinbergen)

4. Ruffs on lek (Photo by F. P. J. Kooymans) 40

Unusual nest relief by a Lesser Black-backed Gull (Photo by M. G. Rutten)

5. Young Herring Gulls in submissive posture (Photo by N. Tinbergen) 48

A 'creche' of the King Penguin in South Georgia (Photo by Brian Roberts)

6. Herring Gull feeding chick (Photo by N. Tinbergen)

Two experiments with head models (After Tinbergen and Perdeck, I950)

7. Eyed Hawk Moth at rest (Photo by N. Tinbergen) 90 Eyed Hawk Moth displaying 'eye'-spots (Photo by N. Tin­

bergen)

8. Larvae of the Cinnabar Moth, showing true warning colora-tion (Photo by N. Tinbergen) 94

x

FOREWORD

T HIS book is a revised and translated version of a Dutch text which originally appeared in 1946. Tinbergen had

written it during the war, much of it when he was imprisoned in a German hostage camp. He based it largely on his own observations and research which he had carried out in the late 1920s and the 1930s, a time that included the seven years in which he introduced the newly developing discipline of ethology into the biological curriculum of the University of Leiden.

Ethology as Niko Tinbergen saw it, aimed at a broad study of the 'instinctive' or species-characteristic behaviour of animals, with a strong emphasis on the adaptiveness to the ecological niche in which each species is living. It was to him obvious that such work had to start from observing animals in their natural surroundings, preferably in the field or, if that were impossible, under semi-natural conditions. When Tinbergen began his career in the early 1930s, the study of animals in the field was not held in very high esteem by most professional zoologists of the day, who tended to leave the confines of their laboratories only for catching and killing the objects of their research. Most publications on wildlife had been written by amateurs and this made it easy for such work to be depreciated as a 'hobby'.

Tinbergen was convinced that to make ethology respectable as a biological science, clear questions had to be derived from the observations made and then methods developed for answer­ing them. Following Huxley, he therefore pointed out that three different sorts of 'why-questions' about behaviour should be asked: questions about itsfunction or adaptiveness, questions about its immediate causation and questions about the way it develops in the course of evolution. In Social Behaviour in Animals

Tinbergen shows his readers how to look at the behaviour of Xl

XlI SOCIAL BEHAVIOUR IN ANIMALS

animals in the field with these three questions ill mind, emphasizing that they are separate questions which should not be confused but are at the same time mutually dependent.

The original Dutch title can be translated as 'Animal Sociology'. The book was conceived at a time when in botany plant sociology had become very popular. This made eco­logically oriented zoologists keen to develop a zoological counterpart. Tinbergen, however, pointed out that whereas plant sociology was mainly concerned with types of vegetation and the relationships between different species of plants, animal sociology should primarily focus upon the interrelation­ships between individuals of the same species, and should thus be seen as more closely allied to human sociology.

The book has become a classic. Many established profes­sional ethologists and ecologists have testified that this book put them on the right track and, in particular, gave them the confidence to yield to their desire to spend a considerable part of their time with their animals in the field, thus turning their hobby into a scientific discipline. For this reason alone the book is of historical interest. But it is not the only reason for welcom­ing the publication of a facsimile reprint, almost 40 years after the book first came out. Young scientists of today who intend to devote themselves to the study of animal behaviour will still find the book a valuable introduction. This is because instead of relying on already published theories and facts, Niko Tinbergen gave such a high priority to showing what the interesting problems are and then indicated ways of solving them.

Instead of loading the reader with knowledge, the book inspires him to join in the adventure of wresting from free­living animals the intimate secrets of their lives. Niko Tinbergen was at his best when he was taking his students into the field, watching for something to happen and then wonder­ing what it meant and speculating about possible ways to answer the questions that arose. The reader of the book can get

FOREWORD XUI

a flavour of what Niko's pupils learned from being in direct contact with him. The book expresses the open-minded attitude to investigation that characterizes the ethological approach, an important reason why, in 1973, the Nobel Prize for physiology or medicine was awarded collectively to Niko Tinbergen, Konrad Lorenz and Karl von Frisch, as the founders of ethology. Because of this attitude the book is still attractive and useful reading for many people outside the science of animal behaviour who may feel the desire to draw comparisons between the behaviour of animals and of man.

Although the book is modest in size, it is long enough to serve its purpose. Its brevity is characteristic of the same hand that once wrote over the door of the library of the zoological laboratory of Leiden University the words: 'study nature and not books'.

Before he died in December 1988, Tinbergen felt somewhat ambivalent about the appearance of a facsimile edition of his book. On the one hand he liked the idea because he believed its educational value had not diminished. On the other hand, he was aware that the book contained certain interpretations of behaviour which no longer hold today and which he himself had abandoned or revised. This, however, only demonstrates how productive Tinbergen's approach has been; it has contri­buted to the spectacular development of the discipline of behavioural ecology in the last three decades. At the request of the publisher I have in the following tried to point out, for newcomers in this field in particular, where views have changed importantly, combining this with a rough sketch of the trends taken in behavioural ecology.

In line with his own aims Tinbergen based the book on his own experiences. Consequently, he deals mainly with studies of birds, fishes and insects, and with relationships between part­ners - between rivals and between parents with their young. These are all relatively simple relationships because a small number of individuals is involved. Readers of today may notice

XIV SOC I ALB E H A V IOU R I NAN I MAL S

that there are no references to primate societies. They should realize that at the time the book was written, knowledge about the societies of monkeys and apes in the wild was extremely scarce. The study of these societies only became widespread in the 1960s, especially under the influence of anthropologists who hoped to extend their insight in the early evolution of human behaviour by studying the behaviour of man's animal relatives. Since the mid-1950s primatologists working in the field in Africa, Asia and Latin America have collected a vast amount of information on the often species-characteristic structures of various primate societies and relationships between the individuals of which they are composed.

The first question that often arises when attention is drawn to a particular behaviour pattern of an animal is what function it serves its performer - in other words, how it might influence its reproductive fitness. Functional questions can refer to different levels of integration in the total structure of behaviour. For instance, within the overall function of making a nest, the function of each of the separate building activities can be studied. On a finer scale, it is possible to study the function of the different individual motor patterns and how they are adapted to the particular circumstances in which an animals finds itself.

Before the 1930s questions about function or biological significance of an activity had usually been answered by logical reasoning from behind a desk. Such answers are obviously liable to criticism. In particular, they are unsatisfactory if used to try to understand the evolution of structures and behaviours apparently showing a surprisingly high degree of adaptedness, as a result of random mutation and natural selection. Tinbergen was among the first to undertake an experimental test of such hypotheses on the function of a behaviour, using quantitative methods by which the strength of the alleged selec­tive force could be assessed. In designing his experiments, he consistently took the complementary questions about evolution

FOREWORD xv

and causation of the elements into account. In this way he made functional questions respectable and laid the foundations for interesting new developments in the study of function.

One of these developments has been the study of the trade­off between the benefits and the costs involved in the fulfilment of behavioural functions. The degree to which benefit can be maximized is likely to be restricted by various kinds of constraints, such as competition with other vital functions. To what extent, under the pressure of the different selective forces, the behaviour of an animal or a species has developed towards an optimal compromise, and how this has come about in the course of evolution is an interesting problem. Several species have more than one set of behaviour patterns (behavioural strategies) at their disposal for a given major function and are able to switch between them when the ecological conditions change.

Another novel approach, closely connected with the optimality concept, has been the development of research for assessing the probability that the selective pressures, hypothesized to underly the evolutionary development of a particular behavioural trait, could indeed have been at work. Theoretical reasoning and mathematical modelling, in which ideas borrowed from game theory and economics are made full use of, are at the core of such studies and have become impor­tant in designing research and data collection in the field. The variation among the social organizations of different primate species are a fascinating target for this approach. Some species are monogamous, but most live in groups of more than two adult individuals. Two major group types can be distinguished, depending on whether only one male or several adult males live together with several females and their offspring. Within these groups further species-characteristic differentiations can be made and in some species one-male groups live together in large troops. Two ecological factors, risk from predators and intraspecific food competition, are considered the main

XVI SOCIAL BEHAVIOUR IN ANIMALS

determinants for the structure of the society. The factors favour co-operation between individuals, including the formation of coalitions or alliances. Not only in primates, but in widely different taxonomic groups, examples can be found of the development of special social relationships leading to mutual co-operation and the achievement of tasks that would be impossible for a single individual.

When considering the effectiveness of selection pressures one needs to specify the target on which selection is supposed to act. Ethologists used to talk of the benefit of a character for the maintenance of the species; the reader will also find this in this book. It implies that selection would act on a group. Super­ficially, at one time this seemed to be the easiest way to under­stand the occurrence of co-operation between group members. However, sophisticated mathematical modelling has now shown that, if it does occur, 'group selection' has to be an extremely complicated process. It is much less likely to occur than selection acting on individuals. This means that for the interpretation of the many cases in which members of a group take risks to their own health and life for the benefit of com­panions (alarm calling, feeding and protecting young, castes in insect societies), the possibility of individual selection should be considered first. This task has attracted scientists of different disciplines (ecologists, population biologists, geneticists and mathematicians as well as ethologists). A new branch of behavioural research called 'sociobiology' has emerged from it and has strongly influenced the direction of field research in the last two decades. Practically all cases of 'altruistic' behaviour can in fact be interpreted as being beneficial to genes present in the individual who takes the risk, thus contributing to its reproductive success. Most of it is directed at individuals with which kinship relationships exist or else with individuals that can be expected to reciprocate.

With respect to the 'why-question' of causation, Tinbergen gives various examples of studies of mechanisms in an animal

FOREWORD XVII

through which particular social functions are achieved. These studies were highly influenced by two of Lorenz's concepts: the fixed action pattern, as the fundamental unit of motor activity, and the 'key-lock' combination of social releaser in the sender and releasing mechanism in the receiver, as the explanatory principle for selective sensitivities to particular stimulus situa­tions. Lorenz called these species-characteristic capacities innate. With this adjective he meant to stress that the informa­tion an animal needs for performing these motor co-ordinations or for reacting adequately to specific stimulus situations is not obtained through learning by trial and error, imitation or cultural transmission (teaching), but has - in the course of evolution, via the process of mutation and selection - become encoded in the genes. Very impressed by the high degree of adaptiveness of the morphology and behaviour of such species and of the links between the two, early ethologists attached much weight to the role of genes in bringing about species­characteristic or 'instinctive' behaviour. They were strongly opposed to the way genetic factors were ignored in favour of conditioning by the 'behaviourist' approach. As a consequence 'innate' and 'learned' came to be considered as incompatible features.

A sharp critique of Lorenz's theory, published by Lehrman in 1953, heralded a gradual turning away from the tendency to label a behavioural element as either innate or learned. While recognizing the role of genes in the development of behaviour, Lehrman argued that blinkered thinking about the innate versus learned dichotomy has inhibited research on the genuinely fascinating problem of how information encoded in the genes comes to be expressed during the development of behaviour in the individual. By seeing that experience, especially some form of learning, could be under the control of influences emanating from genes, he provided a conceivable mechanism for this process. Since 1953, this principle has indeed been found to apply frequently, for instance to the

XVlll SOC I ALB E H A V IOU R I NAN I MAL S

species-characteristic song pattern of several birds. Conse­quently, classification of such songs as either innate or learned has been seen to be impossible. Tinbergen was among the first to accept this viewpoint and it made him add a fourth category to the four fundamental 'why-questions', namely the problem of the ontogeny of behaviour. But that happened after this book had been written.

It is clear that the opportunities for incorporating learning into an ontogenetic process increase with the average lifespan of the animal and particularly with the length of its juvenile development. Thus programmed integration oflearning can be expected to become more frequently and more elaborately applied in vertebrates than in invertebrates and in higher vertebrates than in lower ones. Since Tinbergen's examples rarely concerned mammals, the use of the term innate in the book is not too disturbing. Nevertheless, the reader should be aware- that in the lower vertebrates responsiveness to specific stimulus situations will also far more often involve learning than was formerly thought. Social interactions in primates are heavily dependent on early experience with individually known conspecifics. The young primate learns its place in the group, to avoid unfriendly responses or to seek allies. But also in other mammals and in birds, fishes and even some invertebrates, there is increasing evidence that personal friendships are important in social relationships. The addition of learning processes to the underlying 'Lorenzian mechanisms' makes this possible.

The consistent, but at the same time flexible lines of thought and the continuous references to the behaviour of real animals, as demonstrated in this book, were essential parts of its impact. Tinbergen conveys his message in a form that invites participa­tion and his special gift was to impart a sense of urgency by making readers want to go out and see animal behaviour for themselves.

c. P. Baerends