The Tinbergen Legacy

The Tinbergen Legacy

The Tinbergen Legacy

Edited by

M.S. DAWKINS Research Lecturer Oxford University

T.R. HALLIDAY Reader in Biology Open University and

R. DAWKINS Reader Oxford University

CHAPMAN

&

HALL

London • New York • Tokyo • Melbourne • Madras

Published by Chapman & Hall, 2-6 Boundary Row, London SE1 8HN Chapman & Hall, 2-6 Boundary Row, London SE1 8HN, UK Chapman & Hall, 29 West 35th Street, New York NY10001, USA Chapman & Hall Japan, Thomson Publishing Japan, Hirakawacho Nemoto Building, 7F, 1-7-11 Hirakawa-cho, Chiyoda-ku, Tokyo 102, Japan Chapman & Hall Australia, Thomas Nelson Australia, 102 Dodds Street, South Melbourne, Victoria 3205, Australia Chapman & Hall India, R. Seshadri, 32 Second Main Road, CIT East, Madras 600 035, India First edition 1991 © 1991 Chapman & Hall Typeset in 101/2 on 12pt Palatino by Mews Photosetting, Beckenham, Kent Printed in Great Britain by St Edmundsbury Press, Bury St Edmunds ISBN 0 412 39120 1 Apart from any fair dealing for the purposes of research or private study, or criticism or review, as permitted under the UK Copyright Designs and Patents Act, 1988, this publication may not be reproduced, stored, or transmitted, in any form or by any means, without the prior permission in writing of the publishers, or in the case of reprographic reproduction only in accordance with the terms of the licences issued by the Copyright Licensing Agency in the UK, or in accordance with the terms of licences issued by the appropriate Reproduction Rights Organization outside the UK. Enquiries concerning reproduction outside the terms stated here should be sent to the publishers at the London address printed on this page. The publisher makes no representation, express or implied, with regard to the accuracy of the information contained in this book and cannot accept any legal responsibility or liability for any errors or omissions that may be made. A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication data available

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Contents

Contributors Introduction Richard Dawkins

vii ix

1. Early ethology: g r o w i n g from Dutch roots Gerard P. Baerends 2. S t u d y behavioural adaptations Nicholas B. Davies

18

3. From animals to h u m a n s Robert A. Hinde

31

4. War and peace revisited Felicity A. Huntingford

40

5. Animal communication: ideas derived from T i n b e r g e n ' s activities John R. Krebs 6. The nature of culture Juan D. Delius

60 75

7. Niko Tinbergen, comparative studies and evolution Michael H. Robinson

100

8. The Tinbergen legacy in p h o t o g r a p h y and film Lary Shaffer

129

Afterword Aubrey Manning

139

Index

141

Contributors

Gerard P. Baerends

Hoofdweg 265, 9765 CH Paterswolde, Netherlands Nicholas B. Davies

Department of Zoology, University of Cambridge, UK Richard Dawkins

Department of Zoology, University of Oxford, UK Marian S. Dawkins

Department of Zoology, University of Oxford, UK Juan D. Delius

Universitfit Konstanz, Konstanz, Germany Timothy R. Halliday

The Open University, Milton Keynes, UK Robert A. Hinde

Department of Zoology, University of Cambridge, UK Felicity A. Huntingford

Department of Zoology, University of Glasgow, UK John R. Krebs

Department of Zoology, University of Oxford, UK Aubrey Manning

Department of Zoology, University of Edinburgh, UK Michael H. Robinson

Smithsonian Institute, Washington DC, USA Lary Shaffer

Department of Psychology, SUNY, Plattsburgh, USA

Introduction RICHARD DAWKINS

A conference with the title 'The Tinbergen Legacy' was held in Oxford on 20th March, 1990. Over 120 of Niko Tinbergen's friends, family, colleagues, former students and people who had never met him in person converged at Oxford for what turned out to be a memorable day. To reflect the rather special atmosphere of the conference, we decided to begin this book with Richard Dawkins' opening remarks exactly as he gave them on that day.

W e l c o m e to O x f o r d . For m a n y of y o u it is w e l c o m e back to O x f o r d . P e r h a p s e v e n , for s o m e of y o u , it w o u l d be nice to t h i n k t h a t it m i g h t feel like w e l c o m e h o m e to Oxford. A n d it is a great p l e a s u r e to w e l c o m e so m a n y f r i e n d s f r o m the N e t h e r l a n d s . Last w e e k , w h e n e v e r y t h i n g h a d b e e n s e t t l e d e x c e p t final, last m i n u t e a r r a n g e m e n t s , w e h e a r d t h a t Lies T i n b e r g e n h a d d i e d . O b v i o u s l y w e w o u l d not h a v e c h o s e n such a time to h a v e this meeting. I ' m sure w e ' d all like to e x t e n d o u r d e e p s y m p a t h y to the family, m a n y of w h o m , I ' m h a p p y to say, are at this m e e t i n g . W e d i s c u s s e d w h a t w e s h o u l d d o a n d d e c i d e d that, in t h e c i r c u m s t a n c e s , t h e r e w a s n o t h i n g for it b u t to c a r r y on. T h e m e m b e r s of t h e T i n b e r g e n f a m i l y that w e w e r e able to c o n s u l t w e r e fully in a g r e e m e n t . I t h i n k w e all k n e w that Lies w a s a n e n o r m o u s s u p p o r t to Niko, b u t I t h i n k that v e r y f e w of us really k n e w h o w m u c h of a s u p p o r t s h e w a s to him, p a r t i c u l a r l y d u r i n g t h e d a r k t i m e s of d e p r e s s i o n . I s h o u l d s a y s o m e t h i n g a b o u t this m e m o r i a l c o n f e r e n c e a n d w h a t led u p to it. P e o p l e h a v e t h e i r o w n w a y s of g r i e v i n g . Lies' w a y w a s to take literally N i k o ' s characteristically m o d e s t i n s t r u c t i o n t h a t h e w a n t e d n o f u n e r a l or m e m o r i a l rites of a n y k i n d . T h e r e w e r e t h o s e

x

Introduction

of us w h o w e r e fully s y m p a t h e t i c to t he desire for n o religious observance, b u t w h o n e v e r t h e l e s s felt t he n e e d for s o m e k i n d of rite of passage for a m a n w h o m w e h a d l o v e d a n d r e s p e c t e d for so m a n y years. We suggested various kinds of secular observance. For instance, the fact that t h e r e was such musical talent in t he T i n b e r g e n family led s o m e of us to suggest a m e m o r i a l c h a m b e r concert with r e a d i n g s or eulogies in the intervals. Lies m a d e it v e r y clear, h o w e v e r , that she w a n t e d n o t h i n g of the ki nd a n d that Niko w o u l d h a v e felt the same. So we did n o t h i n g for a while. T h e n , after s o m e time h a d elapsed, we realised that a memorial conference w o u l d be sufficiently different f r o m a f u n er al as not to c ount . Lies a c c e p t e d this, a n d t here cam e a time, d u r i n g o u r p l a n n i n g of the c o n f e r e n c e , w h e n she said that she h o p e d to a t t e n d the conference, a l t h o u g h she later c h a n g e d her m i n d about that, thinking, again with characteristic m o d e s t y and completely e r r o n e o u s l y , that she w o u l d h a v e b e e n in the w ay. It is an e n o r m o u s p l e a s u r e to w e l c o m e so m a n y old friends. It is a tribute to Niko, a n d the affection that his old pupi l s felt for him, that so m a n y of y o u are h e r e t oda y, c o n v e r g i n g on O x f o r d from, in s o m e cases, v e r y far away. T he list of p e o p l e c o m i n g is a galaxy of old friends, s o m e of w h o m m a y not h a v e set eyes on one a n o t h e r for 30 years. Just r e a d i n g the g u e s t list was a m o v i n g e x p e r i e n c e for me. We shall all of us h a v e m e m o r i e s of Niko a n d of the g r o u p of his associates with w h o m we h a p p e n to be c o n t e m p o r a r y . My o w n begin w h e n I was an u n d e r g r a d u a t e a n d he l e c t u r e d to us, not at first on animal b e h a v i o u r but on molluscs - for it was Alister H a r d y ' s quaint idea that all the lecturers s h o u l d participate in the 'A ni m al K i n g d o m ' course wh ich is one of the sacred cows of O x f o r d zoology. I d i d n ' t k n o w , then, w h a t a di s t i ngui s he d m a n Niko was. I think that if I had, I' d h a v e b e e n r a t h e r aghast at his being m a d e to lecture on molluscs. It was bad e n o u g h that he gave u p being a Professor in L e i d e n to b e c o m e , by O x f o r d ' s s nobbi s h custom, just plain 'Mr T i n b e r g e n ' . I d o n ' t r e m e m b e r m u c h f r o m t hos e early mollusc lectures, but I do r e m e m b e r r e s p o n d i n g to his w o n d e r f u l smile: friendly, kindly, avuncular as I t h o u g h t then, a l t h o u g h he m u s t h a v e b e e n scarcely older t h an I am n o w . I think I m u s t h a v e b e e n i m p r i n t e d on Niko a n d his intellectual s ys tem then, for I asked m y college tutor if I could h a v e tutorials with Niko. I d o n ' t k n o w h o w he m a n a g e d to swing it, because I d o n ' t think Niko gave u n d e r g r a d u a t e tutorials as a rule. I suspect that I m a y have b e e n the last u n d e r g r a d u a t e to h a v e h a d tutorials with him. T h o s e tutorials h a d an e n o r m o u s influence on me. N i k o ' s style as a t ut or was unique. Instead of giving a r eadi ng list with s o m e sort of com preh e n s i v e co v er ag e of a topic, he w o u l d give a single, highly detailed

Introduction

xi

piece of work, such as a DPhil thesis. M y first one, I remember, was a m o n o g r a p h by A.C. Perdeck, w h o I am h a p p y to say is here today. I was asked simply to write an essay on a n y t h i n g that occurred to me as a result of reading the thesis or m o n o g r a p h . In a sense it was Niko's w a y of making the pupil feel like an equal - a colleague w h o s e views on research were w o r t h hearing, not just a s t u d e n t m u g g i n g up a topic. N o t h i n g like this h a d ever h a p p e n e d to me before, a n d I revelled in it. I wrote h u g e essays that took so long to read out that, w h a t with Niko's frequent interruptions, t h e y were s e l d o m finished by the e n d of the hour. He strode up a n d d o w n the r o o m while I read m y essay, only occasionally coming to rest on w h a t e v e r old packing case was serving him as a chair at the time, chain-rolling cigarettes a n d obviously giving me his whole attention in a w a y that, I ' m sorry to say, I cannot claim to do for most of m y pupils today. As a result of these marvellous tutorials, I decided that I very m u c h w a n t e d to do a DPhil with Niko. A n d so I joined the 'Maestro's Mob', a n d it was an experience never to be forgotten. I r e m e m b e r with particular affection the Friday e v e n i n g seminars. Apart from Niko himself, the d o m i n a n t figure at that time was Mike Cullen. Niko obstinately refused to let sloppy language pass, and proceedings could be stalled for an indefinite period if the speaker was not able to define his terms with sufficient rigour. These were a r g u m e n t s in which e v e r y b o d y became engaged, eager to make a contribution. If, as a result, a seminar w a s n ' t finished at the e n d of the two hours, it simply r e s u m e d the following week, no matter w h a t m i g h t have been previously p l a n n e d . I s u p p o s e it m a y have been just the na'fvet6 of y o u t h , but I u s e d to look forward to those seminars with a sort of w a r m glow for the whole week. We felt ourselves members of a privileged 61ite, an Athens of ethology. Others, w h o belonged to different cohorts, different vintages, have talked in such similar terms that I believe that this feeling was a general aspect of w h a t Niko did for his y o u n g associates. In a way, w h a t Niko stood for on those Friday evenings was a kind of ultra-rigorous, logical commonsense. Put like that, it m a y not sound like much; it m a y seem even obvious. But I have since learned that rigorous c o m m o n s e n s e is by no m e a n s obvious to m u c h of the world. I n d e e d c o m m o n s e n s e sometimes requires ceaseless vigilance in its defence. In the world of ethology at large, Niko stood for b r e a d t h of vision. He not only f o r m u l a t e d the 'four questions' view of biology, he also assiduously c h a m p i o n e d a n y o n e of the four that he felt was being neglected. Since he is n o w associated in peoples' m i n d s with field studies of the functional significance of behaviour, it is w o r t h

xii

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recalling h o w m u c h of his career w as gi ve n o v e r to, for instance, the s t u d y of motivation. A n d , for w h a t it is w o r t h , m y o w n d o m i n a n t recollection of his u n d e r g r a d u a t e lectures o n animal b e h a v i o u r w as of his r u t h l e s s l y mechanistic at t i t ude to animal b e h a v i o u r a n d t he m a c h i n e r y that u n d e r l a y it. I was particularly t a k e n with t w o p h r a s e s of his - " b e h a v i o u r m a c h i n e r y " , and " e q u i p m e n t for survival". W h e n I came to write m y o w n first book, I c o m b i n e d t h e m into the brief phrase "survival machine". In p l a n n i n g this c onf er e nc e , w e o b v i o u s l y d e c i d e d to c o n c e n t r a t e o n fields that Niko h a d b e e n p r e - e m i n e n t in, but w e d i d n ' t w a n t the talks to be o n l y retrospective. Of cour s e we w a n t e d to s p e n d s o m e time looking back at N i ko's a c hi e ve m ent s , but w e also w a n t e d p e o p l e to pick u p the torches that Niko h a d p a s s e d t h e m , a n d r u n on w i t h t h e m t o w a r d s the future. T o r c h - r u n n i n g b e h a v i o u r , in n e w a n d exciting directions, bulks so large in the e t h o g r a m s of N i ko's s t udent s a n d associates that p l a n n i n g the p r o g r a m m e was a major h e a d a c h e . " H o w on e a r t h " , w e asked ourselves, " c a n w e possibly leave out so-and-so? O n the o t h e r h a n d , w e h a v e space for onl y six t al ks " . We could h a v e limited oursel ves to N i k o ' s o w n pupils - his scientific children, but this w o u l d h a v e b e e n to d e v a l u e his e n o r m o u s influence via g r a n d p u p i l s a n d others. We could h a v e c o n c e n t r a t e d on p e o p l e a n d major areas not c o v e r e d in the Festschrift v o l u m e e d i t e d by G e r a r d Baerends, Colin Beer a n d A u b r e y M a n n i n g , but that too w o u l d h a v e b e e n a pity. In the end, it s e e m e d almost not to m a t t e r w h i c h half a d o z e n of N i k o ' s intellectual d e s c e n d a n t s s t ood up to r e p r e s e n t the rest of us. A n d p e r h a p s that is the true m e a s u r e of his greatness.

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Early ethology: growing from Dutch roots GERARD P. BAERENDS

In the Netherlands, b e t w e e n 1930 and 1940, ethology grew from w h a t w a s originally seen as a pleasant and harmless h o b b y , to a n e w biological discipline, recognized by the academic world. Together with the A u s t r o - G e r m a n school, Dutch ethology came to play a leading role in this n e w study of animal behaviour. Its spectacular growth was d u e to the leadership of Niko Tinbergen, and I have been asked to give y o u here a kind of e y e w i t n e s s report on h o w it all h a p p e n e d . Before doing this, I w a n t to deal with s o m e aspects of the cultural climate of the N e t h e r l a n d s in the first quarter of this c e n t u r y which w e r e responsible for making that c o u n t r y one of the birthplaces of ethology and for facilitating Niko's development as one of its pioneers. In the 1880s, coinciding with a g r o w i n g a w a r e n e s s of the n e e d for a more socially just society, cultural attitudes towards nature changed. Literature and the fine arts became increasingly interested in a realistic representation of nature. Writers a n d p o e t s (Kloos, Albert V e r w e y , Gorter, Van Eeden), painters (Maris brothers, Israel, Mauve, Breitner, Wenckebach) and sculptors (Mendes da Costa) began to deal with landscapes, plants and animals in a style that took as m u c h care with the correctness of naturalistic details as with the emotional impressions felt b y the observer. Entirely n e w m e t h o d s w e r e d e v e l o p e d for the teaching of children in primary schools, aimed at making t h e m aware of the life and w o r k of p e o p l e in different c o m m u n i t i e s and professions, and with particular emphasis on informing urban children about rural life. Inspired b y this a t m o s p h e r e t w o schoolmasters, E. H e i m a n s a n d Jac P.Thijsse, b e g a n in 1893 a lifelong cooperation a i m e d at enlightening the general public a b o u t the natural world a r o u n d them. They

2

Earlyethology: growing from Dutch roots

b e g a n by writing a series of six p o p u l a r books, each dealing w i t h the life of plants a n d animals in a characteristic Dutch habitat a n d a field guide for identifying the more c o m m o n animals a n d plants. In these books the a u t h o r s guide the readers from one example to a n o t h e r , helping t h e m to look for details in structure a n d b e h a v i o u r a n d inspiring t h e m to w o n d e r about the mechanisms at work. The interest which was aroused by these books is reflected in the fact that by a r o u n d 1915 t h e y already had gone t h r o u g h three editions. Furthermore, in 1896 H e i m a n s a n d Thijsse f o u n d e d a m a g a z i n e n a m e d 'De Levende N a t u u r ' (The Living Nature) in which naturalists were e n c o u r a g e d to describe their o w n observations. Between 1927 a n d 1986 Niko Tinbergen contributed nearly 100 papers to this magazine; moreover, from 1947 to 1978 he also acted as one of its editors. The greatest impact H e i m a n s a n d Thijsse probably h a d was with the publication of a series of large illustrated albums of wildlife, which were published by the biscuit factory Verkade b e t w e e n 1906 a n d 1915. Several o u t s t a n d i n g artists belonging to the naturalistic revival school I m e n t i o n e d earlier contributed illustrations for these guides. Some of the pictures were packed with the biscuits a n d this practical exploitation of the 'collecting drive' that so m a n y people have, p r o v e d to be a very successful w a y of c o n v e y i n g a message about natural history. As a consequence of the increasing interest in natural history, naturalist societies were f o r m e d all over the country. These were mainly started by amateurs, but a few professional biologists joined t h e m as well. A unique feature of the N e t h e r l a n d s - and one that in m y opinion was very important for the d e v e l o p m e n t of e t h o l o g y in our o w n c o u n t r y - was that y o u n g naturalists, from 11 to 23 years old, formed societies of their own, quite separate from those of adults. In 1920 most of these y o u n g naturalists' clubs came together into one national association devoted to the s t u d y of nature: the ' N e d e r l a n d s e J e u g d b o n d voor N a t u u r s t u d i e ' , abbreviated as NJN. The e m e r g e n c e of societies r u n entirely by y o u n g m e m b e r s themselves was a characteristic of this period and can be seen as one result of the m o v e m e n t for more social justice and democracy that took place at the e n d of the 19th century. It was part of a reaction against the heavy h a n d with which adult society always treated y o u n g people. This m o v e m e n t a m o n g y o u n g people originally arose in G e r m a n y a n d t h e n rapidly spread to the Netherlands, but only there did it become i n s t r u m e n t a l in the p r o m o t i o n of interest in a n d k n o w l e d g e about nature. Niko Tinbergen was born in 1907 in The Hague, w h e r e he grew up in a family of one sister a n d four brothers. The cultural a n d intellectual changes taking place at the turn of the century h a d already

Early ethology: growing from Dutch roots

3

m a d e their mark on the life of the Tinbergen family. His father taught Dutch language and literature at a s e c o n d a r y school a n d h a d a great interest in the fine arts. All m e m b e r s of the family took a delight in close contact with nature, at that time still a b u n d a n t l y p r e s e n t in the dunes, w o o d s and m e a d o w s a r o u n d The H a g u e . The family u s e d to s p e n d their vacations in an area of heath and p i n e w o o d on an expanse of glacial sands near Hulshorst, a b o u t 150 k m inland. Both parents were very h a r d - w o r k i n g and set high s t a n d a r d s for their children, while at the same time giving t h e m all possible f r e e d o m in their individual d e v e l o p m e n t . Niko w a s the first m e m b e r of the family to take a d e e p e r interest in wildlife. Later his y o u n g e s t brother, Lukas, w o u l d follow his example. The other brothers t u r n e d to the physical sciences, while his sister b e c a m e a linguist. Niko's interest in nature mostly involved making his o w n observations and d e d u c t i o n s rather than s t u d y i n g the scientific literature. H e followed in the track of H e i m a n s a n d Thijsse, w h o m he greatly admired. H e particularly e n j o y e d the experience of secretly watching animals in the wild a n d capturing their b e h a v o u r in sketches a n d p h o t o g r a p h s . To a considerable extent these activities also satisfied his great passion for outdoor sports. Such pleasures were often shared with m e m b e r s of a small g r o u p of like-minded friends. W h e n in 1920 the NJN was f o u n d e d , Niko and his c o m p a n i o n s soon joined this association. While he w a s at s e c o n d a r y school, the NJN gave Niko the o p p o r t u n i t y to d e v e l o p his gift for passing his k n o w l e d g e and experience on to others with clarity and incisiveness. A lecture he gave in 1929 to recruit n e w m e m b e r s for the association not only m a d e m e join the NJN, but also imprinted me on biology forever. At school, Niko was u n h a p p y with the institutionalized teaching p r o g r a m m e s . H e considered having to go to lessons a frustrating restriction on his freedom, but he wisely took care to m a k e sure the marks on his school reports were always just above the level n e e d e d to avoid further curtailments on the time he could s p e n d on naturewatching and sport. During this period t w o older p e o p l e p l a y e d an important role in encouraging Niko's wildlife observations and his thinking about the p r o b l e m s they raised. These w e r e his biology teacher, Dr A. Schierbeek, and an outstanding amateur ornithologist, G.J. Tijmstra (maths teacher and h e a d m a s t e r of a drill school for obstinate boys!) After finishing school in 1925, Niko w a s not at all certain that he should embark on an academic s t u d y of biology. He d o u b t e d w h e t h e r the kind of biology that w a s at that time taught at the Dutch universities w o u l d help him in further d e v e l o p i n g his interest in nature in the wild. He seriously t h o u g h t of b e c o m i n g a sports teacher.

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Early ethology: growing from Dutch roots

H o w e v e r , the problem of w h a t to do w h e n at 50 years of age he w o u l d have become too old for that job, s t o p p e d him. In order to o p e n Niko's eyes to the potential of academic study, s o m e of his older friends, w h o had recognized his gift for biological work, contrived a plan. They advised his parents to allow him to s p e n d three m o n t h s at the 'Vogelwarte Rossitten', on the Kuhrische N e h r u n g in the easternmost part of Germany, w h e r e high quality field w o r k on bird migration w a s going on. The r e m e d y w o r k e d ; after his return from Rossitten, Niko enlisted for the biology course at the University of Leiden. There he f o u n d more u n d e r s t a n d i n g from his teachers than he h a d expected. Very importantly, he met Jan V e r w e y (Figure 1.1), a staff m e m b e r 8 years his senior, w h o in 1924 m a d e a n o w classic s t u d y of the

Figure 1.1 Dr Jan Verwey.

Early ethology: growing from Dutch roots

5

pair-formation b e h a v i o u r of the grey heron. Jan V e r w e y w a s the son of the poet Albert Verwey, one of the pioneers of the literary r e n e w a l of the 1880s. H e had s p e n t his y o u t h in the coastal dunes, w h e r e the family lived in a small village. V e r w e y fully shared Niko's d e v o t i o n to wildlife studies, but in contrast to Niko he w a s well aware of the merits of the more conventional disciplines of biology and conscientiously kept track of w h a t w a s a p p e a r i n g in the scientific literature. V e r w e y ' s example and s u p p o r t m a y well have been decisive in Niko's further d e v e l o p m e n t . They became, a n d always remained, great friends. Niko w a s given a great deal of f r e e d o m to model his p r o g r a m m e of s t u d y in any w a y he liked. H e could, for instance, include his ecologically oriented field w o r k on the food and feeding of raptors, in which his brother Lukas (8 years his junior) assisted him (Figures 1.2 and 1.3). In the s u m m e r of 1930 on the sands of Hulshorst, he began, entirely on his o w n initiative and with the aim of completing it for a P h D thesis, an experimental s t u d y of the w a y in w h i c h the digger w a s p Philanthus triangulum m a n a g e s to relocate its individual hole in the sand w h e n it returns with p r e y for its larva. The earlier

Figure 1.2 Niko Tinbergen building a hide around 1925.

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Earlyethology: growing from Dutch roots

studies m a d e by Von Frisch and his co-workers on the orientation and homing of h o n e y bees h a d inspired him to try this. H o w e v e r , before this study could be completed (data collection w e n t rather slowly since the Dutch climate did not allow m u c h m o r e than 25 w o r k a b l e (i.e. sunny) days per summer) Niko w a s offered the o p p o r t u n i t y to s p e n d a year with a Dutch geophysical expedition to south-east Greenland. At that time this w a s such an exceptional o p p o r t u n i t y that his official supervisor, Professor H. Boschma, allowed him to p r e s e n t the results he had obtained so far in an u n u s u a l l y slim thesis. H e trusted Niko to return to this work and continue developing it later. In 1932, shortly before leaving for Greenland, Niko obtained his doctoral degree a n d

Figure 1.4 Niko Tinbergen in Greenland 1932-33.

Early ethology: growing from Dutch roots

9

married his girlfriend, Elisabeth Rutten, a sister of one of his birdwatching c o m p a n i o n s . Thus, the expedition w a s also to serve as Niko's h o n e y m o o n . Lies w e n t with him a n d took part in all aspects of the field work. The G r e e n l a n d year (Figure 1.4) offered Niko every o p p o r t u n i t y to satisfy his desire to live amidst u n s p o i l e d nature. H e m a d e a t h o r o u g h s t u d y of the reproductive b e h a v i o u r of two bird species, the red p h a l a r o p e a n d the s n o w bunting. H e was also fascinated by the life of the A n g m a g s s a l i k m u t Eskimos and b y the behavioural aspects of the symbiosis t h e y h a d with their dogs. After his return from Greenland in S e p t e m b e r 1933, Niko obtained an a p p o i n t m e n t as an assistant - the lowest-paid position in the academic hierarchy - at the Zoological Laboratory at Leiden. Officially charged with the task of r u n n i n g the e l e m e n t a r y practical courses in invertebrate and comparative anatomy, Niko w a s also expected to develop ethology as a n e w part of the biology curriculum. This m e a n t that he had the opportunity to prove that the h o b b y of nature-watching could be t u r n e d into a serious scientific e n d e a v o u r . The director of the Zoological Laboratory, Professor C.J. van der Klaauw, himself a comparative anatomist with great interest in theoretical biology, gave him every possible support. In Niko's view, the task of ethology w a s to s t u d y the p h e n o m e n o n generally described as instinct - that is, the ability to perform speciescharacteristic b e h a v i o u r a d a p t e d to survival in a specific ecological niche - with objective scientific methods. Following Julian Huxley, he e m p h a s i z e d that w h e n watching behaviour, f u n d a m e n t a l l y different categories of questions could be distinguished, and that these should be kept carefully separated. In his early w o r k Niko restricted himself to t w o of these questions, that of function (adaptation) and that of causation of the behaviour performed. Whereas for several behaviour patterns such as feeding activities or nestbuilding the function s e e m e d to be evident, this certainly did not hold for the displays exhibited during social interactions. These displays h a d already attracted the attention of Niko and his friends, and were one of the features of b e h a v i o u r that fascinated t h e m most, as well as being w o n d e r f u l subjects for p h o t o g r a p h y . C o n s e q u e n t l y , the analysis of c o m m u n i c a t i o n b e h a v i o u r was an o b v i o u s choice for Niko's next research p r o g r a m m e . The species most appropriate for s t u d y w o u l d be available in the n e i g h b o u r h o o d of Leiden and easily observable in the wild or u n d e r semi-natural conditions. This led him to choose the herring gull for fieldwork on the nearby d u n e s and the three-spined stickleback - a b u n d a n t in the ditches a r o u n d the t o w n and easy to b r e e d in aquaria - for laboratory studies. In

10

Earlyethology: growing from Dutch roots

addition, during the s u m m e r m o n t h s the work on the nest-orientation of Philanthus was r e s u m e d in the H u l s h o r s t area. Because of the prevailing economic crisis, financial resources were minimal. H o w e v e r , Niko did not see this as m u c h of a handicap. In fact, apart from the G r e e n l a n d expedition, he h a d always d e f r a y e d the expenses for his research from his o w n pocket. Fortunately, the first steps in e t h o l o g y did not cost very much. Clear a n d disciplined thinking was the p r i m a r y requirement, a n d at that time there was no real n e e d for complicated a n d expensive e q u i p m e n t for data collection a n d processing (tools which in a n y case never interested Niko very much).

Figure 1.5 Jan Joost ter Pelkwijk.

Early ethology; growing from Dutch roots

11

W h e n Niko started work in Leiden, only a few of the more advanced biology s t u d e n t s were attracted to animal b e h a v i o u r and fieldwork - in contrast to the y o u n g e r students, m a n y of w h o m h a d discovered biology t h r o u g h the NJN. T w o s t u d e n t s w h o arrived in the first year in S e p t e m b e r 1933 were Niko's y o u n g e r brother Lukas and Jan Joost ter Pelkwijk (Figure 1.5). These t w o w e r e of great help to Niko at the beginning because of their o w n e n t h u s i a s m and the stimulating effect t h e y had on their colleagues. For several years both had shared m a n y birdwatching activities with Niko and his other friends. Ter Pelkwijk w a s an extremely gifted man: he w a s highly original a n d u n c o n v e n tional; he was an excellent artist, wrote v e r y well and h a d very broad interests. H e loved being in the field, a n d h a d f o u n d it even more difficult than Niko to follow the institutionalized path of school work. Unfortunately, his contribution to ethology e n d e d far too soon. During a stay in the Dutch East Indies, he w a s t r a p p e d b y the war against the Japanese. In 1942 he w a s killed in action. In m y opinion ter Pelkwijk's contribution to early stickleback studies w a s of vital importance, over and above his imagination a n d skill in devising d u m m i e s for experiments. The Dutch university s y s t e m p r o v i d e d excellent opportunities for developing n e w fields of experimental research. O n e opportunity came in the third year, w h e n all biology s t u d e n t s h a d to s p e n d six w e e k s on experimental work. In 1936 ethology w a s officially accepted as a subject for such w o r k and this probably led to the first ethology course in the world. At the beginning of the course the s t u d e n t s were asked just to observe the b e h a v i o u r of their animals and record it as carefully as possible, with pencil a n d paper. Following this introductory period of watching, they w e r e e n c o u r a g e d to start asking questions, and thus to w o n d e r about the b e h a v i o u r they h a d observed. These questions were then critically discussed and w h e r e necessary corrected and refined. Finally, the students were invited to design and carry out experiments for testing their o w n h y p o t h e s e s . The feeling of working on their o w n project, which no-one h a d tackled before, was very stimulating to the students. M a n y of the projects were later to be used as stepping stones for approaching larger problems. The s t u d y of the role of the different features of male and female sticklebacks that released specific elements of their reproductive b e h a v i o u r started in this way. A second source of s t u d e n t help for Niko came with the larger research projects (lasting several months) that students were required to u n d e r t a k e before they could pass their final examinations. The problems suggested for these projects had often arisen from promising

12

Earlyethology: growing from Dutch roots

results obtained in the third-year course. Studies on the stimuli releasing a n d directing f o o d p e c k i n g in herring gull chicks, a n d begging in t h r u s h nestlings, are examples of such projects. Undergraduate projects which h a d proved to be particularly promising t h e n provided a g o o d basis for longer PhD research. Niko e x p a n d e d the m a n p o w e r of his e t h o l o g y group by inviting u n d e r g r a d u a t e s to help as u n p a i d assistants with the field studies. It was a great privilege to serve as such a 'slave'. We gladly d e v o t e d the greater part of our vacations, a n d in spring also gave up m a n y hours b e t w e e n sunrise and the start of our lectures (which were t h e n in constant d a n g e r of being missed). For me, it m e a n t the start of m y work on stimulus selection in the herring gull as well as on the reproductive behaviour of the digger wasp Ammophila. Niko took part in the fieldwork as m u c h as his duties at the laboratory allowed, setting an example for w o r k i n g efficiently a n d in a well disciplined way, not allowing the h a r d s h i p s a n d blessings of the prevailing field conditions to get in the way. Unobtrusively, he t a u g h t us to keep our eyes o p e n all the time to p h e n o m e n a not directly related to our o w n project. Moreover, w o r k i n g a n d living in the field together provided excellent opportunities for personal contact between teacher and s t u d e n t s a n d for informal education. This was particularly true w h e n - as for the insect studies at Hulshorst - there were long periods of camping out in the field. Here, students also learned h o w to behave in the field, with respect for the flora and fauna as well for the people, particularly the w a r d e n and o w n e r s living and working in the s t u d y area. Niko always tried to base his research on knowledge of the environment, behaviour and m o r p h o l o g y of the animals he was s t u d y i n g as well as those of related species. Because of this attitude, he h a d an aversion to most of the work of the behaviouristic schools. In the early 1930s his teaching and planning with respect to the functional aspects of behaviour was often inspired by the writings of ornithologists such as Huxley, Selous and H o w a r d , or insect-watchers like Fabre a n d Ferton. In his o w n country, the impressive knowledge and experience of Frits Portielje, a self-taught animal psychologist at the A m s t e r d a m Zoo, was a source of inspiration to him. Nevertheless, Niko strongly rejected Portielje's view - fervently d e f e n d e d by the vitalistic animal psychologist Bierens de Haan - that the p h e n o m e n o n of instinct would not be accessible to analysis. For the s t u d y of causal mechanisms, the work of behavioural physiologists such as Von Uexk~ill a n d KLihn, but above all that of Karl Von Frisch, was even more important. Von Frisch can be said to have f o u n d e d the art of making an animal answer questions; this was exactly w h a t Niko n e e d e d a n d w a n t e d to extend

Early ethology: growing from Dutch roots

13

his o w n experiments. Von Frisch's approach inspired various studies of the Leiden g r o u p on h o w animals perceive a n d recognize those stimulus situations in their e n v i r o n m e n t that are of biological significance to them. Interest in applying ethological findings to h u m a n behaviour did not exist at that time. O n the contrary, the e m p h a s i s was rather on the a p p a r e n t differences b e t w e e n animal a n d h u m a n behaviour. It was not until the mid-1930s that K o n r a d Lorenz' ideas about the n a t u r e of instinctive behaviour came to the Leiden g r o u p a n d began to influence the w a y t h e y t h o u g h t as well as the structure of their research programme. The theoretical concepts of 'fixed action patterns' (FAP) a n d 'innate releasing m e c h a n i s m ' (IRM) p o s t u l a t e d by Lorenz provided a challenge as to h o w they were to be experimentally verified. Experimental testing of the IRM concept was entirely in line with studies already going on in Niko's group. The FAP concept, however, inspired h i m to extend his interest to a n e w area, the problem of the evolution of behaviour, and thus to ask a third f u n d a m e n t a l biological question. Lorenz and Tinbergen first met in person in N o v e m b e r 1936, w h e n Lorenz visited Leiden on the occasion of a s y m p o s i u m dedicated to the concept of instinct organized by Professor Van der Klaauw. In the spring of 1937, the Tinbergens spent several m o n t h s with Lorenz in his h o m e research station at Altenberg, near Vienna. During this stay Lorenz learned to appreciate Niko's gift for experimentation as together they studied the nature of the egg-retrieving activity of the greylag goose and the stimulus situation evoking the flight responses of geese and fowl chicks to aerial predators. Niko a n d K o n r a d differed greatly in personality but their attitude t o w a r d s nature was the same. They shared a predilection for living with their animals - Niko preferably as a non-participating h i d d e n observer and Konrad as an adopted alien member and protector - and they both obtained great satisfaction from the sense of u n d e r s t a n d i n g them. They also h a d a similar sense of h u m o u r . Both were impressive personalities, but of very different kinds. Konrad was a great talker, k n o w l e d g e a b l e in a wide field a n d always bursting with ideas, which h o w e v e r he was not particularly keen to verify systematically. Niko was a good listener, w h o always tried to put what he heard or saw into a clearly formulated framework, accessible to critical verification and therefore open to improvement in the future. Consequently their contributions to ethology were complem e n t a r y . They m u t u a l l y appreciated this and recognized that t h e y n e e d e d one another. It m a d e t h e m become a n d remain close friends. Lorenz' concept of the FAP influenced Niko's t h i n k i n g a n d his research programme in two ways. First, the characteristics Lorenz h a d

14

Earlyethology: growing from Dutch roots

attributed to FAPs d e m a n d e d experimental verification. In particular the assertions that each FAP possessed its o w n internal a u t o n o m o u s impulse-generating mechanism and that the occurrence of an FAP was not subject to superimposed control mechanisms c o m m o n to different FAPs, n e e d e d to be tested. Second, the notion that the concept of homology could be applied to behaviour as well as morphology o p e n e d the door to a s t u d y of the factors u n d e r l y i n g the evolutionary radiation of behaviour, a n d the w a y s in w h i c h a behaviour repertoire can in the course of p h y l o g e n y , be e x t e n d e d by the addition of n e w elements. As to the nature of FAPs, the experiments with sticklebacks by Niko and his co-workers forced t h e m to reject Lorenz' view that mechanisms for control of different FAPs did not overlap. They f o u n d that specific stimulus situations could exert a c o m m o n influence on the t h r e s h o l d for the release of different FAPs. Since the threshold c h a n g e often persisted after this triggering stimulation h a d gone, it was c o n c l u d e d that internal factors inducing a particular behaviour state are involved in this c o m m o n control of several FAPs. Behavioural states of different levels of integration could be distinguished and evidence was obtained that between states of equal level, inhibitory relationships existed. The conclusion was d r a w n that a hierarchical structure is basic to the w a y behaviour is organized. The various behavioural states - for w h i c h Niko claimed the n a m e 'instincts' t e n d e d to subserve different survival functions. In the h a n d s of the Leiden ethologists (in particular Van Iersel a n d Sevenster) the exploration of the structure of the behavioural organization by m e a n s of 'black-box' analysis became increasingly sophisticated. If the concept of h o m o l o g y is applied to behaviour, comparative studies of FAPs in different species can be expected to provide answers to questions about p h y l o g e n y - that is, from w h a t antecedents often bizarre-looking displays m a y have been derived in the course of evolution. Niko observed that often a display, either parts or all of it, could be seen as homologous to other activities serving a direct, instrumental, function in a different context. The w a y in which such activities could have become involved in c o m m u n i c a t i v e displays s e e m e d to be revealed w h e n in a n u m b e r of cases displays were f o u n d to be c o m p o s e d of incomplete elements of attack and escape behaviour, b l e n d e d into a compromise. Such displays could be t h o u g h t of as resulting from s i m u l t a n e o u s activation of tendencies to attack a n d to escape, likely to occur w h e n conspecifics, u n k n o w n to each other, meet. At that time, in the abscence of the game theory approach, it seemed obvious that it would be adaptive for animals to evolve displays by which they could appease their opponents. Studies of considerable -

Early ethology: growing from Dutch roots

15

sophistication supported the view that displays (which often resembled so called ' d i s p l a c e m e n t activities') could have e v o l v e d as a result of the interaction b e t w e e n incompatible b e h a v i o u r states. Thus, in this 'conflict h y p o t h e s i s ' specific properties of the structure of the behavioural organization w e r e t h o u g h t to p r o v i d e a basis for the evolution of n e w activities. The hypothesis can also help to u n d e r s t a n d the variation and adaptive radiation of displays. This conceptual f r a m e w o r k h a d b e c o m e one of the guiding principles of the research p r o g r a m m e of the Leiden ethologists w h e n the war broke out. Most of the research a n d the official teaching h a d to be s t o p p e d , b u t at least initially, w o r k on data that h a d already been collected and on committing results and ideas to p a p e r still w e n t on. H o w e v e r , contact b e t w e e n the m e m b e r s of the g r o u p b e c a m e gradually m o r e difficult, especially w h e n , in S e p t e m b e r 1942, Niko w a s taken hostage b y the o c c u p y i n g Germans. H e w a s p u t in a c a m p w h e r e prisoners were in constant danger of being shot in reprisal for attacks b y the Dutch U n d e r g r o u n d forces (Figure 1.6). After the liberation in 1945, the University of Leiden was r e o p e n e d and the work of the ethological department resumed on a prewar basis. Niko, w h o b e t w e e n 1933 and 1939 h a d b e e n gradually p r o m o t e d to higher academic ranks, w a s n o w n o m i n a t e d for a full professorship. This promotion, h o w e v e r , m e a n t that he w o u l d be charged with the directorship of the Zoological Laboratory. H e h a d g o o d reasons for fearing that the administrative duties involved w o u l d seriously handicap him in his principle aim, the promotion and further developm e n t of ethology. Lecture visits to America and Britain just before and just after the war had m a d e Niko aware of the rising interest in ethology in these countries. H e had c o n c l u d e d that for the discipline to b e c o m e really established in the English-speaking world, the emigration of continental ethologists w o u l d be helpful or e v e n essential. C o n v i n c e d that the survival of ethology in the N e t h e r l a n d s was secured, in 1949 Niko accepted an invitation to move to the University of Oxford, to which he felt especially attracted by the high level of research into evolutionary questions. In Oxford, Niko initially continued his previous research programme and m a n y P h D s t u d e n t s were attracted to ethology. Some of t h e m embarked u p o n studies inspired b y the concept of the IRM b u t u n d e r the influence of L e h r m a n ' s sharp critique of the Lorenzian 'innate vs learned' d i c h o t o m y were careful to give d u e attention to the role of experience in the d e v e l o p m e n t of an animal's k n o w l e d g e of its environment. The need for a fourth ' w h y ' question in ethology, the ontogenetic one, e m e r g e d clearly, b u t the major part of the research p r o g r a m m e in the first decade of Niko's Oxford period still dealt with

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Early ethology: growing from Dutch roots

17

studies on the evolution of behaviour, with comparative studies on the displays of different gull species f o r m i n g the core. The possibilities of giving causal a n d phylogenetic interpretations of displays on the basis of ethological h y p o t h e s e s about the organization of behaviour were so p r o m i s i n g and fascinating that it t e n d e d to be forgotten that these hypotheses still n e e d e d to be critically verified a n d m o r e explicitly w o r k e d out. Therefore, quantitative m e t h o d s applying the ethological black-box analysis h a d to be developed and techniques for recording a n d processing data h a d to be improved. Care had to be taken to avoid p r e m a t u r e conclusions about the physiological basis of the causal processes involved, an error early ethologists had sometimes c o m m i t t e d in order to m a k e their discipline look m o r e respectable. The type of w o r k required h e r e did not appeal to Niko. Moreover, in the meantime his studies on the adaptive radiation of displays had m a d e him aware of another urgent need, that for empirical assessment of selection pressures s h o w i n g natural selection at work. Filling this gap was m u c h m o r e to his liking; h e r e m e a s u r e m e n t s had to be obtained in the field, p r e c e d e d by w a t c h i n g and w o n d e r i n g . Consequently, after 1960, functional research on the adaptive n a t u r e of behaviour came to d o m i n a t e Niko's research p r o g r a m m e . This p r o v e d to be a step t o w a r d s the integration of ethology and ecology, from which in the 1970s the discipline of Behavioural Ecology emerged. It also led to his i n v o l v e m e n t in the wildlife research of the Serengeti Research Institute in Tanzania, which gave Niko a second and last great o p p o r t u n i t y to feel himself part of unspoiled nature.

--2

Studying behavioural adaptations NICHOLAS B. DAVIES

W h e n I was a schoolboy, every S u n d a y I u s e d to go to the local p i n e w o o d s a n d sand d u n e s to s p e n d the d a y w a t c h i n g birds. I wrote an account of the species I saw for the school natural history competition a n d w o n a book by Niko Tinbergen (1953), 'The Herring Gull's World'. (Some time later I discovered that m y prize was automatic as mine was the only entry.) Reading this book was a revelation. It revealed to me for the first time a whole n e w w a y of asking questions about natural history, a subject which until t h e n I h a d a s s u m e d to consist simply of m a k i n g species lists. Later, d u r i n g m y undergraduate days, the impression I got was the rather depressing one that y o u h a d to be incredibly clever to do research a n d that n e w ideas w o u l d emerge only from long hours in the laboratory or library. It was refreshing to return to Tinbergen's book, with its e m p h a s i s on patient field observation, w h i c h gave the encouraging idea that a n y birdwatcher could make a great discovery if only he h a d a spare afternoon a n d a pair of binoculars. In this essay I shall consider h o w Tinbergen's legacy has influenced the w a y we n o w s t u d y behavioural adaptations, particularly the approach a d o p t e d in m o d e r n d a y 'behavioural ecology'. Is w h a t we do n o w so very different from the work of Tinbergen and his students in the 1950s and 1960s? To w h a t extent are Tinbergen's ideas relevant to a s t u d e n t embarking on behavioural research today?

LESSONS FROM TINBERGEN I think that Tinbergen has h a d two i m p o r t a n t influences.

Lessons from Tinbergen

19

Asking questions A mark of the most creative scientists is not only the kind of a n s w e r they provide to p r o b l e m s b u t the n e w kinds of questions t h e y ask. As Tinbergen wrote in his introdution to 'The Herring Gull's World': ' A w a r e n e s s of ignorance is in itself the result of s o m e sort of understanding, the u n d e r s t a n d i n g a n d k n o w l e d g e of p r o b l e m s to be solved'. The questions Tinbergen asked were interesting because they s t e m m e d from a good k n o w l e d g e of the animal a n d its world. For example in 1963 he wrote: 'It took me ten years of observation to realize that the removal of the e m p t y eggshell after hatching, w h i c h I h a d k n o w n all along the black h e a d e d gulls to do, might have a definite function'. Then followed the f a m o u s experiments with b r o k e n shells laid out in artificial nests, which s h o w e d that their white interior attracted predators to an otherwise camouflaged nest, d e m o n strating that eggshell removal w a s i n d e e d adaptive (Tinbergen et al., 1963). Tinbergen also had a knack of asking questions w h i c h could be answered; he framed questions clearly so that the reader w o u l d think 'I k n o w h o w to a n s w e r that'. As Lorenz c o m m e n t e d in his f o r e w o r d to 'The Herring Gull's World' 'Tinbergen k n o w s exactly h o w to ask questions of nature in such a w a y that she is b o u n d to give clear answers'. Tinbergen's (1963) distinction b e t w e e n the four kinds of questions (causation, function, d e v e l o p m e n t and evolution) is still very relevant today and his 1963 Zeitschrift paper still stands as a valuable reference on s t u d e n t reading lists.

Answering questions Tinbergen not only had a genius for asking g o o d questions, in contrast to Lorenz he also followed u p his intuition b y r i g o r o u s testing of his h y p o t h e s e s . Here his main contribution was to s h o w that the field can be u s e d as a laboratory for observation and experiments. Tinbergen was not the first to do field experiments of course, but he w a s o n e of the first to collect quantitative data, to do careful controls, and to influence others b y his example that field experiments were valuable for dissecting both cause and effects of b e h a v i o u r patterns. By controlling variation ourselves in an experiment w e can eliminate the possibility that another variable correlated with the feature u n d e r s t u d y is the cause or effect of an event, e.g. is it the red spot on the p a r e n t ' s bill that causes pecking b y the chicks,

20

Studying behavioural adaptations

or s o m e other feature? Experiments can be u s e d to increase the range of natural variation to create circumstances that rarely or never occur. A n d e r s s o n (1982) u s e d this to g o o d effect w h e n considering the question of w h y male widowbirds Euplectes progne have such extraordinarily long tails. H e s h o w e d by experimentally elongating tails not only that males with longer tales attracted m o r e females, b u t also that increasing tail length b e y o n d that normally o b s e r v e d increased the n u m b e r of mates. T h u s female preference selects for still longer male tails and the observed tail length must represent a balance b e t w e e n the opposing forces of natural selection a n d sexual selection. Tinbergen's emphasis on the importance of the 'animal's world' also s h o w e d the value of the comparative m e t h o d . Different species are expected to have adaptations relevant to their different worlds, as s h o w n for example b y the differences in parent and chick b e h a v i o u r b e t w e e n the black h e a d e d gull Larus ridibundus and the kittiwake Rissa tridactyla, w h i c h reflect differences appropriate to their different nest sites, on the g r o u n d and on cliffs respectively (Cullen, 1957). The comparative m e t h o d is a powerful tool u s e d today to s t u d y adaptation (Clutton-Brock and Harvey, 1984), in effect using the w a y selection has d e s i g n e d species as the results of 'natural e x p e r i m e n t s ' w h e r e evolution has had to solve p r o b l e m s p o s e d by differences in ecology. All these ideas, derived from Tinbergen, form an important basis for current research. What, then, is different? Differences become obvious if one c o m p a r e s any m o d e r n textbook on animal b e h a v i o u r with Tinbergen's 'Social Behaviour in Animals' (2nd e d n 1964, reprinted 1990). I shall highlight four differences in the e m p h a s i s of research today.

DIFFERENCES IN CURRENT RESEARCH Measuring the success of behavioural design When Tinbergen referred to the 'survival value' of behaviour, he clearly recognized that this m e a n t 'fitness consequences'. H e asked h o w the behaviour helped the animal in maintaining itself and its offspring. There have been two major changes in current thinking about design success. First, thanks to Hamilton (1964), we n o w realize that behaviour can be f a v o u r e d by selection not only because of its beneficial effects on d e s c e n d e n t kin (offspring) b u t also b e c a u s e of beneficial effects on non-descent kin (e.g. siblings). Second, the d e v e l o p m e n t of the theory of evolutionarily stable strategies (Maynard Smith, 1982) has s h o w n that there m a y not be a single 'best' design for a b e h a v i o u r pattern.

Differences in current research

21

W h e r e the success of a strategy is f r e q u e n c y - d e p e n d e n t , the stable o u t c o m e of selection m a y be for variability in the p o p u l a t i o n (e.g. variability in male d u n g f l y Scatophaga stercoraria waiting times at a cowpat; Parker, 1970).

Studying trade-offs Tinbergen e m p h a s i z e d that there are conflicts b e t w e e n different selection p r e s s u r e s and so characters m a y r e p r e s e n t a c o m p r o m i s e . For example, black-headed gulls do not r e m o v e eggshells at once but wait until one or two hours after hatching. Two factors m a y favour a delay. First, the chick n e e d s time to free itself completely from the shell: too early removal m a y hurt the chick. Second, n e w l y hatched chicks are w e t and easily swallowed by predatory neighbours; by waiting until the chick has dried out a n d b e c o m e fluffy, and so less easily s w a l l o w e d , the parent decreases the chance of that chick being predated during the brief absence to remove the shell. The result is a compromise: r e m o v e the shell 'not too early b u t not too late' (Tinbergen et al., 1963). This idea is very influential today, with mathematical m o d e l s u s e d to measure trade-offs quantitatively and so predict optimal design (Stephens and Krebs, 1986). Design features of b e h a v i o u r are often linked to life history theory to predict, for example, h o w much a parent should risk for its y o u n g at the expense of its o w n survival (Regelmann and Curio, 1986; Dijkstra et al., 1990).

Individual differences O n e of Tinbergen's main interests w a s to u n d e r s t a n d w h y different species b e h a v e d in different ways. H e realised that to u n d e r s t a n d these differences y o u h a d to look at h o w b e h a v i o u r w a s of advantage to the individuals of the species, so he s t u d i e d individuals to reveal the significance of species-specific b e h a v i o u r patterns, for example removal of eggshells, fear of cliffs, and crypsis (Tinbergen, 1974). David Lack too w a s especially interested in species characteristics. His book on the robin Erithacus rubecula (Lack, 1965) is all about what the species does: w h y it d e f e n d s territories, w h a t its lifespan is, a n d so on. Likewise, Lack's interest in clutch size w a s to u n d e r s t a n d w h y selection has f a v o u r e d a particular average clutch size for the great tit Parus major and the swift Apus apus (Lack, 1966). His interest in breeding s y s t e m s w a s to u n d e r s t a n d questions

22

Studying behavioural adaptations

such as w h y s o m e species are m o n o g a m o u s while others are p o l y g a m o u s (Lack, 1968). While these remain important p r o b l e m s for study, m u c h current w o r k is a i m e d at u n d e r s t a n d i n g individual differences within a population. Long-term studies are m a d e , often over individuals' lifetimes, to elucidate w h y s o m e individuals d e f e n d territories while others do not, w h y s o m e individuals lay larger clutches or have more mates than others. Individual differences are the raw material for natural selection a n d s t u d y i n g t h e m can be useful both for u n d e r s t a n d i n g adaptation a n d selection in progress (Grafen 1988). A good example of h o w a long-term s t u d y of individual differences is s o m e t i m e s n e e d e d to u n d e r s t a n d the adaptive significance of design features is the s t u d y b y Clutton-Brock et al. (1982; 1984) of maternal b e h a v i o u r in red deer Cervus elaphus. Individual differences in birth weight and early growth affect adult size and reproductive success, especially in males. This p r o b a b l y explains w h y hinds allow sons to suckle almost twice as frequently as daughters, even t h o u g h this is costly to the mother. Rearing a son increases the chance that the m o t h e r will die the following winter and r e d u c e s her chance of breeding successfully the next year even if she d o e s survive. The lifetime reproductive success of a son increases more rapidly with the m o t h e r ' s quality (related to d o m i n a n c e rank, w h i c h is correlated with b o d y size) than d o e s the lifetime reproductive success of a daughter. All females breed, e v e n poor-quality individuals. H o w e v e r , because of intense competition for harems, only good-quality males can gain mates. The most successful males, which gain large harems, have the highest lifetime reproductive success of all individuals. Thus d o m i n a n t hinds, able to p r o d u c e goodquality sons, w o u l d maximize their reproductive success b y biasing their sex ratio t o w a r d s male offspring. S u b o r d i n a t e mothers, unable to raise g o o d male competitors, w o u l d do better by p r o d u c i n g daughters. These predicted biases in the sex ratio were, in fact, observed. N o n e of these results could have been established without following individuals over their lifetime. The most important contribution of longitudinal studies (e.g. Clutton-Brock, 1988; Stacey and Koenig, 1990) is that they allow us to relate events at one stage of an animal's life history to its survival and reproductive success at s u b s e q u e n t stages. The costs and benefits of an individual's actions are often delayed and there is no w a y of measuring these realistically unless individuals are followed t h r o u g h time.

Differences in current research

23

Social behaviour: conflicts of interest In his 1964 b o o k on social behaviour, T i n b e r g e n ' s main interest w a s in h o w cooperation w a s achieved b e t w e e n individuals t h r o u g h signalling. T h u s he w a s mainly c o n c e r n e d with causal explanations of social interactions, for example h o w a stickleback's or gull's displays caused others to approach or retreat, h o w signals from the parent caused offspring to beg and h o w signals from the offspring caused parents to f e e d them. By contrast, the e m p h a s i s in current research is more on the conflicts of interest b e t w e e n individuals in relation to h o w they might best maximize their reproductive success. Recognition of conflicts of interest has played a seminal role in m o d e r n interpretations of mate choice, mating systems and parent-offspring interactions (Trivers, 1972; 1974). Some of T i n b e r g e n ' s interpretation of b e h a v i o u r in social g r o u p s w a s g r o u p selectionist. For example, he interpreted the m o b b i n g of a s p a r r o w h a w k b y a g r o u p of wagtails as b e h a v i o u r which, although of danger to the individual, was advantageous to the group. He argued that 'only g r o u p s of capable individuals survive - those c o m p o s e d of defective individuals do not, and hence cannot reproduce properly. In this w a y the result of cooperation of individuals is continually tested and checked, and thus the g r o u p d e t e r m i n e s ultimately, t h r o u g h its efficiency, the properties of the individual'. (Tinbergen, 1964; n e w edition 1990). In his later writings, Tinbergen (1973) argues clearly against the idea of g r o u p selection, e m p h a s i z i n g that cooperation comes a b o u t because individual participants gain an advantage. H o w e v e r he did not s t u d y the conflicts b e t w e e n individuals which underlie even apparently cooperative enterprises such as g r o u p m o b b i n g or breeding. O n e of the reasons for these differences in e m p h a s i s is that behavioural ecologists have focused mainly on the fitness consequences of behaviour, w h e r e a s Tinbergen gave equal time to studies of both causation a n d function. H e w a s interested not only in w h y the blackh e a d e d gull r e m o v e d eggshells, in the sense of w h a t good it did t h e m but also in the stimuli w h i c h elicited removal (Tinbergen et al., 1962). For example, he s h o w e d that various characteristics such as a 'thin edge' elicited removal (a whole egg with a flange glued to it was removed), w h e r e a s others such as ' s h a p e ' did not (a half egg filled with plaster of Paris w a s rolled back into the nest). B e h a v i o u r a l ecologists, b y contrast, h a v e largely i g n o r e d mechanism. In the rest of this essay I shall discuss one of the 'hot topics' in behavioural ecology, n a m e l y helping at the nest, to s h o w the relevance of three aspects of the Tinbergen legacy to t o d a y ' s

24

Studyingbehavioural adaptations

research: a) the importance of distinguishing different kinds of question a b o u t behaviour; b) the usefulness of s t u d y i n g both m e c h a n i s m a n d function together, and c) the role of field observation and experiments.

LINKING CAUSAL AND FUNCTIONAL STUDIES OF HELPING AT THE NEST In m a n y species of birds the y o u n g are fed not only b y their p a r e n t s b u t also b y one or more 'helpers'. The question arises, w h a t benefit does a helper gain from such altruism? W h y d o n ' t helpers go off a n d rear their o w n y o u n g instead of helping others to breed? Field studies have revealed that in m a n y cases the helpers are p r e v i o u s offspring of the breeders. They remain at h o m e often because the habitat is full, so there are no breeding vacancies. Because the y o u n g in the nest are sibs of the helper, the helper can increase its genetic fitness b y feeding t h e m (Brown, 1987; Stacey and Koenig, 1990). The traditional behavioural ecology view of helping is therefore that ' g e n e s for helping' have spread by kin selection. This interpretation has recently b e e n criticized by Jamieson a n d Craig (1987; see also Jamieson, 1989). T h e y p r o p o s e that individuals have simple 'provisioning rules' f a v o u r e d in the context of parental care. Such a rule might be 'Feed begging chicks in m y territory'. W h e n the habitat is full and juveniles remain in their natal territory, they encounter nestlings w h e n their parents have another breeding attempt and the presence of the begging chicks elicits provisioning. The standard reply to Jamieson a n d Craig has b e e n that theirs is a causal explanation of helping (i.e. w h a t elicits feeding) w h e r e a s behavioural ecologists have b e e n interested in a different level of analysis, namely its functional significance (Sherman, 1989; Ligon and Stacey, 1989, Koenig and M u m m e , 1990). H o w e v e r , I do not think that this is the key issue. Jamieson and Craig are suggesting that 'helping' is not a trait. Rather 'provisioning' is the trait and helping is simply a b y - p r o d u c t of a rule f a v o u r e d in the context of parental care. Their point is that helping b e h a v i o u r m a y not have arisen b e c a u s e of the s p r e a d of a 'gene for helping'. Just b e c a u s e helping brings a benefit does not m e a n that selection has specifically f a v o u r e d it as a trait. In his 1963 paper, Tinbergen highlights this p r o b l e m w h e n he refers to a difficulty ' c a u s e d by our habit to coin terms for major functional units and treat t h e m as units of m e c h a n i s m ' . To examine Jamieson and Craig's h y p o t h e s i s w e n e e d to look at the design of helping b e h a v i o u r , to u n d e r s t a n d alternative mechanisms, before w e can ask sensible functional questions. O u r

Linking causal and functional studies of helping at the nest

25

functional questions n e e d to be of the form ' W h y does this animal do x w h e n it could do y?' Selection chooses b e t w e e n alternative mechanisms; which alternatives are available is important for any functional argument. So the key question is: is 'not helping' an alternative? Or do individuals blindly follow a crude provisioning rule? U n d e r standing the m e c h a n i s m will tell us w h e t h e r w e s h o u l d be m e a s u r ing the costs a n d benefits of 'provisioning' or of 'helping'. S o m e recent studies have s h o w n that individuals do not always provision chicks but rather do so only w h e n they are likely to e n j o y a genetic gain from doing so. For example, white fronted bee-eater Merops bullockoides helpers almost always only help feed the offspring of close relatives and furthermore, given the choice b e t w e e n helping close versus m o r e distant kin they almost always choose to help the closer kin. Individuals w h o do not have close relatives in the colony tend not to help (Emlen and Wrege, 1988). Such intricacy of behavioural design s h o w s that the question ' w h y help?' is a sensible one to ask, o n e that begs a functional interpretation. T w o other studies also argue against Jamieson and Craig's v i e w and provide an interesting comparison.

Acorn woodpeckers (Melanerpes formicivorous) This species is a c o m m u n a l breeder, with several related females laying in the same nest and several related males breeding in the g r o u p (Koenig and M u m m e , 1987). O n e male is dominant and m a y gain most of the mating access to the females. Limited data s h o w there can be multiple paternity in a brood. Often all the breeding males help to feed nestlings. A male m a y thus gain t w o kinds of genetic benefit from feeding nestlings. First he may gain 'direct fitness' benefits (Brown, 1987) from feeding his o w n offspring in the brood. Second, he m a y gain 'indirect fitness' benefits from feeding n o n - d e s c e n d e n t b u t related offspring, namely those sired b y other b r e e d i n g males (to w h o m he is related - co-breeding males m a y be father a n d son, or brothers for example). Koenig (1990) asked ' w h a t causes a male to feed the chicks?' H e p e r f o r m e d a neat field experiment w h i c h involved asking the w o o d p e c k e r s a clear question. H e r e m o v e d a male during egg laying, so that he did not have the chance to father any of the chicks. H e t h e n replaced the male during incubation to see w h e t h e r he fed the young. The experiment thus allowed Koenig to test w h e t h e r the 'indirect fitness' benefits of helping were sufficient to cause feeding. The data s h o w e d that w h e n d o m i n a n t males w e r e r e m o v e d , they d e s t r o y e d the clutch on their return to the territory, thus forcing

26

Studying behavioural adaptations

a re-nest. In control experiments, w h e r e dominant males were r e m o v e d during incubation after all the mating was over, they never destroyed the clutch; this s h o w s that it w a s their absence during the egg-laying period that i n d u c e d clutch destruction, not the removal per se. By contrast, subordinate males did not d e s t r o y the clutch, e v e n t h o u g h t h e y h a d the o p p o r t u n i t y to do so. S o m e subordinates, at least, t h e n w e n t on to help feed the nestlings (Koenig, 1990). These results s u g g e s t that for d o m i n a n t s the fitness gain from forcing a re-nest m a y be greater than the indirect fitness gain from feeding n o n - d e s c e n d a n t kin, while for subordinates the reverse m a y be true. It seems likely that d o m i n a n t s are usually able to gain greater paternity a n d so the payoff to t h e m of a re-nest m a y be more profitable. The next step m u s t be to m e a s u r e paternity bias and to calculate these payoffs to see if these different decision rules for helping in d o m i n a n t s and subordinates i n d e e d maximize fitness. The main point from this example is that by revealing differences in w h a t causes feeding of nestlings b y d o m i n a n t s and subordinates, the s t u d y can n o w go on to ask interesting functional questions.

D u n n o c k s (Prunella m o d u l a r i s ) D u n n o c k s are often p o l y a n d r o u s , with t w o males sharing a female. Unlike the w o o d p e c k e r s above h o w e v e r , the males are not close relatives (Davies, 1990). D N A fingerprinting s h o w s that b r o o d s are sometimes sired entirely by one of the males (usually the d o m i n a n t , or alpha, male) while s o m e t i m e s paternity is shared b e t w e e n alpha and beta male. The interesting result is that beta males are m o r e likely to help feed the chicks if they have s o m e paternity (Burke et al. 1989). Do the males have an equivalent of D N A fingerprinting to guide their behaviour, or do they rely on simple rules? The data s u p p o r t the latter view. First, beta males s o m e t i m e s help feed b r o o d s w h e n t h e y h a v e no paternity. S o m e t i m e s alpha a n d beta males cooperate to feed a single chick (clearly they cannot b o t h be the father). Second, w h e n the chicks fledge they are usually divided a m o n g the parents, with each male taking sole care of s o m e of t h e m until t h e y reach i n d e p e n d e n c e . There is no t e n d e n c y for a male to pick out his o w n offspring for care. H o w then does the relationship b e t w e e n paternity and chick feeding come about? Behavioural observations s h o w that a male's mating access to the female predicts paternity reasonably well and that males use their degree of mating access to determine w h e t h e r they feed the y o u n g (Burke et al., 1989). It is a simple rule which works quite well in the sense that it results in a male provisioning b r o o d s w h e r e he has some paternity.

Is behavioural ecology different from ethology?

27

This example provides a nice contrast to the acorn w o o d p e c k e r , w h e r e a s u b o r d i n a t e male will feed chicks e v e n if he has no mating access to the female. In the w o o d p e c k e r s the males are close relatives. In d u n n o c k s they are not, so there is no kin-selected benefit for a beta male d u n n o c k to help feed an alpha male's offspring. T h u s the different m e c h a n i s m s leading to chick feeding in the t w o species each make g o o d functional sense. These studies of helping at the nest illustrate the i m p o r t a n c e of linking studies of m e c h a n i s m and function. Behavioural ecologists interested in function should ask q u e s t i o n s of the form ' w h y h a v e particular mechanisms been favoured in s o m e species while different mechanisms have b e e n f a v o u r e d in others?' The subject is in part a c o m p a r a t i v e s t u d y of m e c h a n i s m in relation to e c o l o g i c a l circumstances.

IS B E H A V I O U R A L E C O L O G Y D I F F E R E N T F R O M E T H O L O G Y ? In his 1963 paper, Tinbergen b e g a n with the following warning: 'I believe that if w e do not continue to give t h o u g h t to the p r o b l e m s of our overall aims, our field will be in danger of either splitting u p into seemingly unrelated subsciences, or of becoming an isolated " i s m " . ' This t h e m e was taken u p b y Wilson (1975) w h o p r e d i c t e d that ethology w o u l d be 'cannibalized by neurophysiology and sensory physiology from one e n d and sociobiology a n d behavioural ecology from the other'. In part, Wilson's p r o p h e s y s e e m s to have b e e n fulfilled. W e n o w have separate societies and journals in neuroethology and behavioural ecology, w h i c h appears to leave ethology d w i n d l i n g in b e t w e e n . H o w e v e r I d o not think this gives a fair picture of current trends. Although in its early days behavioural ecology t e n d e d to ignore mechanism, it is interesting to note a rising interest in questions of causation and d e v e l o p m e n t . For example, optimal foraging studies began by trying to u n d e r s t a n d w h y animals preferred particular patches or prey. Recent studies have t u r n e d to questions of h o w foragers assess patch quality, h o w t h e y assess travel costs a n d other problems concerning m e c h a n i s m ( S t e p h e n s a n d Krebs, 1986). W h a t animals can do will be constrained b y the m e c h a n i s m s available to t h e m and obviously w e n e e d to u n d e r s t a n d these m e c h a n i s m s . S t u d e n t s of cooperative breeding a n d mating s y s t e m s are likewise becoming more interested in studies of causation and development. W h a t causes individuals to feed nestlings? H o w do helpers recognize kin?

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In m y s t u d y with Michael Brooke of cuckoos Cuculus canorus a n d their hosts we were mainly interested in h o w the cuckoo tricked the host a n d h o w hosts h a d evolved counteradaptations. O n e of the discoveries, using Tinbergen-type experiments with model eggs, was that m a n y hosts rejected eggs w h i c h were different from their o w n colour a n d pattern, thus explaining w h y the cuckoo has evolved a mimetic egg for these hosts (Davies a n d Brooke, 1988; 1989a a n d b). This raises an interesting d e v e l o p m e n t a l question, n a m e l y h o w do hosts k n o w w h a t their o w n eggs look like? There is an interesting developmental question to ask about the cuckoos: h o w does the cuckoo come to select the right host, namely the one for w h o m its egg is a good match? Some hosts, like the d u n n o c k , show no discrimination against eggs unlike their own. For them, the cuckoo has not evolved a mimetic egg, but this raises an interesting evolutionary question: h o w long might it take for egg discrimination to evolve in a host population? The conclusion is that students interested in behavioural adaptations should clearly not only s t u d y function, they should also look at causation, d e v e l o p m e n t and evolution. The future trend m a y well be for behavioural ecologists to rediscover ethology, n a m e l y the s t u d y a n d interrelationships b e t w e e n the four questions first asked by Niko Tinbergen (1963).

ACKNOWLEDGEMENTS I t h a n k Tim Clutton-Brock, Rudi Drent and Walter Koenig for helpful discussion.

REFERENCES Andersson, M. (1982) Female choice selects for extreme tail length in a widowbird. Nature, Lond., 299, 818-20. Brown, J.L. (1987) Helping and Communal Breeding in Birds. Princeton University Press, Princeton. Burke, T., Davies, N.B., Bruford, M.W. and Hatchwell, B.J. (1989) Parental care and mating behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature, Lond., 338, 249-51. Clutton-Brock, T.H. (ed) (1988) Reproductive Success. University of Chicago Press, Chicago. Clutton-Brock, T.H., Guinness, F.E. and Albon, S.D. (1982) Red Deer: behaviour and ecology of two sexes. University of Chicago Press, Chicago. Clutton-Brock, T.H., Albon, S.D. and Guinness, F.E. (1984) Maternal dominance, breeding success and birth sex ratios in red deer. Nature, Lond., 308, 358-60.

References

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Clutton-Brock, T.H. and Harvey, P.H. (1984) Comparative a p p r o a c h e s to investigating adaptation, in Behavioural ecology: an evolutionary approach, 2nd edn, (eds J.R. Krebs and N.B. Davies) Blackwell Scientific Publications, Oxford, pp. 7-29. Cullen, E. (1957) Adaptations in the kittiwake to cliff nesting. Ibis, 99, 275-302. Davies, N.B. (1990) Dunnocks: cooperation and conflict a m o n g males a n d females in a variable mating system, in Cooperative breeding in birds, (eds P.B. Stacey and W.D. Koenig), Cambridge University Press, Cambridge, pp. 457-85. Davies, N.B. and Brooke, M. de L. (1988) Cuckoos versus reed warblers: adaptations and counteradaptations. Animal Behaviour, 36, 262-84 Davies, N.B. and Brooke, M. de L. (1989a) An experimental study of co-evolution between the cuckoo Cuculus canorus and its hosts. I. Host egg discrimination. Journal of Animal Ecology, 58, 207-24. Davies, N.B. and Brooke, M. de L. (1989b) An expeimental study of co-evolution between the cuckoo Cuculus canorus and its hosts. II. Host egg markings, chick discrimination and general discussion. Journal of Animal Ecology, 58, 225-36. Dijkstra, C., Bult, A., Bijlsma, S. et al. (1990) Brood size manipulations in the kestrel (Falco tinnunculus): effects on offspring and parent survival. Journal of Animal Ecology, 59, 269-85. Emlen, S.T. and Wrege, P.H. (1988) The role of kinship in helping decisions a m o n g white-fronted bee-eaters. Behavioural Ecology and Sociobiology, 23, 305-15. Grafen, A. (1988) On the uses of data on lifetime reproductive success, in Reproductive Success, (ed T.H. Clutton-Brock), Chicago University Press, Chicago, pp. 454-71. Hamilton, W.D. (1964) The genetical evolution of social behaviour. I, II. Journal of Theoretical Biology, 7, 1-52. Jamieson, I.G. (1989) Behavioural heterochrony and the evolution of birds' helping at the nest: an unselected consequence of c o m m u n a l breeding? The American Naturalist, 133, 394-406. Jamieson, I.G. and Craig, J.L. (1987) Critique of helping behaviour in birds: a departure from functional explanations, in Perspectives in ethology Vol. 7., (eds P. Bateson and P. Klopfer), P l e n u m Press, N e w York, pp. 79-98. Koenig, W.D. (1990) O p p o r t u n i t y of parentage and nest destruction in p o l y g y n a n d r o u s acorn woodpeckers: an experimental study. Behavioural Ecology, 1, 55-61. Koenig, W.D. and M u m m e , R.L. (1987) Population ecology of the cooperatively breeding acorn woodpecker. Princeton University Press, Princeton. Koenig, W.D. and M u m m e , R.L. (1990) Levels of analysis and the functional significance of helping behaviour, in Interpretation and Explanation in the Study of Animal Behaviour, (eds M. Bekoff and D. Jamieson), Westview Press, Boulder, San Francisco and Oxford, pp. 268-303. Lack, D. (1965) The life of the robin. Witherby, London. Lack, D. (1966) Population studies of birds. Clarendon Press, Oxford. Lack, D. (1968) Ecological adaptations for breeding in birds. Methuen, London. Ligon, J.D. and Stacey, P.B. (1989) On the significance of helping behaviour in birds. The Auk, 106, 700-5. Maynard Smith, J. (1982) Evolution and the theory of games. Cambridge University Press, Cambridge.

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Parker, G.A. (1970) The reproductive behaviour and the nature of sexual selection in Scatophaga stercoraria (Diptera: Scatophagidae). II. The fertilization rate and the spatial and temporal relationships of each sex around the site of mating and oviposition. Journal of Animal Ecology, 39, 205-28. Regelmann, K. and Curio, E. (1986) Why do great tit (Parus major) males defend their brood more than females do? Animal Behaviour, 34, 1206-14. Sherman, P.W. (1989) The clitoris debate and the levels of analysis. Animal Behaviour, 37, 697-8. Stacey, P.B. and Koenig, W.D. (eds) (1990) Cooperative breeding in birds. Cambridge University Press, Cambridge. Stephens, D.W. and Krebs, J.R. (1986) Foraging theory. Princeton University Press, Princeton. Tinbergen, N. (1953) The Herring Gull's World. Collins, London. Tinbergen, N. (1963) On aims and methods of ethology. Zeitschrifl fiir Tierpsychologie, 20, 410-33. Tinbergen, N. (1990) Social behaviour in animals. Facsimile reprint of 1964 edition. Chapman and Hall, London. Tinbergen, N. (1973) The animal in its world : Laboratory experiments and general papers 1932-1972. George Allen and Unwin, London Tinbergen, N. (1974) Curious naturalists. Penguin, London Tinbergen, N., Kruuk, H., Paillatte, M. and Stamm, R. (1962) How do blackheaded gulls distinguish between eggs and eggshells? British Birds, 55, 120-9. Tinbergen, N., Broekhuysen, G.J., Feekes, F. et al. (1963) Eggshell removal by the black-headed gull Larus ridibundus : a behaviour component of camouflage. Behaviour, 19, 74-117. Trivers, R.L. (1972) Parental investment and sexual selection, in Sexual selection and the descent of man, (ed B. Campbell), Aldine, Chicago, pp. 139-79. Trivers, R.L. (1974) Parent-offspring conflict. American Zoologist, 14, 249-64. Wilson, E.O. (1975) Sociobiology : the new synthesis. Belknap Press, Harvard.

--3 From animals to humans ROBERT A. HINDE

As a DPhil student at Oxford I was doubly fortunate. First, m y research supervisor, David Lack, gently accepted that I was not motivated to work on the subject he h a d i n t e n d e d for me - a comparative s t u d y of the feeding ecology of crows - and, while giving me a great deal of help, g u i d a n c e and stimulation, allowed me to do w h a t I w a n t e d to, a s t u d y of behaviour. Second, Niko Tinbergen arrived in Oxford and, not yet firmly established in n e w research projects, h a d time to talk with me a n d teach me. This h a d a p r o f o u n d influence on me, and has coloured m y research ever since. Later we started to write a book together, and one of m y greatest regrets is that other d e m a n d s forced him to forgo authorship: it was a loss both to me a n d to the enterprise. Re-reading, for the purpose of this essay, some of his papers on the applications of ethology to h u m a n behaviour, I find that m a n y ideas that have n o w become widely accepted, including some that until n o w I t h o u g h t were m y own, were there already. The application of a biological approach to h u m a n behaviour has met with two major obstacles biologists a n d popularizers w h o so overstated the case that they p r o v o k e d opposition a n d derision from social scientists, and social scientists w h o d e n i e d totally the relevance of biological considerations. Tinbergen fell into neither of these groups. In his carefully argued review paper - and I refer especially to the Science article ' O n war a n d peace in animals a n d m a n ' (1968), his C r o o n i a n lecture on 'Functional ethology a n d the h u m a n sciences' (1972) - a n d in his later work on autism (Tinbergen a n d Tinbergen, 1983), he naturally pressed a biological viewpoint, but always with discretion and humility. The ' S t u d y of instinct' (1951) contained only 6 pages on the ethological study of man. Acknowledging that it h a d not yet advanced very far, -

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he d e v o t e d most of these pages to an attack on the prejudices that r e g a r d e d h u m a n b e h a v i o u r as not accessible to ethological m e t h o d s . In k e e p i n g with the Zeitgeist a m o n g s t ethologists, this w a s largely an attack on subjectivism. H o w e v e r , he included a n u m b e r of specific examples of 'processes usually considered as typical of animals (that) are also f o u n d in m a n ' - reflexes, coordination b e t w e e n r h y t h m s , aspects of motivation, 'innate releasing mechanisms' and displacement activities. 'Social b e h a v i o u r in animals' p u b l i s h e d in 1953, contained only a f e w references to c o m p a r i s o n s b e t w e e n h u m a n a n d animal behaviour. H o w e v e r , in his later p a p e r s he d e v o t e d little space to simple parallels b e t w e e n animal and h u m a n behaviour. 'What w e ethologists do not w a n t ' he wrote in his 1968 paper, 'is uncritical application of our results to man'. There w e r e at least three reasons for this. First, he felt that s o m e authors writing in the 1960s, such as Lorenz and Morris, ' p r e s e n t as k n o w l e d g e a set of statements w h i c h are after all no more than likely g u e s s e s ' (1968), t h o u g h in other respects he a p p l a u d e d their efforts to find 'the animal roots of h u m a n behaviour'. Second, he argued that most writers w h o had tried to apply ethology to h u m a n s had tried to explain h u m a n b e h a v i o u r b y selecting, from the diversity of animals' behaviour, facts to suit their theses. 'Therefore' he writes (1968) 'instead of taking this easy w a y out, w e ought to s t u d y m a n in his o w n right'. A n d third, an issue to which we shall return later, he s a w that 'both our b e h a v i o u r and our e n v i r o n m e n t have c h a n g e d so m u c h since cultural evolution began to gather m o m e n t u m ' (1972) that it is more profitable to apply the ' a p p r o a c h ' of biology to the p h e n o m e n a of h u m a n behaviour. It is evident that, during the 1950s and 1960s, Tinbergen gave m u c h t h o u g h t to the application of ethological principles to h u m a n s : in his later p a p e r s on h u m a n ethology Tinbergen referred several times to the h o u r s he and his wife had s p e n t child-watching. The application of ethological m e t h o d s a n d principles to h u m a n b e h a v i o u r w a s his primary concern. H o w e v e r , it was his pupil Blurton Jones (1972), no d o u b t inspired b y his supervisor, w h o p i o n e e r e d the application of ethological m e t h o d s to the s t u d y of h u m a n behaviour. Alongside his empirical work, Blurton Jones provided a masterly s u m m a r y of a rather extreme ethological position, laying emphasis on the need for objective description in terms of behavioural elements, with more global concepts, such as aggression, anxiety and attachment, being eschewed. This h a d s o m e important consequences, leading for instance to a distinction in child b e h a v i o u r b e t w e e n those a p p a r e n t l y aggressive acts that form part of rough-and-tumble play and true aggression. Blurton Jones's w o r k facilitated a recrudescence of observational studies

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of children's behaviour but, in m y view (Hinde, 1983), was overcritical of current work in developmental psychology. In laying emphasis on the identification of behaviour elements by 'physical description' (i.e. description in principle capable of reduction to movements of muscles, bones, etc.), the importance of 'description by consquence' and of the use of variable means to obtain a given end or goal-directedness was neglected. Whilst studies of particular m o v e m e n t patterns identified by physical description, such as those of sucking by babies (Gunther, 1955; Prechtl, 1958) smiling (van Hooff, 1972) and other adult facial expressions (Eibl Eibesfeldt, 1972, 1975), have greatly enhanced our understanding of some aspects of h u m a n behaviour, an out-and-out molecular approach has clear limitations. Stated baldly, h u m a n s are not fish, and descriptive methods that were outstandingly successful in studies of sticklebacks in the 1930s - 1950s, cannot be applied directly to the h u m a n case. Interestingly, these studies were barely mentioned by Tinbergen in his later writings on h u m a n behaviour. Instead he emphasized other aspects of behaviour that humans share with some other species - aspects which are characterized primarily by flexibility rather than by stereotyped m o v e m e n t patterns, such as exploration. Nevertheless, Tinbergen did insist that description must precede analysis and/or explanation. 'Intense, long, repeated 'plain' or 'simple' observation, guided by a truly inquiring, not prematurely prejudiced state of mind has to come first', was the Tinbergens' (1983) precept for understanding autism, and they reported that their main clues came from 'gesturing, facial and body expressions, details of where the children go, of their starting or stopping, of the orientation of their bodies or body parts etc.' - in fact, a mixture of physical description and description by consequence aimed at understanding the meaning behind actions. In understanding something like autism, they emphasized that observation and description could be more revealing if coupled with comparison with what is 'normal' (1974). However, an issue on which Tinbergen laid even more emphasis, and which arises directly from ethology's biological basis, lies in his insistence on the need to distinguish between the four questions of immediate causation, development, evolution and function, and not to neglect any one of them if full understanding is to be achieved (Tinbergen, 1963). In fact the Science article 'On war and peace' is much more than its title implies, and provides a brilliant overview of the manner in which asking each of these 'Four Whys' can help in the understanding of behaviour, exemplified by the particular problem of h u m a n aggressiveness. In discussing aggression, Tinbergen wrote of the factors determining aggression in individuals and then, unlike m a n y biologists writing at

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the time, e m p h a s i z e d that additional factors o p e r a t e d in aggression by animal groups a n d by h u m a n groups, but left o p e n h o w far the special features of h u m a n g r o u p aggression were directly derived from an animal heritage of g r o u p territoriality. Thus, while he stated in his 1968 Science article that he considered that h y p o thesis 'the most likely one', a few p a r a g r a p h s later he wrote 'Ethologists tend (my italics) to believe that we still carry with us a n u m b e r of behavioural characteristics of our animal ancestors . . . a n d that g r o u p territorialism is one of those ancestral characters'. The next sentence suggests that in using the w o r d ' t e n d ' he was trying to disassociate himself from some ethologists, for he p o i n t e d out that 'cultural evolution, which resulted in the parcelling-out of our living s p a c e . . , w o u l d , if a n y t h i n g , have t e n d e d to e n h a n c e group territorialism'. I u n d e r s t a n d Tinbergen to have m e a n t here that h u m a n territorialism as a simple r e m n a n t of our animal ancestry (as claimed for instance by some writers at that time), was at least an oversimplification. In writing about group aggression, Tinbergen e m p h a s i z e d h o w members of h u m a n groups unite in the face of an outside danger using, like other species, threat gestures against the e n e m y a n d friendly communication with members of the in-group. He also acknowledged the role of leaders in the h u m a n case, pointing to the m a n n e r in which m e t h o d s of mass c o m m u n i c a t i o n could be used to disseminate p r o p a g a n d a which exploited our aggressive tendencies. While in no way disagreeing with Tinbergen's analysis, more recent work might p u t the e m p h a s i s slightly differently. While Tinbergen e m p h a s i z e d the role of external forces in uniting groups - individuals coming together 'in the face of an outside d a n g e r ' - more recent work has been concerned with the internal forces that cause individuals to form groups a n d groups to become differentiated from each other. Social categorization m a y itself cause a significant bias in favour of same-group members. Individuals m a y be attracted to others similar (or perceived as similar) to themselves, in part because communication is easier b e t w e e n individuals w h o perceive the world similarly (Kelly, 1955, 1970), a n d also because others w h o hold similar attitudes to oneself help to confirm o n e ' s social beliefs (Festinger, 1957; Clore a n d Byrne, 1974). Furthermore, current work regards the tendencies to exaggerate the differences b e t w e e n in-group a n d the out-group a n d to see the in-group as superior, as intrinsic to the process of group formation a n d differentiation (Tajfel, 1978; Rabble, 1989). G r o u p formation also introduces m a n y n e w factors relevant to the incidence of aggression - escalation due to the desire of group members to show off their aggressiveness to their peers, or resulting from a n o n y m i t y

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within the group; g r o u p values c o n d o n i n g violence; the example of charismatic leaders, and so on. Unlike m a n y other biologists, Tinbergen did not u n d e r e s t i m a t e the role of cultural factors in h u m a n warfare. H e e m p h a s i z e d social values that m a d e cowardice despicable, the d e v e l o p m e n t of m o r e effective w e a p o n s , and the capacity to kill w i t h o u t being e x p o s e d to the suffering or a p p e a s e m e n t gestures of the victims. It can n o w be argued that w e m u s t also take into account the institutionalization of war. Aggressive propensities play little direct part in the b e h a v i o u r of soldiers in battle: rather their behaviour is influenced primarily by their rights and duties as i n c u m b e n t s of a particular role in the institution of war (Hinde, 1989, 1991). Aggression comes in, as Tinbergen noted, in that the p r o p a g a n d a helping to stabilize the institution of war plays u p o n aggressive propensities. We m u s t r e m e m b e r here not only, as Tinbergen p o i n t e d out, that h u m a n beings are p r o d u c t s of an interaction b e t w e e n their biological propensities and the physical and social e n v i r o n m e n t in which they g r o w u p - that e n v i r o n m e n t including the sociocultural structure of beliefs, values and institutions with their constituent roles and so on but also that the sociocultural structure is itself a p r o d u c t of h u m a n beings. Thus w e m u s t come to terms with dialectic relations b e t w e e n h u m a n behaviour, interactions, relationships and groups, their physical environment, and the sociocultural structure (Hinde, 1987). A n o t h e r aspect of h u m a n b e h a v i o u r concerning w h i c h Tinbergen d r e w lessons from the ethology of other species, w a s education. Impressed by the learning opportunities provided by play-like activities in animals, he questioned the balance b e t w e e n formal instruction and self-initiated exploratory activities in our present educational system. Joining m a n y educational innovators, he p l e a d e d for less inbibing of 'knowledge' and more 'self-activity', arguing that too much instruction suppresses exploratory learning and sets u p resistances against further instruction. H e stressed the n e e d for the child to be given security in order to maximize playful exploration, and he d i s c u s s e d at some length (Tinbergen manuscript) the role of adults in children's exploratory play. A c k n o w l e d g i n g the n e e d for sensitive participation (cf. Vygotsky, 1934), Tinbergen emphasized also the deleterious effects of too m u c h interference in y o u n g children's play, and the d e a d e n i n g effect of too m u c h formal instruction later. The issue into which Niko Tinbergen and his wife p u t most of their energies in the last years of their lives w a s that of c h i l d h o o d autism. They were convinced that the distinction b e t w e e n normal and autistic children is far from sharp, and application of the s a m e m e t h o d s as they had u s e d for analysing the threat a n d courtship b e h a v i o u r of -

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From animals to humans

gulls s h o w e d that a conflict b e t w e e n h y p e r a n x i e t y a n d frustrated sociality were often involved. T h e y s u g g e s t e d that w h e n this conflict becomes severe the child w i t h d r a w s a n d socialization is severely hampered. As a result of this, the child fails to learn from social interaction and exploratory behaviour. This view brought the Tinbergens into headon collision with m a n y psychiatrists, w h o believed both that autism has organic causes and that genetic factors play a determining role. This debate continues, a n d I am in no w a y c o m p e t e n t to give a view: while there has been increasing evidence that some type of organic brain d y s f u n c t i o n is involved (Rutter 1988) a n d that genetic predispositions are of importance in m a n y cases (Rutter, in press), that in no w a y argues against the views that psychogenic factors are also important, or that there is a spectrum of cases from normal to extreme autism, or that certain forms of treatment may be capable of providing marked improvem e n t in m a n y cases. The recent view that the specific cognitive defect characterizing autism involves the retarded d e v e l o p m e n t of a t h e o r y of m i n d (Baron-Cohen, 1989), is compatible with Tinbergen's thesis. In writing about aggression, education a n d autism, one issue p e r v a d e d Tinbergen's views about the possible contributions of ethology to the u n d e r s t a n d i n g of h u m a n behaviour - m a n ' s influence on his e n v i r o n m e n t . This was not merely a matter of the impact of culture, t h o u g h his Croonian lecture e m p h a s i z e d the increasing rate of cultural change and the increase in 'adjustabilty' this requires from individuals in each succeeding generation. Tinbergen was concerned also with the g r o w t h in the w o r l d ' s h u m a n population, the depletion of n o n - r e n e w a b l e resources and the accumulation of toxic wastes. While such facts are n o w well e n o u g h k n o w n , Tinbergen was a m o n g the first to realize their importance. His special concern was h o w they relate to behaviour: 'The cultural evolution is a behavioural evolution, and with it the relationship between what we are doing and what the new environment requires from us' and 'The prevention of possible disadaptation a n d the creation of a n e w a d a p t e d n e s s will be a matter of behavioural p l a n n i n g ' (1972). Tinbergen's message is of special importance because, while fully aware of m a n ' s flexibility a n d adaptability, he saw that t h e y are limited, a n d asked w h e t h e r t h e y are capable of coping with the n e w e n v i r o n m e n t s we are creating. He focused not only on global questions, but on the intimate details of e v e r y d a y life. In his essay on education he wrote: 'Once he h a d experienced these other types of child-rearing, the contrast with our m o d e r n society becomes even more striking. Relatively suddenly, conditions for under-fives have become far less conducive for play. Families are smaller. The work of fathers is done

From animals to humans

37

m o r e in th e past far a w a y f r o m h o m e , a n d is a n y w a y b e y o n d a child's c o m p r e h e n s i o n . More a n d m o r e m o t h e r s go out to w ork. Contact b e t w e e n families is r e d u c e d . T he street, until fairly recently such a widely used pl aygr ound, has b e e n m a d e unsafe by the m o t o r car. W h e n the parents are at hom e , t h e y are often tired and irritable, or r u s h e d , or p r e o c c u p i e d . C h i l d r e n see less a n d less of the craftsman-at-work, a nd of the m o t h e r doing h o u s e h o l d chores; a n d a n y w a y the mechanical d o m e s t i c appliances offer little scope for participation in such chores. W h a t I find e v e n m o r e d i s t u r b i n g is that the m o o d e v e r y w h e r e a r o u n d t he children has b e c o m e so serious. The T i n b e r g e n s h a d lived with t he Eskimos, but t here is no starrye y e d g lamo r izat i on of h u n t e r - g a t h e r e r in w h a t he w rot e. Rat her he implied a p o i n t - b y - p o i n t c o m p a r i s o n of issues w h i c h he bel i eved to be i m p o r t a n t in child d e v e l o p m e n t a n d asked w h a t c o n s e q u e n c e s the characteristics of the m o d e r n w o r l d are h a v i n g on o u r b e h a v i o u r . Elsewhere he ad dr es s ed the relationship b e t w e e n accelerating cultural change, the e x t e n d e d period of h u m a n d e v e l o p m e n t , and the generation gap. In all these cases he related the d e m a n d s of m o d e r n life to the limitations of the h u m a n individual. I c a n n o t do better, in conclusion, t han to quot e in full the last t hree p a r a g r a p h s of his C r o o n i a n lecture, w h e r e , after stating the n e e d to identify the n e w e n v i r o n m e n t a l p r e s s u r e s we are creating, he points out the r o ad that m u s t be taken: ' A n d while functional e t h o l o g y helps us in identifying these p r es s u r es , it will be the k n o w l e d g e of b e h a v i o u r m e c h a n i s m s , a n d of m e c h a n i s m s of b e h a v i o u r d e v e l o p m e n t , that will h a v e to f o r m the basis for w h a t e v e r e n g i n e e r i n g will h a v e to be u n d e r t a k e n . Th e execution of such an e n g i n e e r i n g task m a y at the m o m e n t s e e m to b elo ng in science fiction, but I am c o n v i n c e d that s o o n e r or later it will b e c o m e a political issue. K n o w i n g w h a t w e do about political decision-making, I believe that it will be useless to call u p o n p e o p l e ' s altruism or use other a r g u m e n t s of a moral nature. Rather, the scientist will ha ve to poi nt out that the p r e v e n t i o n of a b r e a k d o w n , a n d the building of a n e w society is a m a t t e r of enlightened self-interest, of e ns ur i ng survival, health and happi ness of the children a n d g r a n d c h i l d r e n of all of us - of p e o p l e we k n o w a n d love. No o n e can say h o w soon science will be called u p o n for advice, but if an d w h e n that time comes, we shall have to be better p r e p a r e d t h a n we are now . The m ai n p u r p o s e of m y p a p e r is t h e r e f o r e to u r g e all sciences c o n c e r n e d w i t h the biology of Man to w o r k for an

38

From animals to humans in teg r atio n of their m a n y a n d di ver s e a p p r o a c h e s , a n d to st ep u p the pace of the building of a c o h e r e n t c o m p r e h e n s i v e science of Man. In this effort t o w a r d s integration, animal e t h o l o g y c a n n o t s tan d aside - i n d e e d I for o n e believe that p r o v i d e d it will be g i v e n the o p p o r t u n i t y for f u t h e r d e v e l o p m e n t , it can r e n d e r i nval uabl e services. '

T h e r e is a special m e s s a g e h e r e for t h o s e i n t e r e s t e d in c o n s e r v a t i o n . T h e w o r k of biologists a t t e m p t i n g to c o n s e r v e species or habitats has b e e n less effective t h a n it m i ght h a v e b e e n because of i n a d e q u a t e regard for h u m a n be ha vi our . Physicists a n d chemists can u n r a v e l the n atu r e of a t m o s p h e r i c pollution, but ultimately the cure lies in t he h a n d s of e c o n o m i s t s a nd social scientists. We s h o u l d do well to bear Niko T i n b e r g e n ' s w o r d s c o n s t a n t l y in m i n d if w e wish to save the w or ld f r o m destruction.

REFERENCES Baron-Cohen, S. (1989) The autistic child's theory of mind: a case of specific developmental delay. Journal of Child Psychology and Psychiatry, 30, 285-98. Blurton Jones, N. (1972) Ethological studies of child behaviour. Cambridge University Press, Cambridge. Clore, G.L. and Byrne, D. (1974) A reinforcement-effect model of attraction, in Foundations of interpersonal attraction, (ed T.L. Huston) Academic Press, New York. Eibl Eibesfeldt, I. (1972) Similarities and differences between cultures in expressive movements, in Non-verbal communication, (ed R.A. Hinde) Cambridge University Press, Cambridge. Eibl Eibesfeldt, I. (1975) Ethology. Holt, Rinehart & Winston, New York. Festinger, L. (1957)A theory of cognitive dissonance. Rowe, Peterson, Evanston, Illinois. Gunther, M. (1955) Instinct and the nursing couple. Lancet, 1955, 575-78. Hinde, R.A. (1983) Ethology and child development, Mussen Handbook of Child Psychology, Vol. II (eds M.M. Haith and J. Campos), Jon Wiley, New York pp. 27-94. Hinde, R.A. (1987) Individuals, relationships and culture. Cambridge University Press, Cambridge. Hinde, R.A. (1989) Towards integrating the behavioural sciences to meet the threats of violence and war. Medicine & War, 5, 5-15. Hinde, R.A. (1991) (ed.) The Institution of War. Macmillan, London. Hooff, J.A.R.A.M. van (1972) A comparative approach to the phylogeny of laughter and smiling in, Non-verbal communication, (ed R.A. Hinde), Cambridge University Press, Cambridge. Kelly, G.A. (1955) The psychology of personal contacts. Norton, New York. Kelly, G.A. (1970) A brief introduction to personal contact theory, in Perspectives on personal contact theory, (ed. D. Bannister), Academic Press, London.

References

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Prechtl, H.F.R. (1958) The directed head-turning response and allied movements of the h u m a n body. Behaviour, 13, 212-42. Rabbie, J.M. (1989) Group processes as stimulant of aggression, in Aggression and war, (eds J. Groebel and R.A. Hinde), Cambridge University Press, Cambridge. Rutter, M. (1988) Biological basis of autism, in Preventative and curative intervention in mental retardation, (eds F.J. Mendascino and J.A. Stark), Brookes, Baltimore. Rutter, M. (in press) Autism as a genetic disorder, in Advances in psychiatriic genetics, (eds P. McGuffin and R. Murray), Heinemann, Oxford. Tajfel, H. (ed) (1978) Differentiation between social groups. Academic Press, London. Tinbergen, N. (1951) The study of instinct, Clarendon Press, Oxford. Tinbergen, N. (1953) Social behaviour in animals. Methuen, London. Tinbergen, N. (1963) On the aims and methods of ethology. Zeitschrift fiir Tierpsychologie, 20, 410-33. Tinbergen, N. (1968) On war and peace in animals and man. Science, NY 160, 1411-18. Tinbergen N. (1972) Functional ethology and the h u m a n sciences (Croonian Lecture). Proc. Royal Society of London, B, 182, 385-410. Tinbergen, N. (manuscript). The importance of being playful. Tinbergen, N. (1974) Ethology and stress diseases. Science, NY 185, 20-7. Tinbergen, N. (1983) 'Autistic' children. Allen & Unwin, London. Vygotsky, L.S. (1934) Thought and language. MIT Press, Cambridge, Mass.

--4 War and peace revisited FELICITY A. HUNTINGFORD

INTRODUCTION The aim of this paper is to identify the influence of Niko T i n b e r g e n ' s ideas on the m o d e r n s t u d y of the m e c h a n i s m s that control behaviour. To do this, it is necessary first to give an account of Tinbergen's views on the subject, then to see h o w these ideas were d e v e l o p e d in the light of the research that they stimulated (the second wave of ethology), and lastly to identify those aspects of m o d e r n theory on the causation of behaviour that can be traced back to Tinbergen's ideas a n d scholarship. While the first of these steps is easy (because Tinbergen wrote so well) and the second relatively easy (because this topic is already well reviewed), the last has p r o v e d surprisingly difficult. I have chosen to illustrate this paper with reference to aggression, partly because Tinbergen u s e d this behaviour to illustrate m a n y of his ideas about causation a n d partly because the s t u d y of aggression illustrates very clearly the problems of m o d e r n research into behavioural mechanisms. The title of the paper refers to an article Tinbergen published in 1968 called ' O n war a n d peace in animals a n d m a n ' in which he spelled out his views about the causation of aggression, as well as its d e v e l o p m e n t a n d functions.

TINBERGEN'S VIEWS O N THE C A U S A T I O N OF A G G R E S S I O N Tinbergen's views on the m e c h a n i s m s that cause animals to fight,

Tinbergen's views on the causation of aggression

41

as e x p o u n d e d in 'The s t u d y of instinct' (1951), concern both the external stimuli a n d the internal factors involved.

The role o f external s t i m u l i Fighting is triggered by one or a few relatively simple key features of an o p p o n e n t (the sign stimuli), other factors being ignored. These key features t e n d to be those that characterize a rival (usually an individual of the same species and sex). The red chest of the breeding male three-spined stickleback is the most famous example (Figure 4.1), of which Tinbergen wrote ' . . . the fish reacted essentially to the red and neglected the other characteristics'.

N

Figure 4.1 The dummies used by Tinbergen in his study of the stimuli that cause aggression in sticklebacks. R indicates dummies with red undersides that were attacked. N indicates an all-silver dummy that was not attacked (from Tinbergen, 1951).

42

War and peace revisited

Increasing temperature and day length

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Suitable territory site

Territorial centre

I i

I

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.

centre

~ centre

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Figure4.2 Tinbergen's hierarchical model of the control of reproductive behaviour,

including aggression, in sticklebacks. Action-specific energy accumulates in and flows between centres at different levels in the hierarchy as sign-stimuli become available; the energy is finally released as the stickleback performs overt behavioural responses (from Huntingford, 1984, after Tinbergen, 1951).

The internal organization of aggression These key attack-eliciting stimuli interact with a s y s t e m inside the animal that controls the performance of aggression. Tinbergen depicted this as a hierarchical set of control centres at different levels (Figure 4.2). Considering the stickleback again, w h e n external and internal conditions are right (for example, w h e n d a y lengths and t e m p e r a t u r e are increasing in spring) e n e r g y accumulates in the highest level reproductive centre. This energy is prevented from flowing to the next level by a block, which is r e m o v e d b y the appropriate sign stimulus (a suitable territory). Once the stickleback is on its territory, energy accumulates in the territorial centre where, once again, descent to the next centre is blocked. The sight of an intruding red male r e m o v e s

Tinbergen's views on the causation of aggression

43

this block, so that the aggression centre is activated. D e p e n d i n g on the exact stimulus p r e s e n t e d b y the rival ( w h e t h e r it bites, threatens or flees), the energy flows d o w n to the next level a n d so on until the lowest units are activated and the appropriate action is p e r f o r m e d . Although this model was based on behavioural data, Tinbergen m a d e use of existing physiological information a n d clearly s a w the centres as anatomically localized neural entities; in other words, it is a software m o d e l with strong h a r d w a r e elements. The m o d e l postulates a specific, unitary drive, in that there is just one single system that controls aggression and does not control any other kind of behaviour. In addition, c o u c h e d as it is in terms of flow b e t w e e n centres a n d dissipation of drive, Tinbergen's m o d e l is clearly b a s e d on the concept of drive as an activating or energizing process. O n e special feature of this f a m o u s and widely q u o t e d m o d e l is the m o d e s t w a y in w h i c h Tinbergen treated it. Thus he writes: 'I s h o u l d like to e m p h a s i z e the tentative nature of such an attempt (at synthesis). While such a graphic representation m a y help us to organize our thoughts, it has grave dangers in that it tends to make us forget its provisional a n d hypothetical nature', and again, 'It should be e m p h a s i z e d that these diagrams represent no more than a working h y p o t h e s i s of a type that helps to p u t our t h o u g h t s in order' (Tinbergen, 1951). This is an object lesson of h o w models should be regarded, especially by their inventors.

Interactions between aggression and other motivational systems W h a t h a p p e n s during a fight d e p e n d s not just on the state of the aggression s y s t e m b u t also on a a second s y s t e m activated b y the presence of a rival, namely fear. W h e n an animal is simultaneously motivated to perform aggression and fear responses, these s y s t e m s interfere with each other's expression. Instead of performing either in its pure form, the animal s h o w s s o m e sort of agonistic display. This view of the causation of displays is usually referred to as the conflict theory. It is interesting to note that Tinbergen explains this dual system of control in terms of the cost of intense, uninhibited fighting, anticipating games theory analyses of animal fights by some 20 years. According to Tinbergen's conflict theory of the causation of agonistic displays (Figure 4.3), w h e n the level of activation of aggression and fear is low, each is expressed incompletely and the animal s h o w s intention m o v e m e n t s or ambivalent p o s t u r e s c o m p o s e d of elements of both. In contrast, w h e n both are strongly activated, there is

44

War and peace revisted

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