Social Behaviour in Animals WITH SPECIAL REFERENCE TO VERT EBRAT ES 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 Chapman and Hall, 11 New Fetter Lane, London EC4P 4EE USA Chapman and Hall, 29 West 35th Street, New York NY10001 JAPAN Chapman and Hall japan, Thomson Publishing japan, Hirakawacho Nemoto Building, 7F, 1-7-11 Hirakawa-cho, Chiyoda-ku, Tokyo 102 AUSTRALIA Chapman and Hall Australia, Thomas Nelson Australia, 480 La Trobe Street, PO Box 4725, Melbourne 3000 INDIA 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 89-77968 591.5'1 - dc20 CIP CONTENTS CHAP. P40a I INTRODUCTION I Statement of the problems - The Herring Gull - The Three-spined Stickleback - The Grayling - Types of social co-operation II MATING BEHAVIOUR 22 The functions of mating behaviour-Some instances of timing-Persuasion and appeasement-Orienta tion-Reproductive isolation-Conclusion 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 be haviour of the reactor-Review of releasers-Con clusion VI RELATIONS BETWEEN DIFFERENT SPEcms The release of reactions-The avoidance of release VII THE GROWTH OF SOCIAL ORGANIZATIONS 99 Differentiation and integration-The establishment of social ties-Further developments-Conclusion Regulation 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 problems function, causation, evolution; by emphasis on an appro priate sequence of description, qualitative analysis, quanti tative 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 ofd es crip tion. 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 pheno menon 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 descrip tions 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 court ship 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 answer ing 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