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

Printed on permanent acid-free text paper, manufactured in accordance with the proposed ANSI/NISO Z 39.48-199X and ANSI Z 39.48-1984

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

Introduction

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.

--1

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.

4

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.

0

QJ

a~

O ~

~.~

t'¢3

~2 ~.~ . ~

i! iilii !~i i i i l i ilii ii iii iilii I[t ii i i ii i i ~ ! ~ i i i i ii iii i ii~ i i !i iii!iiiiiiiiiiiiii!iii!ii]!iii!iiiiiiiiiiiiiiiiiiiiiiiiilti,iil ii!iiliiiiii i ii%,iii!!iiii! i!iiliiiiiiiiiiiiiiiiii iiii!iii!iiii!iiiilti,liiiiiiiiill iiiiiiiiiliiiii,!i!iiiii!iiiiliiiiiiiiiiii!i!ii !ii,i,iiiiiiiiiii!iiii!i!ii !i!iiii!t i!iiiiii!i!!iii!i!iiiiiiiii!! i!!iiiiii!i!iiiiiiiiii i!i iiiiii!ii,i ii!!£iliiiiiiii!iiiiii!iii !iiiilii iiiiiii iiiiii i!!i!iii!i!iiii!iiiiiii!i!ii!ii

:

iiiiiiiiiiiiiiiii!iiliiiiiiliiiiliiiiill i~+ iliiiiiliilii~ili iiiiiiiliiii =iiili!iiiiiiiiiiiii ii !ililiiii!iiiii ii ii iiiiiili i iiiiiiiiilii i i ii i ii i~iiii iiiiii ii ii i i iii ii iii i ii i i ! , i i i i iili~i~iiiiiii ii i ! i i i i i ii ~!= i ! i i ! ii iiiii i i l i iii= i i ! !ii i i i ! iii i ! ii i !iii:ii:!iiiiiiiiii:iii:iiiii i~QI!I:I:!:!I!I!:!:!I!i:!i!i:!:i ~!:!:!i:!i:ili::i :!ii%1!:!:!:i!:!: ii!!!i:!:!:!ii:!:!iiI:!i:!:!:!:!i :i:i:!:!i:!::!:i:!h:li:!: ii!:::i:!:!!i:!:!::ii i iili i i i i i ii!i iii i i ii iiiiiii i ii iiliiiiiiiiiii:i:iiliiiii!ii~i~iiii!iii ........................................... !iii:iiIiiiii i:iiii iii iiiiiiiii ii ii ~=~ii iiiiiiiii!!! !i i iii!ii!£i!!ii ii!!ii ! ilili!iiiii i i!!! i!! ! i ii i! !! i=iiiili!!iii iii ii! i i! i~ i ii ii!!iiilii!i!~!!ii! ii!!ii!! !! :i::!:!i: iiii$iiiiiiiii11111!iiiiii11111111111iili11111111111 iiiiiiiiiiii1111111111 ~i!1111 iiii111111ilii iiiiii11111 iiii!iiiii11 111111111111131111111 ~ 111111ilililiiiliiiililiiiii iii1i!iiiili1 :iiii!iiqiliiii!!1iiii3ili~iiiilililiiiii!!iiiililili1!1ilililililili1 iiiii!:iiiii:ilii:!i!:i:ii!ili:!:iiiiii:iii:!i:i:iiii:ill !iii i i ~ ililili1!i!ii!i!iili!iiii!i!ii ~1ilililiiililii1!!1ilii!!ilililililililii i:ii!i!tii¢i:!i!iiiiii:i:!:i:i:i:!:!:!:i:iiii:!@ !8 iii:i:i:i:i:iiii!:i:i:i:!:i:i:i:i:i:iis~:i:i:i:i8 i!iiililii!!1ili!!i1!8i!iiiii8iiili

iii

.................................."%:iiiiililiL}iiililiiiBiiiiiiiiiiiiiiiliiii ... :::::==;;=:; iL ~=;::;:::: =::::;:=:==:===:IBItiiiiiiiiiiiiiBi@Ii!!I!IiiiiI~Jliiiiiiiiiil i ~iii!

!iiiiiiili! ililililiiiliiililililiiiiiliililiiililiiilililiilili!i!iliiiiilililili

i~ii!ii~+ii ~iiiiii

iliiiilii!i!i iiiliiiiiliiiiiiliiiiii!ii!iiililiilililililili!iiiiliiliiiiliiliiiiiilili :

i;

:::

;i~:~

:

:

iilii;ii!i!iilii!i!iiii!i!iililii!!iilii!iilii~i!iii!ili ~ii~iiilililililii!iili!iililii!iiili£;iii ilililililii!!iilii!ililii!iililii!ilili;!;i ilililili!ililii!iililiii:ili!;!iili!!ii iiiit~ii;i;ilii;i ii ~iliiii!iiii!ii iiI !;iliii!;ililii]ili;iilili!;!iilii;ilililiiilililiii:i;iilili;i :::::::::::::::::::::::::::::::::::::::::::::::::::::::::::::::::::::::::::: : : : : : : : : : :N : : : : : : : : : : : :

.......... ................. ::::::::::::::::::::::::::::::::::::::::::::

.......... 4 .......... :::::::::::::::::::::::::::::::::

................. :::::::::::::::::::::

~

iilili~ii!iiliiliIii!iliii;ili;==ilili:i:ili:!ii!i!iili:ilili;ililililili;ili !8ii8iii!1ii8;i8ii ~;~8~B~;~;~8;~}~;~;;~;~;;~;~;~;;~t~;~;~;~;~;~;~;t~;;~ ii~ili;~iiili ii!ili!iiiili;!!I!ii;!iii!i ii!ii;iii i!i;iiili;ii!88isi;i; iii= i ~ i ii iii i iliiiii iiiii iiiiiii iiliiiiiiiiiii!ii! iili iliiiiiiiii:iii:iii:iii ili::iiiiiiiiiilii::iiilI£iliiiiliili:::i iliii~iliii=iililiiliiiiiiiiiiiii:i ilili ili ii ii ii i=!i!ii!i i i i!iiii~ilii~@i iilili!! ii ii~ iiliii i i !i i i ii! i = i ii ~i i i i i :::::::::::::::::::::::::::::::::::::::::::::::::::::: ::::::::::::::::::::::::::::::::::::::::::::::::: iiiltli BiiiiilIIiilII iliii!ii iili iiiiiliilii:ii ililii:iiiii:iili iliiii ii:iilii: ii%i:t iiii iliiiiii iI iiliii::iii:iii:iq i:qlii:ii::iiii::iiiii:iii:~iiiiill i::ii:iiiiiiiii:ii:iiiiiii::ii ~iliii::::ii:iiI iaii:ii::7 iiiiiiiiiiiii:::::: iiiiiill ii!ili iili~iiiiiiii iiiii! i ii ii iiiiii i!iii i iliii ~ i i ii~il ii! i iiii!iiiiiii !iiiii i i i ~ililii!iilii!i! !ililii! ii ii ii!i!iilii I!iililililii ilii ~i!i!iiii!iili!i!iili~iii~!i!iiilIi!iilililili~i!i!i!iliiiilI!iiilililililiililililililiii!IiliQ!IiiI!IilililiI£IilililililiI!iililili!IilIi£Iililililili:ilililililiii "ii!iliii ilililii iliiiliiiliiii!iiii::iii!i i: ilililii!iiiili:i:ilii:ili::iii iiiiiii!iiiiiiiili

!~ iiliiiiiliiiii!ilii~ i iiiililiIliiii!iliiilii!i ~ iiliiiiiliililii i i!ii iili!!Iiililiiliililililili!iliiiliiiiili!! @!iilililiii liiiliiililililii!iii ~.iliiliiiii !iiliiliiiii!ili!i iiiiI!iilililiiliilililQIiii i ilililili ~ iililiiiliiiiiiiiiiiiliiiiiiiiiilii iii]~ii;]E~ilii

iiii~i

iliii iiiiiiiiiiilii iiiii@ 8!ii ?~ii ~ii i]ii!iiliili!iliili~iliI@~ii!ii!!iiiii]iiliiiliili]!~;ii:i!:iiii ii ~iiii!!i :ti:i:ii@ii!@ , )H iiii:ii:!!i:i:i!:i:i

.................... === ====~ ...............=ii .iiliii .......~==i¢iiiilIiiiiiilIiiiiiiiii~I ....................Ii..li.!.Ii.i.i..lI.i.l.i.i.R..Ii..i.i.i~.i.i............................................. .i.i.iilii ii!i!iiliiliii!iii!iiiililiililiii~ ii iili ii i == i i i i i i iiiiiiiiiiii!iiiiiiiiiiiiiiiiiiliiiiiliiiiii!~ iiiiiiii!i!iiii iiili tiiiiiiii:iiiiiiii! ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ...............................................................................

i!!i!ilili

= !ii!i!

~,~iiiiiiii iiiiiiiiii!iiiiiiiiiiiiilii!iiiiiiiiiiiiiiiiiiiiliiliiiiiiiiiiiiiiiiiillii iiiiiiliilii iiiiiiiiiili lii!iiiliiii!iii iiiliiiiiiiiiiiiiiiiiiiiiiiiiiiiii !iii i iii

ii!

isl

! ni:i:i:i:i:iiiiiiii!i h i

i iiiiii~!ii iii

8

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

(,~ ~

.~

m

~

0

m

~.;~

.~E

.N~

~.~

• 0

.g~ L~"~

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?

28

Studying behavioural adaptations

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

29

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.

30

Studying behavioural adaptations

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, -

32

From animals to humans

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

From animals to humans

33

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

34

From animals to humans

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

From animals to humans

35

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 -

36

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

39

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

I Reproductive J centre "~

÷

Suitable territory site

Territorial centre

I i

I

Red male intruder

I

i i

f

J

.e ,n0 ! l oore 'vel l °u "noI .

.

centre

~ centre

.

centre

+

~

cenl-re

~

centre

. . . . . .

centre

Intruder bites

!

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

Overt attack

o co

Displacement

¢.. O o

Ambivalent

<

Flee

Approach

Fear tendency Figure 4.3 Graphical representation of Tinbergen's conflict theory of agonistic behaviour. Actions performed during a fight depend on the level of two independent drives, namely aggression and fear.

complete m u t u a l inhibition. The motivational e n e r g y that accumulates in the relevant centre t h e n sparks over into a completely different s y s t e m (such as nest building) w h o s e activation result in the performance of displacement activities - actions p e r f o r m e d out of context that are irrelevant in both functional a n d causal terms. A classic example is the performance of s a n d digging (a c o m p o n e n t of nest building) by male sticklebacks at the territory b o u n d a r y , w h e r e aggression a n d fear are both strongly activated (Tinbergen, 1951).

T H E S E C O N D W A V E OF E T H O L O G I C A L R E S E A R C H Tinbergen's writings, with their lucid a n d critical account of his

The second wave of ethological research

45

ideas, h e l p e d to stimulate a great deal of behavioural research in the 1960s and this inevitably led to a revision of m a n y of his ideas.

External stimuli As far as aggression is concerned, it is n o w clear that the concept of attack as a blind, reflex-like r e s p o n s e to o n e or a f e w k e y stimuli is quite wrong. Taking the case of the breeding male stickleback, it is not at all easy to get the fish to r e s p o n d to m o d e l s (this in itself casts d o u b t s on their relevance of details such as shape) a n d w h e n they do respond, red m o d e l s tend to be attacked less than grey ones (Rowland and Sevenster, 1985), except possibly w h e n the m o d e l is very close to the nest (Collias, 1990). In addition, the probability that an intruding male will be attacked d e p e n d s on m a n y details of the rival - h o w big it is, w h e t h e r the resident has met it before and, if so, w h a t h a p p e n e d (Rowland, 1988a) - and on the circumstance of the e n c o u n t e r - w h e t h e r there is a nest on the territory, w h e t h e r the nest contains young, and w h e t h e r there is a p r e d a t o r p r e s e n t (Wootton, 1970; Huntingford, 1977; U k e g b u and Huntingford, 1988). These are all features that determine the costs and benefits of engaging in a fight. Clearly, attack in sticklebacks and in m a n y other animals (Archer, 1987; Huntingford and Turner, 1987) is the result of a complex decision-making process rather than a blind response to a sign stimulus.

The internal organization of aggression The second w a v e of ethologists identified a n u m b e r of w e a k n e s s e s in Tinbergen's formulation of motivational systems. The problems with unitary drive theories and energy m o d e l s have b e e n extensively discussed, most especially by H i n d e (1960; 1966), so these will be m e n t i o n e d only briefly here. Energy models Analysis of the effects of deprivation a n d of the factors that bring behavioural s e q u e n c e s to an e n d do not s u p p o r t the idea that actionspecific energy accumulates during quiescent periods and is dissip a t e d by action. In the case of aggression, responsiveness certainly changes in animals that are p r e v e n t e d from fighting, and the performance of aggressive actions influences the internal state of the animals concerned (Archer, 1987; H u n t i n g f o r d a n d Turner, 1987).

46

War and peace revisited

SYSTEMS Aggression

ACTIVITIES Mouth fight Chase Butt Tail beat Frontal display Lateral display

S. bend

Flight

¢ ....................................

I

I~ represents one-way facilitatory effects ~ represents mutually inhibiting interaction -~ represents output from sexual & parental systems (not shown)

Figure 4.4 A model of the organization of territorial behaviour in a reef fish Tilapia mariae, (simplified after Baldicini, 1971).

H o w e v e r , this process is m u c h more complex than the simple buildu p and dissipation of energy depicted in Tinbergen's model. A w e a k n e s s of Tinbergen's motivational m o d e l is the o n e - w a y flow of information it envisages and its c o n s e q u e n t failure to a c c o m m o d a t e the various forms of feedback that we n o w k n o w to occur during fights (and other activities, McFarland, 1971).

Unitary drives Detailed analysis of the temporal patterning of the various actions s h o w n t o w a r d s potential rivals often d e m o n s t r a t e s the existence of g r o u p s of co-occurring b e h a v i o u r patterns. This justifies postulating a c o m m o n causal factor influencing performance of all the actions. If such groups of causally-related behaviour patterns all serve a similar overall function, such as deterring or avoiding a rival, then it is legitimate to give these postulated causal factors labels such as aggression a n d fear, that reflect this function (Figure 4.4).

The second wave of ethological research

47

Interaction between motivational systems In many cases, the intensity with which an animal attacks and flees are inversely correlated, suggesting that aggression and fear are mutually inhibitory. In addition, some behaviour patterns shown during fights are temporally associated with both aggression and fear (Figure 4.4), so these actions may well be u n d e r the joint control of these two systems. However, the conflict theory has been rightly criticized on a number of counts (Andrew, 1972). For example, tendencies other than fear, such as the need to stay put, can interact with aggression to generate displays (Blurton Jones, 1968). In addition, interactions between behavioural systems are now known to be much more complex than the simple inhibitory relationship depicted by the conflict theory. More recent models in the same general framework depict stimulatory and inhibitory links at many different levels and look more like networks than independent hierarchies (Figure 4.5). Tinbergen's model was simple and elegant and there is no virtue in complexity for its own sake; however, these more complex schemes account better for the known behaviour of animals and so represent better explanations of the mechanisms involved. This increasingly complex picture of the causation of behaviour can be illustrated by the changing explanations of displacement activities Dawkins, 1986). More recent analyses of the situations in which these occur have shown that in spite of the odd appearance of such acts (and we should not forget that they often do look very odd), displacement activities are not in fact irrelevant in functional terms; in fighting cocks the opportunity to show displacement pecking during a fight increases the performer's chances of winning. Nor are they irrelevant in causal terms, as the frequency of displacement pecking during fights is influenced by the internal and external factors controlling 'normal' pecking (Feekes, 1972). Thus the sparking-over explanation of displacement activities (already weakened by the failure of energy models to provide satisfactory explanations of the causation of behaviour) gave way to the disinhibition hypothesis. This was first postulated by Andrew (1956) and elaborated by a series of behavioural scientists, including Van Iersel and Bol (1958), Sevenster (1961) and Rowell (1961). According to this view, in an agonistic encounter, a cockerel (for example) may be motivated to feed but this tendency is suppressed both by aggression and by fear. When aggression and fear are aroused simultaneously, the mutual inhibition between them interferes with the ability of both to inhibit pecking, which therefore gains expression; the causal irrelevance of displacement pecking is therefore apparent rather than real. The hypothesis was extended by McFarland (1966), who recognized that disinhibition can occur in a

II II ~'~

~.~-~

o .o <

• ~, :>

,.~ x'~ ~

•

\. \ \ \ -- - . - . _

_._.

_

~~

~ 4 "

\ \

~ 6".~

\

I-rr

\

I

% \ \ \ \

N--{~O--i'-~ ~

\

i

i

~

',,~

:::1

i'~

,-,.-, it ,.El .~

I I i I

~#,

I.L1

., i~O II 0 .~ <

I

.~-~..

z

°~-

~

< - 0 ~

~

The second wave of ethological research

49

variety of situations that allow animals to switch their attention to o t h e r stimuli. T h e e n d result of this d e b a t e o v e r the causation of d i s p l a c e m e n t activities is m u c h m o r e s o p h i s t i c a t e d v i e w of t h e w a y in w h i c h m o t i v a t i o n a l s y s t e m s i n t e r a c t t h a n T i n b e r g e n g a v e us, a l t h o u g h h e was right to r e c o g n i z e that d i s p l a c e m e n t activities can potentially reveal a g r e a t deal a b o u t b e h a v i o u r a l o r g a n i z a t i o n .

Tinbergen's influence In the light of the intense scrutiny that t h e y attracted, it is n o t surprising t h a t m a n y of T i n b e r g e n ' s i d e a s h a v e b e e n a l t e r e d or e v e n r e j e c t e d . H e h i m s e l f w e l c o m e d t h e s e d e v e l o p m e n t s a n d c o n t i n u a l l y r e v i s e d his t h e o r i e s to a c c o m m o d a t e all this n e w i n f o r m a t i o n (for e x a m p l e , in his article ' T h e a i m s a n d m e t h o d s of e t h o l o g y ' w r i t t e n in 1963), b u t his role w a s m o r e i m p o r t a n t t h a n this, b e c a u s e it is clear f r o m t h e c o m m e n t s of t h e k e y p e o p l e i n v o l v e d in t h e s e d e b a t e s t h a t T i n b e r g e n actively e n c o u r a g e d t h e m in t h e i r w o r k . A g l a n c e at t h e k e y w r i t i n g of t h e t i m e m a k e s this clear, as T i n b e r g e n is w a r m l y a c k n o w l e d g e d Table 4.1 Acknowledgements to Niko Tinbergen From critics of the lack of feedback in Tinbergen's model "In particular, I am grateful to Niko Tinbergen . . . for encouraging my initial ventures into the realm of feedback theory.' David McFarland (1971) (Preface) Feedback Mechanisms in Animal Behaviour. From critics of unitary drive concepts and energy models 'I am endebted to a number of colleagues for discussion during the preparation of this paper and especially t o . . . Dr N. Tinbergen.' Robert Hinde (1959) Unitary Drives. Animal Behaviour.

'I am greatly endebted to [Niko Tinbergen] for his comments [on the manuscript of Animal Behaviour] and also for the many discussions we have had and all I have learned from him'. Robert Hinde (1965) Preface to Animal Behaviour. From critics of Tinbergen's view of displacement activities 'I am grateful to . . . Niko Tinbergen for discussions in the subject in general' Frazer Rowell (1961). Displacement grooming in chaffinches. Animal Behaviour.

'The author wishes to express his appreciation to Dr N. Tinbergen for reading the manuscript and for his helpful comments'. David McFarland (1965). Hunger, thirst and displacement pecking in Barbary doves. Animal Behaviour. 'Particularly I thank Prof. Dr N. Tinbergen, who introduced me to the study of behaviour and for his kindness and help' Francisca Feekes (1972) 'Irrelevant' ground-pecking in agonistic situations in Burmese jungle fowl.

50

War and peace revisited

for his help a n d e n c o u r a g e m e n t in almost every case (Table 4.1). It is no coincidence that two of the most i m p o r t a n t books of the time ( H i n d e ' s ' A n i m a l b e h a v i o u r ' 1956, a n d McFarland's 'Feedback m e c h a n i s m s in animal behaviour' 1971), were dedicated to him. The fertile a n d e n c o u r a g i n g a t m o s p h e r e that Tinbergen created surely played a critical role in the d e v e l o p m e n t of behavioural biology in the 1960s a n d 1970s. This is an i m p o r t a n t a n d valuable legacy, w h a t e v e r place his ideas m a y have in m o d e r n motivation theory.

1321 1,071

11,51

100

m I..

80

m N.-,

0 f0 im

60

40

L_

0 0 Q,,

~i~i!~i~i i !:~!!i'~~!

20

1959

1969

1979

1989

Figure 4.6 The percentage of papers published in three behavioural journals in

1959, 1969, 1979 and 1989 that concerned motivation (M), external stimuli (S), the functions of behaviour (F) and other issues (O; primarily development and genetics of behaviour)

Modem studies of causation

51

M O D E R N STUDIES OF C A U S A T I O N The status of Tinbergen's ideas So w h a t is the status of Tinbergen's ideas in m o d e r n t h e o r y on causation? To discover this we need to look not just for m o d e r n studies of the causation of behaviour, but for studies of causation b y biologists w h o make u s e of the behavioural techniques a n d concepts that he h e l p e d to develop. This is not easy, b e c a u s e there is a c o n s p i c u o u s shortage of software studies of the m e c h a n i s m s of behaviour. Figure 4.6 s h o w s the proportion of papers on different aspects of b e h a v i o u r p u b l i s h e d in the three main behavioural journals (Animal Behaviour, Behaviour and Ethology) in the period 1950 - 1990. The figures confirm w h a t is already well k n o w n , n a m e l y that in the 1950s a n d 1960s most people were s t u d y i n g causation a n d d e v e l o p m e n t , b u t that b y the end of the 1980s most people were studying function. The turning point came in the late 1970s; for example, in 1979 Caryl r e a n a l y s e d a n u m b e r of classical ethological studies and s h o w e d that the data w e r e better explained b y game theory m o d e l s (which predicted that fighting animals should evolve poker faces - Maynard-Smith and Price, 1973) than by ethological models (which predicted that animals should wear their hearts on their sleeves). In the same year, Jakobsson et al. u s e d sequence analyses of behavioural exchanges during fights b e t w e e n cichlid fish (in more or less the classical ethological m o d e ) to test and s u p p o r t the same g a m e s theory prediction. These t w o studies represent a clear change of e m p h a s i s in research on aggression and other aspects of behaviour. In spite of this change of emphasis, we can see Tinbergen's influence in m o d e r n studies of causation, b u t this influence is complex a n d s h o w s up in different ways. O v e r a n d above providing a m o d e l of h o w to conduct and write about scientific research, Tinbergen's legacy has several c o m p o n e n t s (Table 4.2). Table 4.2 The components of the Tinbergen Legacy The direct legacy: modern studies that incorporate classical ethological techniques and ideas The slightly-less direct legacy: modern theories that grew out of criticisms of Tinbergen's model of motivation The indirect legacy: flourishing interdisciplinary studies encouraged by Tinbergen, such as neuroethology and behavioural endocrinology The (almost) unclaimed legacy: call for links between studies of causation and function.

52

War and peace revisited

The direct legacy

There are still biologists who conduct detailed analyses of behavioural sequences in the classic ethological mode, but who go b e y o n d this to ask questions about other aspects of behaviour. Appropriately, much of this is being conducted by Dutch ethologists, particularly Baerends and his colleagues. Their studies, mainly on cichlid fish and birds (Baerends, 1984), draw on Tinbergen's ideas (for example, their models include a dual system for the control of agonistic behaviour (Figure 4.5)), but they also incorporate other more recent developments in behavioural theory. This combination has produced a great deal of information about the mechanisms that control behaviour, and about its development and functions. To give just one of many possible examples, Groothius (1989) used classic ethological techniques to analyse the causal structure of behaviour in gull chicks, from hatching to adulthood. A m o n g other things, he found that the frequency with which displays such as choking are performed during development correlates positively with the frequency of performance of overt aggression and fear; this is clearly consistent with the conflict hypothesis. The adult form of the choking display develops by the gradual addition of aggressive elements (downwards pointed bill, raised carpels and tilted body) onto the crouching posture typically shown by a frightened chick w h e n hiding in cover (Figure 4.7). Groothius' study identified a key role for the hormone testosterone in the development of agonistic displays in young gulls of both sexes. Levels of circulating testosterone are naturally high at the time w h e n full displays are first shown, and

C

D

E

F

G CHOKING

Figure 4.7 Development of choking in the black-headed gull from the crouching response of very young chicks (simplified from Groothius, 1990)

Modem studies of causation

53

Conlact v

Threaten Signal ~

Retreat"

Fear (F) Figure 4.8 A two-factor model of spider fights, in which choice of action depends on the level of independent tendencies to attack or to flee (from Huntingford and Turner, 1987, simplified from Maynard-Smith and Reichert, 1985). implants of testosterone (which increase aggressiveness) induce the p e r f o r m a n c e of c o m p l e t e displays e v e n in very y o u n g gulls. These observations suggest that the role of testosterone is to create a motivational state that permits the d e v e l o p m e n t of agonistic displays. T w o recent beneficiaries of the T i n b e r g e n legacy are M a y n a r d Smith and Riechert (1985) w h o d e v e l o p e d a two-factor m o d e l of the control of aggression in spiders (Figure 4.8). This model successfully reconstructs the strategic decisions that spiders are k n o w n to take d u r i n g fights, a n d gains s o m e s u p p o r t from a genetic analysis that suggests separate patterns of inheritance for aggression (at sexlinked loci) a n d fear (at a u t o s o m a l loci) (Riechert a n d M a y n a r d Smith, 1989).

The slightly-less-direct legacy In the examples given above, Tinbergen's ideas and concepts are still proving useful (albeit in a modified form) in interpreting behavioural data. Other important areas of modern motivational theory developed,

54

War and peace revisited

Physiological space

-~-

~

Level of hormone X

/~

~ Level of water

Level of food

/ /

Cuespace

Motivational space

Palal-abilityl of food J

Food deficit

Water deficit

\

Avaflobd~ty of wbater /

\

/.

Causal factor space Food defic0r Food deflc0t and polo rabdil'y combine ro determine feeding tendency ; mohvarloflal isochnes join points of equal tendency

I

~

/

l

Availabiht y

Isocline F

/

of w0ter Isochne D2

Water deficit and availability combine to determine drinking tendency ; motivational isochnes join points of equal tendency

''''y

I

"~I

I

sochne

r~ I

Wafer deficit

Candidate space Feeding tendency Isocllne F2 maps to F2 Isocline F1 mops to F1 I

D1 Isochne D1 maps I'o D I

I ~ Drinking tendency D2 Isocline D2 m a p s r o D2

Figure 4.9 McFarland's space-state model of motivation (from Huntingford 1984,

after McFarland and Houston, 1981).

Modem studies of causation

55

in part at least, out of the recognition of the inadequacies of Tinbergen's formulation that became apparent during the second w a v e of ethology. Because Tinbergen e n c o u r a g e d these studies a n d w e l c o m e d their results, these too are part of his legacy. McFarland's Space-State model of motivation (McFarland a n d H o u s t o n , 1981, Figure 4.9) looks v e r y different from T i n b e r g e n ' s Hierarchical m o d e l [McFarland writes 'Traditionalists in the field of motivation will recognize little in this book that is b o r r o w e d or derived from their w o r k ' (McFarland, 1974)], b u t it is still a case in point. In this model, the complex, non-unitary nature of motivational systems is accommodated by making the various internal a n d external factors that influence b e h a v i o u r into axes in a multidimensional causal factor space. The various kinds of feedback are h a n d l e d by depicting the consequences of b e h a v i o u r as m o v e m e n t t h r o u g h state space. This f r a m e w o r k provides a w a y of characterizing the complexities of behavioural organization a n d (if one is clever e n o u g h ) of u n d e r s t a n d i n g them.

The indirect legacy Tinbergen's influence on m o d e r n motivation t h e o r y can also be seen in the effects of his writing and personality on people working in other disciplines. In particular he contributed to an intellectual climate in which interdisciplinary research could flourish. For example, he actively e n c o u r a g e d the integration of behavioural a n d physiological studies, as indicated by the following statement: ' . . . future w o r k could only be d o n e by workers w h o are fully acquainted with the instinctive behaviour as a whole and with its analysis, and at the same time are in c o m m a n d of neurophysiological m e t h o d s and techniques. • . . It is an urgent task of ethologists and n e u r o p h y s i o l o g i s t s to join efforts in the training of " e t h o p h y s i o l o g i s t s " ' (Tinbergen, 1951). Causation

and

function

Tinbergen stressed the importance of research into the functions of behaviour and one of the reasons for the change in e m p h a s i s from studies of causation to studies of function is that he argued very persuasively• It should be said that this extreme trend is not one that he w o u l d have w e l c o m e d unreservedly, since he also argued for continual interaction b e t w e e n causal and functional studies: : . . the t w o a p p r o a c h e s are mutually i n s p i r i n g . . . The discovery of each particular achievement inspires one to find out "how it is done"; converse136 the student of mechanisms derives satisfaction from u n d e r s t a n d i n g h o w the achievements

56

War and peace revisited

of the mechanisms contribute to the animal's success" (Tinbergen, 1972). Until recently, this call for links b e t w e e n causal a n d functional studies has gone largely u n h e a r d - it remains an (almost) u n c l a i m e d legacy. It is fitting that one of the f e w p e o p l e w h o have w o r k e d actively to find a w a y of integrating causal and functional studies is Tinbergen's successor at Oxford, David McFarland. In a series of articles and books (1977, 1989), McFarland (together with Alasdair H o u s t o n , 1981) has d e v e l o p e d a framework that directly links the multivariate mechanisms controlling b e h a v i o u r to the c o n s e q u e n c e s for fitness of different behavioural options. His aim is articulated most clearly w h e n he asks ' H o w are animals so organized that they are motivated to do w h a t they o u g h t to do at a particular time?' (McFarland, 1989). His f r a m e w o r k is necessarily complex and is not easy to apply, but it highlights important behavioural questions. Both causal a n d functional studies suffer if d e v e l o p m e n t s in these t w o fields get out of step. It is e a s y to see h o w thinking a b o u t functions can help studies of causation; for example, if he had k n o w n w h a t w e n o w k n o w a b o u t the strategic decisions animals make during fights, Tinbergen w o u l d not have b e e n satisfied with a theory of causation that h a d animals driven by an irresistible drive to fight regardless of the consequences, and had them responding blindly to just one feature of a potential rival. H o w e v e r , in the p r e s e n t climate of opinion, it is the opposite case that one has to argue. I suggest that w h e n t h e y turn their backs on motivational studies, behavioural ecologists d e n y t h e m s e l v e s an important source of information. For example, it is n o w clear that m a n y animals use simple decision rules to achieve approximately optimal solutions. Recognition of this fact (which in effect concerns the m e c h a n i s m s that control behaviour) represents an important development in understanding h o w selection acts on behaviour. A similar r a p p r o c h e m e n t b e t w e e n functional and causal studies might also be useful in aggression research. To give one example: on the one hand, a long series of games theory models, r u n n i n g from M a y n a r d - S m i t h and Parker's initial w o r k on assessment (1974) to the recent extension of Enquist's Sequential Assessment Game (Enquist et al., 1990), has interpreted behavioural exchanges during fights as a process of acquisition of accurate information a b o u t the relative fighting ability of the contestants. This extremely fruitful approach has h e l p e d to a n s w e r m a n y difficult questions about w h y animals fight in the w a y t h e y do. It m a y be that from a functional perspective there is no n e e d to k n o w about the m e c h a n i s m s b y which this is achieved. O n the other hand, m a n y motivational studies suggest that other important things are going on during fights; a n u m b e r of studies (Archer, 1987; Huntingford and Turner, 1987) have s h o w n that decisions d e p e n d critically on the animal's motivational state, on the

References

57

current level of aggression of its rival, on w h e t h e r this is increasing or decreasing a n d on the part that the a n i m a l ' s o w n previous actions have p l a y e d in bringing about such changes. This seems more complicated t h a n is necessary simply to allow animals to assess their relative fighting ability, suggesting that other functional issues are involved. In 1953 Tinbergen wrote ' . . . the result of a hostile clash is not d e t e r m i n e d by the actual strengths of the two contestants but by their " d a s h " , by the strength of their fighting drive' (Tinbergen, 1953). We n o w k n o w that he was completely wrong to dismiss strength as a determinant of the outcome of fights, but perhaps we should give some t h o u g h t to the functional significant of ' d a s h ' .

THE TINBERGEN LEGACY What Niko Tinbergen wrote about the causation of behaviour 20 years ago a n d more, still has an influence on the w a y behavioural scientists work. In the first place, some of his ideas (especially his recognition of the interacting effects of aggression a n d fear) still have direct value as explanatory concepts helping us to s t u d y a n d u n d e r s t a n d h o w behaviour is organized. Secondly, by e n c o u r a g i n g critical evaluation of his o w n ideas, he p r o m o t e d the d e v e l o p m e n t of the more sophisticated theories of motivation currently in use. Lastly, by his intellectual b r o a d m i n d e d n e s s he contributed to the intellectual climate in which interdisciplinary research into causation flourished. These are no m e a n achievements and as beneficiaries of Tinbergen's intellectual legacy we are richly e n d o w e d .

ACKNOWLEDGEMENTS I w o u l d like to t h a n k a n u m b e r of colleagues, including Mike Hansell, Neil Metcalfe a n d Pat M o n a g h a n , for c o m m e n t s on earlier versions of this paper, a n d in particular, Neil Metcalfe for last-minute help in preparing the figures for the talk on which it is based.

REFERENCES Andrew, R.J. (1956) Some remarks on behaviour in conflict situations with special reference to Emberiza spp. British Journal of Animal Behaviour, 4, 41-45. Andrew, R.J. (1972) The information potentially available in mammalian displays, in Non-verbal communication, (ed R.A. Hinde), Cambridge University Press, Cambridge, pp. 179-206

58

War and peace revisited

Archer, J. (1987) The behavioural biology of aggression, Cambridge University Press, Cambridge. Baerends, G. (1984) The organization of the pre-spawning behaviour in the cichlid fish Aequideus portalegrensis. Neth. S. Zod, 34, 233-366. Blurton Jones, N.G. (1968) Observation and experiments on the causation of threat displays in the great tit Parus major. Animal Behaviour Monographs, 1, 75-158. Caryl, P.G. (1979.) Communication by agonistic displays: what can games theory contribute to ethology? Behaviour, 68, 136-69. Collias, N.R. (1990) Statistical evidence for aggressive responses to red by male three-spined sticklebacks. Animal Behaviour, 39, 401-3. Dawkins, M.S. (1986) Unravelling animal behaviour. Longman, Harlow, Essex. Enquist, M. Leimar, O, Ljungberg, T. et al. (1990) A test of the sequential assessment game: fighting in the cichlid fish Nannacara anomala. Animal Behaviour 40, 1-14. Feekes, F. (1972) 'Irrelevant' ground-pecking in agonistic situations in Burmese red jungle fowl (Gallus gallus spadiceus). Behaviour, 43, 186-326. Groothius, T. (1989) On the ontogeny of display behaviour in the blackheaded gull, Larus ridibundus. PhD Thesis, University of Groningen. Hinde, R.A. (1960) Energy models of motivation. Symposium Society for Experimental Biology, 14, 199-213. Hinde, R.A. (1966)Animal behaviour, McGraw-Hill, New York. Huntingford, F.A. (1977) Inter- and intra-specific aggression in male threespined sticklebacks. Copeia, 158-9. Huntingford, F.A. (1984) The study of animal behaviour. Chapman & Hall, London. Huntingford, F.A. and Turner, A.K. (1987) Animal conflict. Chapman & Hall, London. Jakobsson, S, Radesater, T. and Jarvi, T. (1979) On the fighting behaviour of Nannacara anomala (Pisces, cichlidae). Zeitschrift fiir Tierpsychologie, 49, 210-20. McFarland, D.J. (1966) The role of attention in the disinhibition of displacement activities. Quarterly Journal of Experimental Psychology, 18, 19-30. McFarland, D.J. (1971) Feedback mechanisms in animal behaviour, Academic Press, London. McFarland, D.J. (1974) Motivational control systems analysis, Academic Press, London. McFarland, D.J. (1977) Decision-making in animals. Nature, 269, 15-21. McFarland, D.J. (1989) Problems of animal behaviour, Longman Scientific, Harlow. McFarland, D.J. and Houston, A.I. (1981) Quantitative ethology. Pitman, London. Maynard-Smith, J. and Parker, G. (1974) The logic of asymmetric contests. Animal Behaviour, 24, 159-75. Maynard-Smith, J. and Price, G. (1973) The logic of animal conflict. Nature, 246, 15-18. Maynard-Smith, J. and Riechert, S.E. (1985) A conflicting-tendency model of spider agonistic behaviour: h y b r i d - p u r e line comparisons. Animal Behaviour, 32, 564-78. Riechert, S.E. and Maynard-Smith, J. (1989). Genetic analysis of two behavioural traits linked to individual fitness in the desert spider,

References

59

Agelenopsis aperta. Animal Behaviour, 37, 624-37. Rowell, C.H.F. (1961) Displacement grooming in the chaffinch. Animal Behaviour, 9, 38-63. Rowland, W.J. (1988a) The effect of body size, aggression and nuptial colouring in competition for territories in male three-spined sticklebacks, Gasterosteus aculeatus. Animal Behaviour, 36, 629-38. Rowland, W.J. (1988b) Aggression versus courtship in three-spined sticklebacks and the role of habituation to neighbours. Animal Behaviour, 34, 348-57. Rowland, W.J. and Sevenster, P. (1985) Sign stimuli in the three-spined stickleback (Gasterosteus aculeatus): a reexamination and extension of some classic experiments. Behaviour, 93, 241-57. Sevenster, P. (1961) A causal analysis of a displacement activity (fanning in Gasterosteus aculeatus). Behaviour, (Suppl.) 9, 1-170. Tinbergen, N. (1951) The study of instinct. Clarendon Press, Oxford. Tinbergen, N. (1953) Fighting and threat in animals. New Biology, 14, 9-23. Tinbergen, N. (1963) On aims and methods of ethology. Zeitschrifl fiir Tierpsychologie, 20; 410-33. Tinbergen, N. (1968) On war and peace in animals and man. Science, 160, 1411-18. Tinbergen, N. (1972) Functional ethology and the human sciences. Proceedings of the Royal Society, B 182, 385-410. Ukegbu, A.A. and Huntingford, F.A. (1988) Brood value and life expectancy as determinants of parental investment in male three-spined sticklebacks, Gasterosteus aculeatus. Ethology, 78, 72-82. Wootton, R.J. (1970) Aggression in the early phases of the reproductive cycle of the male three-spined stickleback (Gasterosteus aculeatus). Animal Behaviour, 18, 740-46.

m5 Animal communication: ideas derived from Tinbergen's activities JOHN R. KREBS

INTRODUCTION W h e n I was a n e w research student in the late 1960s, four things struck me about Niko Tinbergen. The first was the breadth of his approach. I personally benefited greatly from this because I w a n t e d to s t u d y a problem in population ecology and I e n d e d up in his Animal Behaviour Group. Niko quite rightly saw no real distinction b e t w e e n the s t u d y of behaviour and the s t u d y of ecology. The second thing that struck me was his insistence on great precision of thought. I can remember one of the first Behaviour G r o u p seminars I ever w e n t to: there was an invited speaker from outside Oxford w h o stood up a n d m a n a g e d to get t h r o u g h two sentences before the discussion broke d o w n into exactly w h a t he m e a n t by those two sentences. The speaker w e n t h o m e w i t h o u t ever having finished the rest of his seminar. A third characteristic of Niko that has been referred to by m a n y other people was his total lack of hierarchy a n d p o m p . This m a d e a particular impression on me because he was at that time at the height of his fame a n d a w e l l - k n o w n international figure, but I never felt, in talking to him, a n y t h i n g other t h a n a colleague a n d an equal, one w h o s e views were to be j u d g e d a n d appreciated in the same w a y as those of more senior colleagues. Finally, there was a feature of Niko that m a d e a great impression on me as an u n d e r g r a d u a t e , namely, his athletic skills. During one of his u n d e r g r a d u a t e lectures, he noticed that s o m e o n e at the back of the steeply tiered lecture theatre that we used in the old zoology d e p a r t m e n t was reading a n e w s p a p e r . W i t h o u t even hesitating, a n d

The Tinbergen/Lorenz view of communication

61

continuing to give his lecture, Niko leapt on to the front bench, strode two benches at a time up to the top row, grabbed the n e w s p a p e r scrunched it up into a ball a n d t h e n strode back d o w n to the front as t h o u g h n o t h i n g h a d h a p p e n e d . Turning n o w to the theme of communication, I have to confess that initially I t h o u g h t it was going to be relatively easy to define N i k o ' s contribution to m o d e r n studies of animal c o m m u n i c a t i o n . M a n y of his views are contained in his classic paper on 'derived activities' (1952). I h a d t h o u g h t that w h a t I w o u l d do w o u l d be to take, say, five major ideas from that paper, then five key ideas from current literature a n d trace the t h r e a d s b e t w e e n them. It t u r n e d out, h o w e v e r , to be m u c h more difficult t h a n I h a d t h o u g h t . The views of c o m m u n i c a t i o n that were prevalent in 1952 a n d even u p to the time of the S y m p o s i u m on Ritualization organized by H u x l e y in 1966 are very different from p r e s e n t - d a y ideas, a n d the connections b e t w e e n t h e n a n d n o w are not at all straightforward. So w h a t I will do is summarize from a purely historical point of view w h a t Tinbergen said in his 1952 p a p e r a n d say s o m e t h i n g about the ideas on c o m m u n i c a t i o n that were a r o u n d at the time. I will try to give a picture as I see it, of w h a t m i g h t be called the Tinbergen/Lorenz view, following this with w h a t I perceive to be the important current issues in the field of animal communication, a n d the links b e t w e e n them, a n d then pick out possible future directions for research.

THE TINBERGEN/LORENZ VIEW OF C O M M U N I C A T I O N A major part of Tinbergen's (1952) view of c o m m u n i c a t i o n was to do with theory of 'derived' activities - that is, the idea that w h a t we n o w see as signals were derived in the course of evolution from other nonsignal m o v e m e n t s , particularly those s h o w n by animals in situations of motivational conflict. Examples of behaviour that Tinbergen saw as the 'raw material' for evolution into signals were intention m o v e m e n t s , ambivalent behaviour, protective responses (a later suggestion of Richard Andrews), autonomic responses, displacement activities a n d redirected activities (Fig. 5.1). All of these were t h o u g h t to arise w h e n an animal was motivated to do two incompatible things at once (for example, to attack a n d to flee). Tinbergen saw this as the activation of two specific 'drives' a n d one of the issues he a d d r e s s e d was w h e t h e r , as signals evolved, t h e y became e m a n c i p a t e d or freed from their original causal factors. Signals m a y have evolved from situations of motivational conflict but by the time t h e y h a d taken on a c o m m u n i c a t i o n function, the original conflict m a y have been lost.

62

Animal communication: ideas derived from Tinbergen's activities

Behaviour or response from which display evolved 1.

Intention movement

The displays to which the ancestral movements in column 1 are thought to have g!ven rise Sky-pointing in the gannet

2. Ambivalent behaviour

Forward threat posture of black-headed gull

3. Protective response

Primate facial expressions

4. Autonomic response (e.g. sweating, urinating, rapid breathing)

(Vr°CmaIirZa~iidns

5. Displacement activities

6. Redirected attack

breathing). Scent marking

\ ~ ~.ii,i.-'i

'

'~ ~ ~,/.~i i~

duckPreeningin '::..i.ii courtship

Grass ~ ~ in herring gulls ~

j

~ , ,

-1

v//~

Figure 5.1 Examples of the kind of behaviour pattern and other responses from which displays in birds, fish and primates are thought to have evolved. (After Hinde (1970); redrawn from Krebs and Davies (1987) An introduction to behavioural ecology. Blackwell Scientific Publications, Oxford.)

The Tinbergen/Lorenz view of communication

63

Tinbergen was, therefore, concerned w i t h the motivation or causal basis of signal m o v e m e n t s . A second aim of Tinbergen's theory, was to describe a n d t h e n to account for the changes that signals u n d e r w e n t as t h e y evolved f r o m ancestral conflict behaviour to fully f o r m e d signals. This is the process referred to as 'ritualization', in w h i c h signals become exaggerated, stereotyped a n d repeated. The evidence for the idea that signals did change in this w a y came from comparative studies of closely related species. The ancestral g r o u n d - p e c k i n g m o v e m e n t s of the jungle fowl courting a hen, for example, seem to have evolved into the exaggerated m o v e m e n t s of the peacock in which no real food is involved. Two ' s n a p s h o t s ' of m o d e r n species give a picture of h o w e v o l u t i o n a r y change m i g h t have taken place in the past. Tinbergen a r g u e d that ritualization increases signal effectiveness. Cullen (1966) m a d e this idea rather more explicit by arguing that ritualized signals evolve because t h e y reduce ambiguity. With a ritualized signal, an animal can signal clearly 'I am going to attack y o u ' a n d not 'I am going to flee' or 'I w a n t to mate' not 'I am not interested in m a t i n g ' . A third aspect of Tinbergen's theory was that as well as evolutionary history, we n e e d to k n o w about the p r e s e n t - d a y function of signals. Then, as n o w , ethologists t e n d e d to concentrate on courtship a n d threat signals, mainly in a restricted range of animals. Tinbergen saw courtship signals as serving functions such as attracting a mate, stimulating or arousing a partner, s y n c h r o n i z i n g the sexual activity of a pair, or c e m e n t i n g a pair bond. He saw threat signals as serving the function of conveying the signaller's intentions about h o w likely he was to attack a rival. Tinbergen was also concerned to give an account of the variety a n d design of signals. This m e a n s he w a n t e d to u n d e r s t a n d w h y signals have the structure they do, w h y the same animal uses different signals at different times and w h y there are such differences b e t w e e n species in w h a t signals they use. He a r g u e d that one reason for such differences was differences in the 'raw material' from which the signals evolved, w h i c h in turn was a reflection of the particular conflict behaviour from which they derived. For example, if a signal was derived from displacement preening, as seems to be the case in certain species of duck, then this w o u l d affect w h a t the final ritualized signal looked like. O n e of the a r g u m e n t s he u s e d to explain w h y the same animal m a y use different signals on different occasions was that the signal u s e d m a y d e p e n d on the posture it h a p p e n s to be in at the m o m e n t of signalling. If the animal h a p p e n e d to be sitting d o w n it might use signal A, a n d if it h a p p e n e d to be s t a n d i n g u p it m i g h t use signal B. As well as the posture of the animal itself, external stimuli

64

Animal communication: ideas derived from Tinbergen's activities

such as w h e t h e r there was food present, m i g h t affect exactly w h i c h signal the animal used. His account of the design a n d variety of signals was, therefore, essentially a causal one.

THE MODERN

VIEW OF ANIMAL

COMMUNICATION

I n o w come to the m o d e r n view of animal c o m m u n i c a t i o n . There has been surprisingly little work on the causal basis of displays over the last 25-30 years, as H u n t i n g f o r d (Chapter 4) also points out, a n d so I shall say very little about this, concentrating instead on those aspects that have attracted considerable attention - namely, e v o l u t i o n a r y change, function a n d variety a n d design. I will deal first with theories about evolutionary change. Here we find two recent views that are decidedly different from the evolutionary ritualization of signals that Tinbergen described. O n e of these views was p u t f o r w a r d by Richard D a w k i n s a n d myself (1978; also Krebs and Dawkins, 1984). The other has been advocated in a series of articles by Zahavi (1975; 1979; 1987). A l t h o u g h these two appear to be very different, I believe that t h e y are essentially similar and are best seen as reflecting two sides of the same hypothesis. They both differ from Tinbergen's account of animal signalling by e m p h a s i z i n g the role of coevolution b e t w e e n actors (the ones performing the signals) a n d reactors (the ones r e s p o n d i n g to them). The key point is that the interests of actors a n d those of reactors are not the same. The 'selfish gene' view of animal behaviour (Hamilton, 1964; Dawkins, 1976) sees the coevolution between actors and reactors as an 'arms race' in which actors are selected to increase the effectiveness of their signals a n d to change the behaviour of reactors to their o w n ends, while reactors will be selected to increase their discrimination a n d their 'sales resistance'. Both the theories of D a w k i n s a n d Krebs (1978) a n d that of Zahavi (1975; 1989) are similar in e m p h a s i z i n g the selfishness of the two parties involved. Both see ritualization as a p r o d u c e of a coevolutionary arms race. W h e r e t h e y appear to differ is in w h e t h e r the reactors can be described as being ' m a n i p u l a t e d ' by the salesmanship of the actors. Dawkins and Krebs (1978; also Krebs and Dawkins, 1984) considered cases w h e r e reactors appear to get the worst of a coevolutionary arms race a n d to be m a n i p u l a t e d into doing things that are not g o o d for them. Two obvious examples are reed warblers being ' m a n i p u l a t e d ' by cuckoos, a n d firefly females attracting a n d t h e n eating males of a n o t h e r species by emitting their species-specific pattern of flashes (Lloyd, 1979). O n e possible explanation for such cases of a p p a r e n t

The modem view of animal communication

65

exploitation is frequency d e p e n d e n c e . If cuckoos in the nest or predators emitting courtship signals are relatively rare events compared to the real thing, t h e n it m a y on average p a y a reactor to r e s p o n d , even if occasionally it e n d s in disaster. H o w e v e r , there is a more general reason w h y reactors s h o u l d be vulnerable to exploitation by actors a n d this can be traced right back to Tinbergen's view of h o w signals evolve in the first place. Tinbergen (1952) argued that the reason w h y conflict behaviour so often provides the raw material for signal evolution is that w h e n an animal is in a conflict, it is in a state of transition b e t w e e n two motivational states. The behaviour that it performs in such a situation therefore has a high predictive value about w h a t it will do next. The reactors can therefore ' m i n d read' or predict the behaviour of the actor (Krebs and Dawkins, 1984) a n d this in turn makes t h e m vulnerable to exploitation over ev61utionary time by actors which t h e n c h a n g e their behaviour, so as to m a n i p u l a t e reactors. Krebs a n d Dawkins (1984) also m a d e a distinction b e t w e e n two kinds of signal which w o u l d have different paths of coevolution. With non-cooperative signals (most of the signals s t u d i e d by ethologists) the path w o u l d lead to an arms race of persuasion by the actor a n d sales resistance by the reactor, a n d c o n s e q u e n t l y to the evolution of conspicuous, repetitive advertising signals which bear all the hallmarks of 'ritualization'. O t h e r signals, h o w e v e r , which can be called cooperative because t h e y occur b e t w e e n relatives or b e t w e e n m e m b e r s of a m a t e d pair, will be selected to be the opposite of ritualized. For reasons of e c o n o m y of production, t h e y will evolve towards d i m i n i s h e d amplitude, d i m i n i s h e d c o n s p i c u o u s n e s s a n d h e i g h t e n e d receiver sensitivity. If it pays the reactor to receive a n d r e s p o n d to a signal, it will be straining its ears or eyes, so that the actor has no n e e d to p r o d u c e a loud blast of s o u n d or bright colours. Because of their inconspicuous nature, ethologists m a y have overlooked m a n y examples of cooperative signals. O u r point was that not all signals s h o u l d be ritualized a n d we s u g g e s t e d that a possible line of research w o u l d be to see w h e t h e r cooperative signals are on the whole the h u s h e d conspiratorial w h i s p e r s we predicted, with noncooperative signals the bright, noisy conspicuous signals that Tinbergen studied. In apparent contrast to the Dawkins-Krebs view of communication, which sees m a n y instances of animals ' m a n i p u l a t i n g ' each other, Zahavi (1975, 1989) e m p h a s i z e s the essential h o n e s t y of signals. He argues that reactors should never respond to a signal - such as a threat or courtship display - unless it is an h o n e s t indictor of s o m e t h i n g the reactor was interested in, such as fighting ability or suitability as

66

Animal communication: ideas derived from Tinbergen's activities

a mate. For example, if females benefit from choosing disease-free males (Hamilton a n d Zuk, 1982), t h e n they s h o u l d be selected to r e s p o n d to s o m e feature of a male that gives a g e n u i n e indication of his disease-resistance. Unless signals are honest, reactors will not r e s p o n d to them. The only w a y in w h i c h h o n e s t y can be m a i n t a i n e d is if signals are costly and only those signals which are, say, genuinely healthy and free of disease will be able to p a y the cost. Differences b e t w e e n individuals in their ability to p a y such costs ( d e t e r m i n e d ultimately by h o w healthy and disease-resistant they are) explain w h y individuals also differ in their level of signalling. Zahavi further argued that in the design of signals there s h o u l d be a relationship b e t w e e n cost (indication of quality that the signal is c o n c e r n e d with) a n d the structure of the signal. Several examples of signalling appear to s h o w this relationship quite clearly. Fitzgibbon a n d F a n s h a w e (1988) studied stotting in gazelles, a curious b e h a v i o u r in which the animals leap into the air while fleeing from a predator. They s h o w e d that gazelles that stot at a high rate are more likely to escape w h e n attacked by h u n t i n g dogs than those that stot at a low rate. Stotting does therefore seem to be a genuine indication of escape ability. The h u n t i n g dogs react to it by picking selectively on gazelles that stot at a low rate. In the dry season, w h e n conditions are poor, the gazelles do not stot very much, as they are not in g o o d e n o u g h condition to do so. Borgia (1985) provides another example of ' h o n e s t ' signalling, this time in the courtship display of b o w e r birds. The male satin b o w e r bird (Ptilinorynchus violaceus) in c o m m o n with other closely related species, decorates its b o w e r with artefacts, s o m e t i m e s natural, s o m e t i m e s unnatural. Females choose as mates those males with the largest n u m b e r of artefacts in their b o w e r s . N o w the n u m b e r of artefacts a male b o w e r bird has is an h o n e s t indication of his fighting ability, because one of the main w a y s the males have of collecting artefacts is to steal t h e m from other males. So the males that have a lot of o r n a m e n t s in their b o w e r s are inevitably those that are best at stealing from others and also d e f e n d i n g their o w n b o w e r s . By choosing a male with a well-ornamented bower, the female is therefore choosing a male with p r o v e n fighting ability. A n o t h e r example of an ' h o n e s t ' signal is the association b e t w e e n b o d y size a n d pitch of calls in amphibia (Davies and Halliday, 1978). Small males simply cannot p r o d u c e low frequency s o u n d s so the pitch of a call is an h o n e s t indicator of b o d y size. There are, therefore, t w o v i e w s a b o u t the evolution of signals the D a w k i n s - K r e b s view that stresses the m a n i p u l a t o r y nature of signals, and the Zahavian v i e w that signals are essentially honest.

The modem view of animal communication

67

Which one is correct? As I stressed before, I do not think these t w o v i e w s are incompatible: both could be correct. D a w k i n s and Krebs discussed a coevolutionary process w i t h o u t specifying an end-point, w h e r e a s Zahavi w a s c o n c e r n e d mainly with the e n d - p o i n t itself, so it is possible to imagine an evolutionary arms race of manipulation and sales resistance which ends u p with honest signalling. This cannot be the w h o l e answer, h o w e v e r , as the cuckoo example illustrates. C u c k o o s are not h o n e s t signallers. It is, incidently, interesting to note that w h e n Zahavi first p r o p o s e d this view of signals being honest through what he called the 'handicap principle' (1975), he w a s met with ridicule. N o w , various theoretical m o d e l s have b e e n p r o d u c e d (e.g. Kodric-Brown a n d Brown, 1984; Enquist et al., 1985; Grafen, 1990) which s h o w that Zahavi's ideas are quite plausible. By postulating a g r a d e d h a n d i c a p (related to underlying quality) instead of the original 'fixed' handicap (handicap the same regardless of quality of the individual), the idea of h o n e s t signalling has b e c o m e widely accepted. I w a n t n o w to turn to a second aspect of the m o d e r n view of signals that of the function of signals. Here the views that Tinbergen held have been largely s u p e r s e d e d . In particular, a variety of g a m e theory m o d e l s p i o n e e r e d by M a y n a r d - S m i t h (1982) a n d M a y n a r d Smith and Parker (1976), have radically changed the w a y w e see courtship and threat signals. For example, w h e r e a s Tinbergen saw courtship signals as serving to arouse m e m b e r s of the opposite sex, to synchronize mating activities and to maintain the pair bond, w e w o u l d n o w say that the signals allow m e m b e r s of the t w o sexes to assess each other as regards paternity, fidelity a n d quality. Similarly, w h e r e a s Tinbergen stressed the universal importance of accurate transmission of information about intentions, it is n o w clear that m a n y so-called threat displays are concerned with the assessment of fighting ability (RHP or resource holding potential Maynard-Smith and Parker, 1976). T w o examples can be used to illustrate the role of signals in assessment. Hamilton and Z u k (1982) p r o p o s e d that females m a y use the elaborate p l u m a g e or other o r n a m e n t s of males to assess the extent to which males are resistant to disease. Z u k et al. (1990a, b) s h o w e d that female red jungle fowl choose males with large red combs, brightly coloured eyes and bright feathers on their hackles and flanks. If male jungle fowl are infected with a n e m a t o d e , Aspiridia galli, it is those same features that are most affected by the parasitic infection, whereas other features of the b o d y are m u c h less affected. So it appears that the females are using as courtship signals those features of a male that most reliably indicate his resistance to disease. -

-

68

Animal communication: ideas derived from Tinbergen's activities

In the field of threat signals, the roaring rate of r e d deer a p p e a r s to be u s e d b y other males to assess fighting ability (Clutton-Brock and Albon, 1979). The ability to roar at a high rate and the ability to fight are closely linked b e c a u s e t h e y are both exhausting a n d both use the same muscles. A stag in p o o r condition is simply unable to do either, so ability to maintain a high roaring rate is an h o n e s t indicator of fighting ability. A n o t h e r area in which g a m e theory m o d e l s have contributed is in the debate about the extent to which signals convey information about intentions. Tinbergen, or course, s a w this as an i m p o r t a n t feature of communication. Maynard-Smith (1982), however, initially argued the opposite. He concluded that the evolutionarily stable strategy in a fight w o u l d be never to give a w a y intentions at the b e g i n n i n g of an encounter, b u t to play ' p o k e r faced'. Caryl (1979) s u p p o r t e d this b y citing studies b y Stokes (1962), D u n h a m (1966) and A n d e r s s o n (1976) which s h o w e d that threat displays w e r e not v e r y accurate predictors of an actor's intentions. H o w e v e r this did not s e e m to be a universal finding. Whereas Jakobssen et al. (1979) a n d S i m p s o n (1968) s t u d i e d examples in which fish do not c o m m u n i c a t e their intentions during a fight, Turner and Huntingford (1986) f o u n d another case w h e r e they do. Theory clearly did not always fit the data. Then Enquist and Leimar (1983) p r o d u c e d another g a m e theory m o d e l in w h i c h (using the Zahavian idea of a cost to signalling) they s h o w e d that it can p a y participants to c o m m u n i c a t e their intentions about a fight. Both empiricists and theoreticians could relax. W h e t h e r animals p l a y e d poker faced or c o m m u n i c a t e d their intentions, there w a s a theory on hand to account for all the data. We need m u c h more detailed analysis of the cost of signals in relation to their benefit before w e can predict accurately w h a t animals will do in any given circumstances. W h e n w e turn to m o d e r n ideas a b o u t the variety and design of signals, we find a shift in emphasis from Tinbergen's account in terms of causal explanations to recent interpretations in terms of function. For example, Morton (1975) and N o t t e b o h m (1975) have looked at the nature of songs in different species and populations of birds in relation to the acoustic properties of the e n v i r o n m e n t in they w e r e living. M y student, Mac Hunter, a n d I ( H u n t e r and Krebs, 1979) recorded the songs of great tits living in t w o contrasting habitats, d e n s e forest and o p e n parkland, in different parts of their range. We thus had recordings of a single species in Spain, Iran, Greece, Oxfordshire, S w e d e n , N o r w a y and Poland. We f o u n d a consistent pattern: birds living in o p e n habitats t e n d e d to have a higher m a x i m u m frequency, a greater frequency range and greater complexity than birds living in forest habitats. In other words, w e h a d f o u n d a w i d e ranging

The modern view of animal communication

69

ecocorrelate for the design of signals. Quite w h y it has arisen, is not clear: it m a y be to do with the attenuation of different s o u n d s in different areas (Morton, 1975) or with degradation of s o u n d t h r o u g h reverberation (Wiley and Richards, 1978), b u t the signals are clearly ' d e s i g n e d ' differently in different habitats. As well as looking to the environment to explain signal design, we can also turn to w h a t can be called 'receiver p s y c h o l o g y ' . Guilford a n d Dawkins (1991) have argued that in order to u n d e r s t a n d w h y signals are the w a y they are, w e have to k n o w about the psychology of the animals that are r e s p o n d i n g to the signal. What reactors find easy to detect, discriminate or r e m e m b e r about a signal will be an i m p o r t a n t selective agent in the evolution of signal design. A recent s t u d y b y Ryan et al. (1990) makes this point simply but effectively. They studied two species of Central American frog, Physalaemus pustulosis and P. coloradorum. In P. pustulosis, the male has a courtship call, called the 'chuck" call, which is crucial for getting the female to mate. The chuck call has its main e n e r g y in the range 2-2.5kHz, a n d neatly matching this, the female's auditory s y s t e m is t u n e d to a b o u t the same f r e q u e n c y - her basilar papilla is particularly sensitive to this same f r e q u e n c y range. Even more interesting was that in the closely related species, P. coloradorum, the male does not give the chuck call, b u t the female does have the same frequency sensitivity. Ryan et al. argue that the s e n s o r y bias in the female p r e c e d e d the evolution of the call in the male, while this is not the only interpretation of this result (Pomiankowski and Guilford, 1990), if it is correct it w o u l d provide a very neat example of h o w the design of the signal has evolved a r o u n d receiver psychology. In Zahavi's view, the design 0f signals would, as w e have already seen, d e p e n d on h o w the signals honestly indicate differences in quality. N o t only w o u l d he explain stotting as an h o n e s t indicator of r u n n i n g speed, he w o u l d also explain the design of all other signals in terms of indicators of quality. It might be quite h a r d to explain, say, the difference in song organization b e t w e e n a blackbird and a song thrush, in terms of honest indicators of s o m e t h i n g that was ecologically important and different b e t w e e n those t w o species. Nevertheless, the idea that signals do honestly indicate s o m e quality is an intriguing and heuristically p o w e r f u l one. In s u m m a r y , the T i n b e r g e n - L o r e n z v i e w of c o m m u n i c a t i o n and the n e w e r view contrast in several different ways. Apart from the few examples referred to b y H u n t i n g f o r d (Chapter 4), the s t u d y of the causation of signals in the sense that Tinbergen meant, has virtually stopped. There is also n o w m u c h more emphasis in coevolutionary processes. A l t h o u g h it is possible to infer from s o m e of Tinbergen's writings that he did u n d e r s t a n d that coevolution occurred in signal

70

Animal communication: ideas derived from Tinbergen's activities

evolution, it is not very explicit. H e w r o t e 'All these changes s e e m to aim at one end, adaptation to the responsive capacities of the reactor' (these changes being the changes of ritualization) (1952). H e m a y have u n d e r s t o o d s o m e t h i n g of the evolutionary interactions b e t w e e n signaller and receiver b u t it w a s not a major part of his explanation of w h y signals became ritualized. N o r did he place a n y e m p h a s i s on the distinction b e t w e e n the different coevolutionary routes taken b y cooperative and noncooperative signals, that D a w k i n s and I have stressed (1984). The idea of signalling and h o n e s t y is also completely absent; so is the link b e t w e e n ecology a n d the design of signals. Ironically, although Tinbergen was usually so clear a b o u t the distinction b e t w e e n the four questions (Tinbergen, 1963), he confused functional and causal explanations w h e n it came to courtship displays, for example, he u s e d basically mechanistic accounts of maintaining the pair b o n d or leading to sexual arousal. P e r h a p s w e are n o w m o r e careful to make the distinction. Rather than being satisfied with an account of courtship as serving to maintain the pair bond, we ask why, in evolutionary terms, this is necessary. M a n y of our p r e s e n t functional explanations of signals in terms of a s s e s s m e n t o w e a great deal to M a y n a r d - S m i t h (1982). Having so far looked back, let us n o w look forward. There is r o o m for a great deal of i m p r o v e m e n t in our basic k n o w l e d g e and our conceptual framework. 'Receiver p s y c h o l o g y ' is one area that w o u l d seem particularly rewarding, as w e k n o w surprisingly little about h o w animals perceive signals. Most of our interpretations are anthropomorphic. The claim that great tit songs are more complex in o p e n habitats than in forest habitats (see above) is b a s e d on the fact that it appears that w a y to me. But h o w do I k n o w that great tits or chickens or other birds perceive signals in the same w a y that w e do? This is a very important area for future research. Geoff Cynx and m y former research student, D a n n y Weary, (1990; N o t t e b o h m et al., in press) have already s h o w n one w a y in which it can be fruitfully p u r s u e d . They have asked h o w birds perceive their songs by using operant procedures. For example, in W e a r y ' s s t u d y (1990) a bird is first trained to r e s p o n d to a song by making some response that is rewarded. Then songs differing in various w a y s are i n t r o d u c e d and the bird is effectively asked w h e t h e r it categorizes these s o u n d s as like or unlike the original song. A n o t h e r approach can be illustrated by an experiment carried out by Falls, Dickinson and Krebs (1990). We were working on the eastern m e a d o w l a r k , a species w h e r e individual birds m a y have h u n d r e d s of songs in their repertoire. O n e bird can have in its repertoire s o m e songs that s o u n d very different (to us) and others that s e e m very

71

The modem view of aniumal communication 8

Simitar

• '"~'

I

Contrasting

~'"11

I

I

m,I

I

~I

I

I,

I

I

\

"qII~,,.

i,

el

g ~-

I

I

I

i

~i

i

o,

I

IiII

Ili

i

I

11

a

ii O

0

'

,

,

,

,

,

Time (s)

Figure 5.2 Sonagrams of the song types used in constructing the playback experiments on eastern meadowlarks. Each row shows songs from one individual bird's repertoire, classified as to whether they were similar (to humans) or contrasting. (From Falls et al., 1990).

similar (Fig. 5.2) We w a n t e d to k n o w w h e t h e r the m e a d o w l a r k s also perceive the songs as either different or similar, and a t t e m p t e d to find o u t b y p lay in g each bird a d o u b l e playback tape a n d r e c o r d i n g its response. The tape might start off with song A and then switch halfway t h r o u g h to s o n g B. S o m e t i m e s A a n d B w e r e v e r y similar (to us) a n d at o th er times v e r y different. W h a t w e w e r e looking for was e v i d e n c e that the birds could detect the c h a n g e o v e r from A to B, w h i c h w o u l d be e v i d e n c e that t h e y could detect the difference. T he a n s w e r w e got w a s v e r y surprising. If t w o songs w e r e t a k e n f r o m t he b i r d ' s o w n repertoire, t h e n it was perfectly well able to detect the switch b e t w e e n t w o 'similar' songs. In fact, for its o w n songs, t here was as m u c h c h a n g e in b e h a v i o u r b e t w e e n t w o songs we h a d classified as similar as b e t w e e n t h o s e songs w e h a d classified as different. H o w e v e r , if the test songs came f r om the r e p e r t o i r e of a n o t h e r bird that was c o m p l e t e l y unfamiliar to the test bird, it a p p e a r e d oblivious to the subtle c h a n g e s a n d onl y r e s p o n d e d to the larger c h a n g e s that w e r e m o r e obvious to us. This s t u d y s h o w s us that the p e r c e p t i o n side of animal c o m m u n i c a t i o n m a y be quite subtle, a n d h o w , in this case, e xp er ien ce can influence w h a t the animal perceives as bei ng similar

72

Animal communication: ideas derived from Tinbergen's activities

or d i f f e r e n t . It also a p p e a r s , as s u g g e s t e d b y N o t t e b o h m et al. (1990) t h a t t h e r e is a close link b e t w e e n p e r c e p t i o n a n d p r o d u c tion. A final area of a n i m a l c o m m u n i c a t i o n w h i c h I see as a c h a l l e n g e for the f u t u r e c o m e s f r o m Z a h a v i ' s (1975, 1987) idea t h a t signal d e s i g n can b e u n d e r s t o o d in t e r m s of h o n e s t signalling m a i n t a i n e d b y cost. I g a v e a f e w e x a m p l e s earlier of h o w ' h o n e s t y ' d o e s s e e m to b e a f e a t u r e of v a r i o u s signals. If this is a w i d e s p r e a d p h e n o m e n o n , t h e i m p l i c a t i o n s for u n d e r s t a n d i n g a v a r i e t y of as y e t u n e x p l a i n e d signals are i m m e n s e .

ACKNOWLEDGEMENTS I t h a n k the Royal Society for financial s u p p o r t . Marian D a w k i n s t u r n e d a r e c o r d i n g of m y l e c t u r e i n t o a m a n u s c r i p t w i t h r e m a r k a b l e skill a n d e n e r g y : I a m m o s t g r a t e f u l to her.

REFERENCES Andersson, M. (1976) Social behaviour and communication in the Great Skua. Behaviour, 58, 40-77. Borgia, G. (1985) Bower quality, number of decorations and mating success of male satin bowerbirds (Ptilinorynchus violaceus): an experimental analysis. Animal Behaviour, 33, 266-71. Caryl, P.G. (1979) Communication by agonistic displays: what can games theory contribute to ethology? Behaviour, 68, 136-69. Clutton-Brock, T.H. and Albon, S.D. (1979) The roaring of red deer and the evolution of honest advertisement. Behaviour, 69, 145-70. Cullen, J.M. (1966) Reduction of ambiguity through ritualisation. Philosophical Transactions of the Royal Society B 251, 363-74. Davies, N.B. and Halliday, T.R. (1978) Deep croaks and fighting assessment in toads, Bufo bufo. Nature, Lond. 274, 683-85. Dawkins, R. (1976) The Selfish Gene, Oxford University Press, Oxford. Dawkins, R. and Krebs, J.R. (1978) Animal signals: information of manipulation?, in Behavioural ecology: an evolutionary approach (eds. J.R. Krebs and N.B. Davies), Blackwell Scientific Publications, Oxford, pp. 282-309. Dunham, D.W. (1966) Agonistic behaviour in captive rose-breasted grosbeaks, Pheucticus ludovicianus (L.) Behaviour, 27, 160-73. Enquist, M., Plane, E. and R6ed, J. (1985) Aggressive communication in fulmars (Fulmarus glacialis) competing for food. Animal Behaviour, 33, 1007-20. Enquist, M. and Leimar, O. (1983) Evolution of fighting behaviour: decision rules and assessment of relative strength. Journal of Theoretical Biology, 102, 387-410. Falls, J.B., Dickenson, T.E. and Krebs, J.R. (1990) Contrast between successive

References

73

songs affects the response of eastern meadowlarks to playback. Animal Behaviour, 39, 717-28. Fitzgibbon, C.D. and Fanshawe, J.H. (1988) Stotting in Thomson's gazelles: an honest signal of condition. Behavioural Ecology and Sociobiology, 23, 69-74. Grafen, A. (1990) Biological signals as handicaps. Journal of Theoretical Biology, 144, 517-46. Guilford, T. and Dawkins, M. (1991) Receiver psychology and the evolution of animal signals. Animal Behaviour (in press). Hamilton, W.D. (1964) The genetical evolution of social behaviour. Journal of Theoretical Biology, 7, 1-52. Hamilton, W.D. and Zuk, M. (1982) Heritable true fitness and bright birds: a role for parasites? Science, NY. 218, 384-87. Hunter, M.L. and Krebs, J.R. (1979) Geographical variation in the song of the great tit (Parus major) in relation to ecological factors. Journal of Animal Ecology, 48, 759-86. Huxley, J. (1966) (organizer) A discussion on ritualization of behaviour in animals and man. Philosophical Transactions of the Royal Society, B. 251, 247-526. Jakobssen, S., Radesater, T. and Jarvi, T. (1979) On the fighting behaviour of Nannacara anomala (Pisces, Cichlidae) Zeitschrifl fiir Tierpsychologie, 49, 210-20. Kodric-Brown, A. and Brown, J.H. (1984) Truth in advertising: the kinds of traits favoured by sexual selection. The American Naturalist, 124, 309-23. Krebs, J.R. and Dawkins, R. (1984) Animal signals: mind reading and manipulation, in Behavioural Ecology. An evolutionary approach, 2nd. edn, (eds J.R. Krebs and N.B. Davies). Blackwell Scientific Publications, Oxford, pp. 380-402. Lloyd, J.E. (1979) Mating behaviour and natural selection. Florida Entomol, 62, 17-34. Maynard-Smith, J. (1982) Evolution and the theory of games, Cambridge University Press, Cambridge. Maynard-Smith, J. and Parker, G.A. (1976) The logic of asymmetrical contests. Animal Behaviour, 24, 159-75. Morton, E.S. (1975) Ecological sources of selection on avrian sounds. The American Naturalist, 109, 17-34. Nottebohm, F. (1975) Continental patterns of song variability in Zonotrichia capensis: some possible ecological correlates. The American Naturalist, 109, 605-24. Nottebohm, F., Alvarez-Buylla, A., Cynx, J. et al. (1990) Song-learning in birds: the relation between perception and production. Philosophical Transactions of the Royal Society B 329. Ryan, M.J., Fox, J.H., Wilczynski, W. and Rand, A.S. (1990) Sexual selection for sensory exploitation in the frog Physalaemus pustulosis. Nature, Lond., 343, 66-7. Simpson, M.J.A. (1968) The display of Siamese fighting fish, Betta splendens. Animal Behaviour Monographs, 1, 1-73. Stokes, A.W. (1962) Agonistic behaviour among blue tits at a winter feeding station. Behaviour, 19, 208-18. Tinbergen, N. (1952) 'Derived' activities, their causation, biological significance, origin and emancipation during evolution. Quarterly Review of Biology, 27, 1-32.

74

Animal communication: ideas derived from Tinbergen's activities

Tinbergen, N. (1963) On the aims and m e t h o d s of ethology. Zeitschrifl fiir Tierpsychologie, 20, 410-33. Turner, A. and Huntingford, F.A. (1986) A problem for game theory analysis: assessment and intention in male mouthbrooder contests. Animal Behaviour 34, 961-70 Weary, D. (1990) Categorization of song notes in great tits: which acoustic features are used and why? Animal Behaviour, 39, 450-57. Wiley, R.H. and Richards, D.G. (1978) Physical constraints in acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behavioural Ecological and Sociobiology, 3, 69-94. Zahavi, A. (1975) Mate selection - a selection for a handicap. Journal of Theoretical Biology, 53, 205-14. Zahavi, A. (1979) Ritualization and the evolution of m o v e m e n t signals. Behaviour, 72, 77-81. Zahavi, A. (1987) The theory of signal selection and some of its implications, in International Symposium of Biological Evolution, (ed. V.P. Delfino), Adriatica Editrice, Bari. Zuk, M., Johnson, K., Thornhill, R. and Ligon, D.J. (1990a) Mechanisms of female choice in red jungle fowl. Evolution, 44, 477-85. Zuk, M., Thornhill, R., Ligon, J.D. et al. (1990b) The role of male o r n a m e n t s and courtship behaviour in female mate choice of red jungle fowl. The American Naturalist, 136, 459-73.

m6 The nature of culture JUAN D. DELIUS

' T o w n l e y . . . h a d said one w o r d only, and that one of the shortest in the language, but Ernest was in a fit state for innoculation, a n d the m i n u t e particle of virus set about w o r k i n g i m m e d i a t e l y ' . (Samuel Butler, 'The Way of All Flesh', 1903)•

CULTURE AND BIOEVOLUTION Niko Tinbergen laid great stress on the essential importance of cultural evolution for the u n d e r s t a n d i n g of h u m a n behaviour a l t h o u g h he never, of course, m a d e it a central subject of his research interests. In a short cautionary note about the future of h u m a n i t y he wrote for example that 'our u n i q u e position in the m o d e r n world is due to the consequences of our cultural evolution, w h i c h . . , h a s . . , progress i v e l y . . , superimposed (itself) on our still ongoing genetic evolution' and that 'we transfer . . . . from one generation to the next, not only our genetic heritage but also (our) accumulated non-genetically acquired • . . experience' (Tinbergen, 1977, see also Tinbergen, 1976). Niko's insights into the details of the processes of cultural evolution w e n t m u c h further than his writings reflect, however. A casual but memorable conversation between him and Konrad Lorenz in Stuttgart, G e r m a n y in 1959, at which I h a p p e n e d to be present, revealed that clearly• The role of song behaviour as a species-isolating m e c h a n i s m in some sympatric birds had s o m e h o w cropped up. They were considering the selective forces that might have shaped the divergence of song patterns in such situations w h e n Niko raised the important

76

The nature of culture

question: Selection of what? Surely not genes since the s o n g of these birds was likely to be learned, not innate. Konrad suggested that song traditions were being selected b u t Niko considered that it might be better to think of song m e m o r y traces being selected. W o u l d m e m o r y evolution always cooperate with gene evolution? In the 20 m i n u t e s or so that followed, w i t h o u t ever mentioning the w o r d culture, if I r e m e m b e r correctly, they h a d w o r k e d out b e t w e e n t h e m the essentials of a m o d e r n theory of cultural evolution. There w e r e h o w e v e r several later dialogues at the Ravenglass field camp where Niko actually p u r s u e d similar a r g u m e n t s explicitly in relation to h u m a n culture. In recent years, I have tried again and again to recapture s o m e of the threads of those discussions. N e e d l e s s to say, b e s i d e s imperfect recollections, this essay also takes into account some of the theoretical ideas and empirical findings (these latter are still scarce) of m a n y scholars that since Tinbergen's times have m a d e cultural evolution a more definite subject of their interest (notably Campbell, 1969; Bajema, 1972; Dawkins, 1976; Cavalli-Sforza and Feldman, 1981; L u m s d e n and Wilson, 1981; Boyd and Richerson, 1985). It is time to h e e d the m a e s t r o ' s ever-recurring a d m o n i t i o n s a b o u t defining one's terms. Indeed, the w o r d culture is c o m m o n l y used with several meanings. For the p u r p o s e s of this essay it is necessary to circumscribe its definition to behavioural culture. Culture will thus mean here the ensemble of traditional behaviours that is characteristic of a population. Traditional behaviours are those that individuals take over from others through s o m e form of social learning. S o m e t i m e s media (for example n e w s p a p e r s , books, television) intervene in this process of transmission. Behaviour patterns that organisms acquire via genetic inheritance (for example hatching, crowing, smiling, crying) or by individual learning (key-pecking, soft landing, nose-picking, masturbating) are excluded by this definition. This t r i c h o t o m o u s classification of b e h a v i o u r is a v o w e d l y simplistic but here it is conceptually useful. Some illustrative examples of cultural behaviour could be birds nesting in a traditional area, singing a certain dialect and m o b b i n g particular predators, or h u m a n s wearing a particular dress, speaking a certain language, reading a certain bestseller, and w o r s h i p p i n g a particular god. Material objects by the a b o v e definition are not really part of culture, but they are often c o n v e n i e n t referents for the cultural b e h a v i o u r that p r o d u c e d t h e m or is elicited by t h e m (the b o o k or the clothing in the above examples). The definition h o w e v e r appears to be able to a c c o m m o d a t e without m u c h strain most other, less tangible 'contents' of culture c o m m o n l y listed in a n t h r o p o l o g y textbooks (Harris, 1987): k n o w l e d g e , beliefs, rituals, institutions, customs, fashions, symbols, etc.

Culture and bioevolution

77

Culture is clearly not a universal attribute of all organisms. In fact, only t w o or three decades ago it w a s t h o u g h t that only h u m a n s w e r e e n d o w e d with culture. This opinion is no longer held. Cultures, or at least protocultures, have n o w b e e n d o c u m e n t e d in m a n y animals (Bonner, 1980), b u t it is also true that the p h e n o m e n o n only occurs in a proportion of the more a d v a n c e d species. The permissive trait, as s u g g e s t e d b y the above definition of culture, is that t h e y m u s t be capable of social learning, a c o m p e t e n c e that c o m e s about t h r o u g h biological evolution. Even w h e n this basic capability is already present, culture is the product of a lengthy historical development. The cultural behaviours p r o p e r for knights, Scots, or ' y u p p i e s ' are clearly not godgiven b u t have d e v e l o p e d gradually over a long time. Their c o m m o n ancestors 50 000 years ago, the C r o m a g n o n s , certainly did not s h o w the cultural traits w e n o w associate with these groups. The cultural evolution process has long b e e n recognized as having at least superficial similarities with that which drives biological evolution. A m o r e t h o r o u g h anlaysis of the potential analogy has h o w e v e r b e g u n only recently. The intention of this essay is essentially to explore h o w far the similarities b e t w e e n biological a n d cultural evolution actually go. Consideration of h o w the capacity for culture might have e m e r g e d affords the opportunity to briefly recapitulate the salient characteristics of biological evolution. It is a game that genes are simply fated to play as a c o n s e q u e n c e of their particular molecular properties (Dawkins, 1976). The essential property is that they are capable of self-replication that is not always perfect. Since the gene m u t a n t s that arise in this w a y interact with and c o m p e t e for an environmental niche in which to survive and replicate, it follows that they will frequently differ in replication potential, that is in fitness. The c o n s e q u e n c e is gene selection. In different niches different mutations m a y be the fittest, and this eventually results in speciation. G e n e s capable of instructing the synthesis of buffering devices, a m e m b r a n e or even a soma, against environmental variability are likely to have fitness advantages. G e n e mutants that could instruct devices that a d d e d motility and also sensitivity, b e h a v i o u r in short, would, given the right circumstances, be even fitter. Which r e s p o n s e s followed w h i c h stimuli w a s initially d e t e r m i n e d exclusively b y genetic instruction (innate behaviour). In e n v i r o n m e n t s that were more variable over time a n d space, selection pressure arose for mutations that could instruct neural structures capable of learning. The capacity, for example, to attach existing r e s p o n s e s to arbitrary stimuli that h a p p e n to be predictive of fitnessinfluencing events (classical conditioning) or to modify b e h a v i o u r in such a w a y as to influence the likelihood of such events (instrumental learning) as a c o n s e q u e n c e of individual experience obviously

78

The nature of culture

magnifies the adaptability of organisms (Staddon, 1983). M u t a n t s extending m e m o r y capacities so that a representation of the environm e n t and the self w a s feasible signified a further b o n u s . A n internal off-line b e h a v i o u r simulation w o u l d b e c o m e possible, w h i c h could even include creative innovation (insight learning). Generally, learning is a device instructed by genes that allows the individual to acquire k n o w l e d g e about the world and itself over and above that implicitly contained in its genetic code. It is naturally also associated with costs, such as more complex brains and s o m e behavioural instability. SOCIAL LEARNING AND CULTURE W h e n an organism acquires behaviour through individual learning, the process is often lengthy, risky and laborious. Genes giving rise to structures that enabled animals to take over the already extant experience of conspecifics w o u l d often yield a fitness advantage. The essential characteristic of social learning (imitation, observation, instruction learning) is indeed that individuals in one way or another take over k n o w l e d g e from others. The precise m e c h a n i s m s s u p p o r t i n g this transmission of information vary considerably (Zentall and Galef, 1988). Pigeons, as do m a n y other species, tend to b r e e d at sites close to those w h e r e they themselves were bred. Successive generations keep to traditional breeding g r o u n d s and this is not for w a n t of mobility, as they may migrate far in b e t w e e n breeding. Through an imprintinglike process, juveniles store information about the location w h e r e they g r o w up. This enables them to navigate back to the h o m e area later (Schmidt-Koenig, 1965). It is not only the geographical location to which the y o u n g birds imprint b u t also to the particular habitat in w h i c h they were raised, to cliffs or buildings for example. As adults they will then s h o w a preference for the same type of s u r r o u n d i n g s in which they grew up (Delius, u n p u b l i s h e d observations; Klopfer and Hailman, 1965). This does not come about by the y o u n g s t e r s directly imitating the parents but rather by the parents bringing their y o u n g s t e r s u p w h e r e they can only learn about one thing. There is often a debate about w h e t h e r this represents true social learning, but it certainly serves to maintain familial traditions. Seeing several flock m e m b e r s fly to a particular site usually induces other pigeons to follow. Such socially facilitated b e h a v i o u r n e e d not involve any learning, often being based on innate behaviour (Tinbergen, 1953). But at the same time follower pigeons can hardly fail to learn about the association b e t w e e n , for example, granaries and grain, something that the leading pigeons already k n e w (Murton et al., 1972). In s o m e altricial species the parents lead their y o u n g to sites w h e r e

Social learning and culture

79

the food that they themselves prefer predominates and each of the young learns on its own to find and deal efficiently with these items (Subowski, 1989). Thus again traditions may simply be maintained by parents biasing the learning opportunities of their offspring. Oystercatchers prey on mussels using one of two techniques, stabbing or hammering. Youngsters appear to learn the particular technique that the parents used through observation and participation (Norton Griffiths, 1967; but see Meire and Ervynick, 1986). In a similar context female cats with kittens may even display behaviour analogous to teaching by repeatedly bringing home and releasing live prey just to catch it again. Kittens gradually join the repeated chases and eventually learn to to do the final killing themselves (Chesler, 1969; Ewer, 1969). Contrived non-natural modes of food gathering have been experimentally arranged to arise through imitative instrumental learning in several species. Having seen another pigeon obtain food from an electromagnetic dispenser after performing the somewhat arbitrary behaviour of pecking an illuminated disc considerably facilitates the subsequent acquisition of that same skill by observer pigeons. A number of experiments show that the information the observer acquires can be multifarious: knowledge of the fact that food is to be found in the particular environment; that it is available at a particular place within that environment; that performance of certain acts make that food more available, and so on. It is rare, however, for an observer to produce the correct food-yielding behaviour on the first attempt. Rather, the observer is only quicker at learning what has to be done. An opportunity to perform the target behaviour while observing is helpful but learning is also facilitated w h e n key-pecking is only possible after a delay (Alderks, 1986; Biederman et al., 1986; Hogan, 1986). Lefebvre (1986) set up an artificial feeding tradition among a flock of urban pigeons. They captured a few flock members and trained them to feed by piercing a tight paper sheet covering their food troughs. When they were released and were back with their flock, the latter was offered paper-covered troughs. The trained birds immediately began to pierce and feed. Soon no fewer than two dozen other birds had acquired the paper-piercing technique. In a control flock that did not have pretrained demonstrators it took almost three times as long before a bird 'invented' paper piercing by himself, but once that happened, the cultural trait spread just as fast among that flock. Novel feeding cultures occasionally arise naturally among freeranging animals. A Japanese female macaque n a m e d Imo discovered in 1953 that sweet potatoes which she had accidently dropped in a brook tasted better than unwashed, earthy ones and began to actively wash them before consumption. By 1958 all the younger monkeys in

80

The nature of culture

her b a n d had imitated her: a potato-washing culture had arisen. Other Japanese m o n k e y groups have never d e v e l o p e d this tradition in spite of similar opportunities, b u t s o m e have d e v e l o p e d other local traditions (Nishida, 1987). Social learning can also be m e d i a t e d b y classic conditioning. Wildcaught blackbirds exhibit m o b b i n g b e h a v i o u r w h e n t h e y see an owl. Curio et al. (1978) arranged it that a predator-naive, hand-raised blackbird s a w a novel inoffensive plastic bottle, while an experienced bird actually m o b b e d an owl. M o b b i n g acts as an u n c o n d i t i o n e d stimulus: the naive blackbird b e g a n to m o b too ( u n c o n d i t i o n e d response, see social facilitation above). The bottle functioned as a conditioned stimulus as it always p r e c e d e d and a c c o m p a n i e d the o w l - m o b b i n g b y the model. After a f e w pairings, conditioned m o b b i n g could be d e m o n s t r a t e d . In the absence of any m o d e l the observer blackbird n o w m o b b e d w h e n e v e r the bottle was presented. The acquired bottlem o b b i n g habit could in turn serve as m o d e l for n e w observers. Thus a novel mobbing tradition or culture had been set up among blackbirds. The cultural nature of songbird song is so well k n o w n that only the most essential characteristics and the most c o m m o n variants of the underlying process will be m e n t i o n e d . Song varieties that y o u n g birds hear from their father or his n e i g h b o u r s are m e m o r i z e d during a critical period. This imprinting usually takes place before the y o u n g s t e r s can t h e m s e l v e s sing. Later the sub-adults learn to match the auditory template with their o w n song. Barring occasional errors, this leads to a fairly accurate replication of the songs originally heard. Normally this m o d e of song acquisition leads to the emergence of song dialects characteristic of local populations within a given species (Barker and C u n n i n g h a m , 1985; Catchpole, 1986). S o m e species continue to be able to acquire songs all their lives and s o m e m a y e v e n imitate the s o u n d of other species. There are almost 4000 species of songbirds and it is resonably certain that, except for a few, all sing according to traditions. This suggests that their c o m m o n ancestor, the original songbird living about 40 million years ago, already had a song culture, long before our primate ancestors had a n y culture. Most other taxonomic bird groups have innate songs b u t parrots are also well k n o w n for learning vocalizations b y imitation. Since parrots are only distantly related to songbirds, b u t closely related to birds that have innate vocalizations, their cultures m u s t have arisen, i n d e p e n d e n t l y (Kroodsma and Miller, 1982). In the h u m a n species, social learning is almost obligatory and often involves yet another, m o r e refined variant. H a v i n g previously seen s o m e b o d y light a camp fire is certainly of assistance if one had to do the same thing for the first time. The demonstrator performs on the basis of

Mnemobiology and memes

81

information stored in his or her m e m o r y . The behaviour thus p r o d u c e d is seen by the observer, w h o in t u m stores these perceptions in memory, only to convert t h e m again into behaviour at a later date. In such cases, the model has to p e r f o r m for the observer to be able to m e m o r i z e the actions. Language, however, enables an energetically more economical form of m e m o r y transfer. Simply being told h o w to light a camp fire is usually sufficient for a reasonable emulation. In most situations where h u m a n individuals adopt behavioural traits from others, language plays an i m p o r t a n t supportive, if not sole m e d i a t i n g role. It has, i n d e e d , been a r g u e d that l a n g u a g e m i g h t have arisen evolutionarily as an extension of social learning, as a vehicle for instruction, w h e r e b y recipes for b e h a v i o u r could be t r a n s m i t t e d in an abstract symbolic way, in a code that m i g h t be related to that of m e m o r y (Catania, 1985; Delius, 1990). For a Homo habilis h u n t e r a million years ago it m u s t have been a w k w a r d to d e m o n strate to novices h o w to stalk antelopes; it w o u l d have been m u c h easier to tell t h e m h o w it s h o u l d be done. Linguistic messages function like an almost effortless short circuit b e t w e e n the m e m o r i e s of individuals. Accordingly, it accounts for m u c h of the sophistication of h u m a n culture vis dl vis animal culture. Indeed, linguistic communication, spoken or written, is sometimes the only m e d i u m by which m a n y h u m a n traditions can be transmitted. Writing greatly amplifies the multiplicative p o w e r of language. Most importantly, it disposes of the necessity for the model a n d the observer to have to coincide in time and space for transmission to be possible. In a way, it makes social learning possible in an asocial setting. M o d e r n c o m m u n i c a t i o n media extend this even further.

M N E M O B I O L O G Y A N D MEMES Generally, learning, w h e t h e r individual or social, can be conceived as a process w h e r e b y experiental information is stored into m e m o r y . Cultural traits, defined earlier as behavioura| items acquired t h r o u g h social learning, are therefore also r e p r e s e n t e d as particular contents in the m e m o r y of the individual bearers of culture. Information storage is necessarily d e p e n d e n t on physicochemical state changes in m e m o r y - s u p p o r t i n g structures. According to neurobiological findings, learning (social or otherwise) leads first to volatile changes, lasting only tens of seconds or m i n u t e s . O n l y w h e n learning is sufficiently incisive in one w a y or another, will the relevant m e m o r y traces be consolidated into a more durable format lasting m o n t h s or years. Culture as a rather persistent p h e n o m e n o n is obviously heavily d e p e n d e n t on these long-term memories.

82

The nature of culture

Long-term m e m o r y , according to current evidence, is laid d o w n as structural brain modifications. M e m o r y deposition chiefly involves changes at the level of the interneuronal transmission sites, the s y n a p s e s (Morris et al., 1988; Dudai, 1989). D u e to the particular patterns of coactivation of pre- and postsynaptic neurons arising during learning, some of these s y n a p s e s pass from a state of relative inefficiency to a state of relative efficiency, from an inactivated to an activated condition, rather like bits in c o m p u t e r m e m o r y that are set from a 0 off-state to a 1 on-state. In s o m e instances, learning e v e n seems to lead to the b u d d i n g of additional synapses and to the growth of neuronal ramifications s u p p o r t i n g t h e m (Horn, 1986). H o w e v e r , m u c h as c o m p u t e r m e m o r y also stores information w h e n bits pass from a 1 to a 0 state, there s e e m s to be instances w h e r e learning is associated with s y n a p s e s passing from an activated to an inactivated state or even disappearing, sometimes together with their supportive structures (Wallhausser a n d Scheich, 1987). That specifically social learning is also associated with such neural modifications is best d o c u m e n t e d for songbird vocalizations ( D e v o o g d et al., 1985). A pigeon brain contains p e r h a p s 101°, the h u m a n brain m a y b e 1015, synapses that are variable in the above sense. Such plastic synapses have to be thought of as the critical c o m p o n e n t s of neural networks functioning as associative arrays. It has b e e n s h o w n mathematically and confirmed empirically that neural networks incorporating large numbers of modifiable junctions are able to store vast quantities of information in a very organized manner. An important property of associative network storage is that the information is content- and not address-retrievable (as in computers), and furthermore that it is stored in a highly distributed but still partially overlapping w a y (Palm, 1982). Special versions of these networks s h o w interesting additional properties, such as being capable of self organization, stimulus pattern categorization, pattern completion or complex stimulus-response conversions (Kohonen, 1984; Rummelhardt and McClelland, 1986). Any cultural trait taken over by a given individual from another individual must accordingly be thought of as the transfer of a particular pattern of activated/inactivated s y n a p s e s from the associative networks of one brain to another. Different traits must be t h o u g h t of as being c o d e d by topologically different synaptic patterns, that is, a given cultural trait borne by an individual is encoded informationally as a particular configuration of modified synapses in his or her brain (Figure 6.1). Naturally the synaptic constellation that a trait has in one brain will not be geometrically arranged in exactly the same way as the pattern that the same trait has in another brain: the brains of different individuals are likely to be too different for that. Functionally however, the two patterns could still be

Mnemobiology and memes

83

Figure 6.1 A meme as a constellation of activated neuronal synapses lodged somewhere in the brain of an individual equivalent w h e n effectively identical traits were r e p r e s e n t e d in memory. In a n y case, following Dawkins (1976), synaptic patterns that code cultural traits will be called memes, by analogy with the molecular patterns that code biological traits and which are called genes. The process of cultural heritage can be seen as passing on these synaptic constellations or m e m e s from one individual to another, or, and that is important, to several other individuals. Obviously it is not a bodily replication of material structures, as is usual with genes, but social learning nonetheless brings about a multiplicative transfer of equivalent structures. Even a m o n g genes, however, replication can sometimes be less than direct. Retrovirus RNA genes for example d e p e n d heavily on mediation by host cellular m a c h i n e r y for reproduction (Davies et

84

The nature of culture

al., 1980). M e m e s are capable of instructing, not protein synthesis as genes do, but behaviour. H o w e v e r , genes can do that too indirectly t h r o u g h protein synthesis. O n the other h a n d m e m e replication, by involving neurostructural modifications, is invariably associated with the induction of protein synthesis. G e n e s can be conceived as specific molecules that code information according to a well u n d e r s t o o d scheme. Until the 1950s however, genes were largely hypothetical constructs that could not be linked to a n y t h i n g more specific t h a n approximate sites on chromosomes. Memetics is not yet as a d v a n c e d as genetics. M e m e s are still largely abstract inferential entities, though we know that they are information coded in neural structures. It is possible and even likely that the memetic code is less universal and more complex than the genetic one. However, the way in which genes code innate behaviour, say the suckling reflex or the crying response of babies, is a n y t h i n g but simple a n d unitary. Some authors (CavalliSforza and Feldman, 1981; Boyd and Richerson, 1985) nevertheless prefer to speak of cultural traits or cultural variants rather t h a n of m e m e s (or culturgenes; L u m s d e n a n d Wilson, 1981). That seems linguistically cumbersome. M e m e s stress the transmittance of coded information rather t h a n of behaviour itself, which is a physical impossibility. In genetics it is conceptually important to separate the p h e n o t y p i c characters and the genes that determine it. It must be admitted, though, that because of the unsatisfactory state of memetics we are still as rule forced to allude to m e m e s by way of trait descriptions. The important point is that m e m e s have the same essential properties that make genes the key protagonists of an evolutionary process (Dawkins, 1976). They are obviously capable of replication, even if in a r o u n d a b o u t way. Replication is reasonably faithful but not perfect, that is, m e m e s mutate. N e w song variants arise a m o n g songbirds, n e w w o r d s are coined, n e w rituals are derived a n d n e w fads emerge a m o n g h u m a n s . Not all m e m e variants are equally effective in reproducing themselves. Some m e m e s spread rapidly in a population, others become extinct. 'I k n o w something, but I w o n ' t tell a n y b o d y ' is a nonstarter as m e m e s go, but 'I will tell y o u a sure w a y to save tax' stands for a m e m e likely to multiply (Ball, 1984). Different m e m e s have different cultural fitnesses, that is, m e m e s vary in their potential to p r o d u c e memetic offspring.

GENE/MEME SYMBIOSES There are two characteristics that seem to make the m e m e s of an individual plainly different from his genes. O n e is that his m e m e s are lodged in the brain that was instructed by his genes, i.e. the former

Gene/meme symbioses

85

d e p e n d on the latter. The other is that the individual's genes come from his parents, but his memes can and often do originate from other conspecifics besides his parents (friends and teachers for example). A host-guest relationship is not at all exceptional among genes themselves, the genes of m a n y symbiotic organisms residing in organisms instructed by the genes of other organisms. Any average human, for example, is normally host to billions of symbiotic organisms belonging to perhaps a thousand different species (Hohorst, 1981). His phenotype is not determined by his h u m a n genes but also by the genes of all the symbionts he happens to be infected with. The symbiont species an individal carries usually have a very varied provenance, with only a few being likely to have come from his parents. Three kinds of organismic symbioses are distinguished: mutualism, where both partner species benefit from the association in terms of Darwinian fitness (gastric flora of ruminants, for example); commensalism, where the fitness of the guest is furthered by the association with little if any fitness cost or gain to the host (intestinal flora of man, for example); and parasitism, where the symbiont profits on fitness at the expense of the fitness of the host (tapeworms in humans, for example; Smith and Douglas, 1987). A striking instance of a symbiosis of the mutualistic kind are the mitochondria, extranuclear cytoplasmatic organelles of eukaryotic organisms. Mitochondria have their own DNA, which replicates independently of the host-cell DNA. The ancestors of mitochondria some 2 billion years ago were almost certainly parasites in prekaryotic organisms, much as viruses are parasites in present day cells (Margulis, 1981). Nowadays, mitochondria are highly integrated into the higher organisms and are not capable of independent existence. On the other hand, essential processes of host cell respiration are controlled by mitochondria and accordingly they are prominent in metabollically very active neurons. In fact, even the slightest behaviour, the most fleeting thought produced by a eukaryotic animal absolutely presupposes the activity of these obligatory symbionts. Infection is always through the egg cytoplasm; sperm do not carry mitochondria. Mitochondrial DNA undergoes an evolution of its own. Mutant mitochondria emerge occasionally, may replicate and can be favoured or disfavoured by natural selection. The selective agency is the intracellular environment, largely but not exclusively controlled by the host cells' nuclear genes (Cannet al., 1987). Many parasitic species can influence the behaviour of their hosts in very specific ways (Moore, 1984). The rabies virus, for example, massively invades the host's salivary glands and causes them to secrete profuse quantities of infected saliva, but it also invades the nervous system and influences its functioning so as to inhibit swallowing and

86

The nature of culture

increase aggressiveness. The sick animal therefore bites with a large reservoir of infested saliva a n d is t h u s very likely to infect its victim, which as a rule is no relation and might even belong to another species (Christie, 1981). But it is a p p a r e n t that the rabies virus furthers its fitness at the cost of the h o s t ' s fitness, partly b y manipulating the latter's behaviour. Parasites inevitably generate selection pressure for host m u t a n t s that are s o m e h o w able to prevent or inhibit infection and/or multiplication of the parasites. Immunological reactions that counteract infections, b u t also innate b e h a v i o u r that minimizes chances of infection (pelage grooming, clear water drinking, avoidance of sick conspecifics, for example) p r o m o t e host fitness. Conversely parasites are u n d e r natural selection to increase their ability to infect a n d replicate. Since they often r e p r o d u c e at high rates within the host organism, evolutionary adaptation to the i m m u n e reactions of the host (or to drug treatment) can come about by selection of resistant mutants within a single host individual. This often mimics Lamarckian evolution because the 'offspring' infection p a s s e d onto the next host expresses w h a t appears to be a trait acquired by the 'parent' infect (antibiotic resistance, for instance; F u t u y m a , 1986). There is obviously also selective pressure u p o n host organisms to d e v e l o p m e c h a n i s m s for resisting infection or turning parasite organisms into mutualists, or at least into commensals, if at all possible. A too-virulent parasite can potentially kill its host before there has been transmission to further hosts, a n d thus kill itself and its kin. Restrained virulence m a y be a better fitness strategy. Parasites m a y therefore also be u n d e r some selection pressure to b e c o m e mutualists or at least commensals (Anderson and May, 1982) but it competes with o p p o s i n g p r e s s u r e s that tend to make parasites more infectious. An i m p r o v e d immunological r e s p o n s e b y a host will generate a selective pressure favouring parasite mutants that can overcome it. This coevolutionary arms-race game is biased by the fact that the usually smaller symbionts have, in general, a much faster generational turnover than the larger hosts. C o n s e q u e n t l y the relative rates of adaptation and counteradaptation are in favour of parasites rather than hosts. In so far as m e m e s are material structures (arrays of modified synapses) that reside in host organisms and can multiply i n d e p e n dently of them, they can be v i e w e d as analogous to the genes of symbionts. In particular, m e m e s are similar to the genes of those s y m b i o n t s that invade the brain of their host and influence its functioning in w a y s that affect the h o s t ' s behaviour. M e m e s are replicating c o d e d information packages, which infect s o m e higher animals and manipulate their behaviour. Furthermore their replication,

Gene/meme symbioses

87

analogously to that of s y m b i o n t genes, is not tied to the g e n e r e p r o d u c t i o n of host organisms. W h e n dealing with organismic symbioses, one distinguishes b e t w e e n the genetic fitness of hosts a n d the genetic fitness of g u e s t s even t h o u g h t h e y are both intimately intertwined. Similarly it is essential to differentiate b e t w e e n the genetic (biological) fitness of bearers of cultural traits and the m e m e t i c (cultural) fitness of the cultural traits t h e m s e l v e s (Ball, 1984). As is the case in symbionts, specific m e m e s or m e m o m e s ( m e m e complexes, in analogy to genomes) could in principle survive and r e p r o d u c e to the advantage, indifference or detriment of the genetic fitness of their hosts, so that cultural traits could be mutualists, c o m m e n s a l s or parasites. Initially, at the phylogenetically protocultural stage, m e m e s m u s t necessarily have been mutualists simply because the capacity for culture, the genetically determined ability for social learning, can only have spread within a population of organisms if individuals having that c o m p e t e n c e were biologically fitter than those that did not h a v e it. The genetic fitness advantage of an individual w a s d e t e r m i n e d b y the actual cultural traits m a d e possible b y that capacity, in other w o r d s the first few m e m e s at least must have furthered the hosts genes. Social learning a m o n g s o m e early hominids, for example, can be imagined to have p r o m o t e d efficient m o d e s of hunting, efficient w a y s of toolmaking and efficient styles of communication, giving social learners an edge over less educable competitors. M e m e s at this early stage can be considered as devices by which g e n e s amplified their fitness ( L u m s d e n and Wilson, 1981). They w e r e then close to the slave-like symbionts of genes, m u c h as mitochondria are today. Slaves though, have a w e l l - k n o w n bent t o w a r d s i n d e p e n d e n c e . The question is w h e t h e r genes can m a n a g e to keep m e m e s u n d e r control past the initial protocultural stage. Symbionts, as explained earlier, are normally subject to the evolutionary process within their hosts and not just w h e n they are transmitted b e t w e e n hosts. The same can be said of memes. Variability of covert and overt b e h a v i o u r d u e to m a n y causes, b u t not least to neural system noise, continuously generates n e w potential m e m e s , or m e m e mutants, within an individual. While still resident in that same individual these m u t a n t s are selected by the same innate processes that make learning generally an adaptive process (Staddon, 1983; G o u l d a n d Marler, 1987). During overt learning, any otherwise neutral events that circumstantially p r e c e d e and predict innately appetitive or aversive events, c o m e to be s o u g h t or a v o i d e d 'through classic conditioning. Similarly, any arbitrary behavioural response which h a p p e n s for some reason to generate or p r o d u c e such

88

The nature of culture

reinforcements is c o r r e s p o n d i n g l y e n h a n c e d or s u p p r e s s e d t h r o u g h instrumental conditioning. During covert learning (insight learning), any event or response identified b y behavioural simulation within the m e m o r y m o d e l of reality as being likely to lead to r e w a r d or p u n i s h m e n t is retained in, or rejected from, the mind. Eventually, such imagined b e h a v i o u r is tested w h e n p u t into practice. Conversely, a n y responses or strategies that are no longer effective in yielding appetitive or avoiding aversive reinforcement extinguish and are finally forgotten. In short, any individual learning (including imagining events, ideating, inventing and creating) is a process b a s e d on variation a n d selection, that is analogous to biological evolution (Pringle, 1951; C h a n g e u x et al., 1984; Staddon, 1983). Emergent m e m e m u t a n t s in that context can be considered as having replicated well within a host organism, in the sense that the c o r r e s p o n d i n g m e m o r y traces have become better consolidated through r e d u n d a n t storage. Unsuccessful m e m e m u t a n t s in the s a m e context are those that cannot establish themselves in the m e m o r y of even one host. Incipient m e m e variants, like symbiotic gene mutants, are thus selected within their hosts, and not only as they spread to n e w hosts. Effectively every potential m e m e u n d e r g o e s a kind of genetically instituted quality control before it has a chance to be p a s s e d to other hosts. The c o m m o n l y held v i e w that cultural evolution is Lamarckian (Medawar, 1976), that it involves the transmission of acquired traits, ignores that fact that the acquisition of those traits is itself the result of a Darwinian intrahost process. The variation and selection principle h o w e v e r also o p e r a t e s as m e m e s are transmitted from individual to individual by social learning. Imperfect transmission is clearly a frequent source of m e m e mutation. Potential hosts on the other h a n d are not completely passive regarding the m e m e s on offer. Host bioevolution can be expected to have ensured that recipient individuals are choosy as to which m e m e variants they pick up. Young songbirds as a rule only imprint on songs similar to those typical of their species. O b v i o u s l y an innate m e c h a n i s m precludes the acceptance of songs that are too aberrant (Catchpole, 1986). A frequent a s s e s s m e n t criterion a m o n g h u m a n seems to be h o w m a n y carriers of a given m e m e offer themselves as models. If many conspecifics exhibit a given cultural trait the likelihood that the m e m e is biologically adaptive is high. If a m e m e was drastically u n a d a p t i v e it w o u l d literally kill off its hosts, so reducing their number. Another sign of biological m e m e quality are obvious signs of fitness exhibited by the bearer of a given trait. If an individual is visibly successful, being, for example the strong alpha male of a group of primates, having access to choice food and m a n y females, then the m e m e s he carries are likely to be fitness-' promoting and worth acquiring (Boyd and Richerson, 1985).

Parasitic memes

89

Even w h e n taken over from other hosts, m e m e s will still h a v e to be consolidated and maintained in the m e m o r y of the recipient. M u c h the same selection mechanisms that operated on the m e m e s generated within an individual, as discussed earlier, will also a p p l y in this situation. There are parallels in s y m b i o n t biology. The gene-instructed i m m u n e system is an impressively sophisticated mechanism designed to select symbiont variants in the interest of host fitness. It is effective in censoring s y m b i o n t varieties, i n d e p e n d e n t l y of w h e t h e r they arise t h r o u g h m u t a t i o n s within an individual or w h e t h e r they enter that individual b y infection. Since genes create the e n v i r o n m e n t on which m e m e s thrive, t h e y s h o u l d in principle be able to select m e m e s such that only those contributing to their biological fitness can survive and proliferate. Culture at this stage of the game is only one more strategy 'invented' by s o m e g e n o m e s to succeed in the harshly competitive g a m e of p h y l o g e n y .

PARASITIC MEMES H o w discerning can gene-instructed brains be a b o u t the m e m e s t h e y are p r e p a r e d to harbour? The c o r r e s p o n d i n g filter m e c h a n i s m for symbionts, the i m m u n e system of vertebrates, definitely falls short of being perfect. C o m m e n s a l and even parasitic organisms often get past its scrutiny and manage to infect some, or even many, individuals. Could at least the occasional c o m m e n s a l m e m e arise and spread in a similar w a y ? Even t h o u g h penalized by the n e e d for a larger brain, an increased ability for social learning, i.e. an a u g m e n t e d capacity for memes, has obviously conferred a biological advantage in some higher animal species. As long as most of the larger n u m b e r of m e m e s thus m a d e possible w e r e a d v a n t a g e o u s to the host, gene selection for indiscriminate reduction of general imitation learning capacities w o u l d be weak. Selection for gene mutants that instruct mechanisms capable of controlling more specifically which m e m e s to accept and which to reject w o u l d arise, h o w e v e r . The preceding section sketched s o m e m e c h a n i s m s that could p e r f o r m this function. But, discrimination b e t w e e n similar m e m e alleles, s o m e of which p r o m o t e the genetic fitness of their hosts and others that do not, can d e m a n d very clever decision mechanisms. Their instruction is likely to require a slow-toevolve cooperation of m a n y genes. If m e m e s w e r e solely cooperative with genes, one w o u l d expect the transmission of the former to be closely c o u p l e d with the transmission of the latter. According to the genetic selfish altruism principle (Hamilton, 1964), the transmission of mutualist m e m e s

90

The nature of culture

s h o u l d occur mainly b e t w e e n genetically related individuals a n d less b e t w e e n unrelated individuals. A m o n g primitive cultures m o s t biologically beneficial m e m e s are i n d e e d t r a n s m i t t e d from parents to children, a n d only a few such m e m e s are p a s s e d on b e t w e e n nonkin (Hewlett a n d Cavalli-Sforza, 1986). Unrelated individuals on the other h a n d are likely to be genetic competitors a n d s h o u l d accordingly be suspected of attempting to pass harmful m e m e s to each other. That m a y be w h y the search for a solicitor, a stockbroker or a physician a m o n g o n e ' s relatives is c o m m o n p l a c e w h e n one n e e d s critical advice. Still, the fact is that even in protocultures such as those of songbirds, m e m e s are being passed a m o n g genetically u n r e l a t e d individuals. M u t a n t m e m e s not contributing to the genetic fitness of their hosts can proliferate if their cultural fitness is high, that is if they are 'catchy', if t h e y can overcome the a b o v e - m e n t i o n e d filters a n d do not appreciably impair their h o s t ' s biological fitness. A few biologically useless but inoffensive cultural traits e m b e d d e d a m o n g m a n y cultural traits p r o m o t i n g gene fitness will not generate a strong genetic selective pressure t o w a r d s m e c h a n i s m s e n s u r i n g their removal. C o m m e n s a l m e m e s seem an almost inevitable d e v e l o p m e n t in a n y a d v a n c e d culture. Even in the case of bird culture there are considerable doubts w h e t h e r all song variants exhibited by a given species are associated with a definite a d v a n t a g e in biological fitness (Barker a n d C u n n i n g h a m , 1985). In h u m a n culture biologically i n n o c u o u s fads or crazes of one kind or a n o t h e r are certainly legion. Pointed rather t h a n r o u n d collar tips, two- rather than three-button jackets seem unlikely to make a n y difference to the survival and the reproduction of wearer, even though generally dressing to keep w a r m certainly does. Interestingly such c o m m e n s a l m e m e s often occur linked to other m e m e s w h o s e function it is to attach p u r p o r t e d biological significance to these. Pointed collars and three-button jackets, for example, were said to be indicative of virility w h e n they were fashionable. O n a more global scale, music, literature, a n d the arts as a whole involve large a n d complex m e m e ensembles that are probably neither beneficial nor harmful to the genes of most of their carriers. They can be seen as c o m m e n s a l s that have colonized a special mental niche, namely the brain structures that more normally control curiosity and exploration, behaviours that contribute m u c h to g e n o m e fitness. Memes, due to the fact that they can m a n i p u l a t e the behaviour of their hosts, are p r e d e s t i n e d to increase their memetic fitness at a cost of some host biological fitness. They have it in their h a n d s , as it were, to put their hosts' b e h a v i o u r to work on their transmission

Parasitic memes

91

rather than that of their hosts' genes, not unlike the rabies virus. M e m e mutations a n a l o g o u s to parasites, that have high cultural fitness at the e x p e n s e of host vigour, s e e m nearly inevitable. It is easy to see, for example, h o w m e m e s inducing drug-taking get past geneinstructed censoring. Addictive drugs h a p p e n to activate the rewardsignalling m e c h a n i s m that is so important for learning, e v e n t h o u g h they are not in fact fitness-promoting, as are the stimuli that normally drive these r e w a r d circuits. In m u c h the same w a y as saccharin fools the alimentary system, so does morphine fool the reinforcement system (Falk and Feingold, 1987). Innate evaluation mechanisms in h u m a n s s e e m undiscerning about the optimal measure of resource seeking and holding efforts. Attempts to get the best out of the e n v i r o n m e n t are certainly biologically a d v a n t a g e o u s to an individual, b u t at s o m e point the returns cease to justify the investment. It is even suspected, for example, that birds occasionally miss mating opportunities on account of exaggerated territorial aggression. A m o n g h u m a n s , greed often inhibits fertility. M a n y a successful parasitic m e m e profits from the q u e s t for capital riches rather than for genetic fitness. Much of the commercial culture that p e r v a d e s the civilized world is a certain c o n s e q u e n c e of this. Celibacy is an obvious parasite m e m e that causes a reduction of host reproduction. It is part of a m e m e complex, a m e m o m e that manipulates the brains of hosts so that it r e d u c e d their sexual activity but increases instead their proselytizing behaviour, much as the rabies virus inhibits the reproductive b e h a v i o u r of its host in favour of infective behaviour. Incidentally, certain organismic parasites go one step further a n d actually castrate their hosts as a m e a n s to increase their o w n fitness (Baudoin, 1975). A m o n g Catholics the celibacy m e m e carried by one set of hosts is compensated by a linked m e m e expressing itself in the d e m a n d that the remainder of the m e m o m e carriers should commit t h e m s e l v e s to relentless reproduction. O n the other hand, competing m e m e s that instruct the use of contraceptives have spread a m o n g Western cultures in recent years, to the extent that relevant populations are numerically decreasing. Contraceptives of course sever the innate link b e t w e e n reproduction and pleasure that normally e n s u r e s fertility. The host's genome should in principle counteradapt against parasitic memes, but the faster evolutionary pace of m e m e s versus genes makes that difficult. Moreover, selection for gene m u t a n t s against infection by specific m e m e s can only b e c o m e effective as these m e m e s spread and are already part of the p o p u l a t i o n ' s cultural heritage. As an analogy, a partial resistance against myxomatosis only began to emerge as a genetic trait a m o n g Australian rabbits after the disease had taken

92

The nature of culture

the character of a p a n d e m i c a n d the rabbits were close to extinction (Fenner and Ratcliffe, 1965). Still, gene mutations that s o m e h o w ensure brains i m m u n e to invasion by parasite m e m e s are at an a d v a n t a g e against those that do not. H o w e v e r , m e m e m u t a t i o n s b y p a s s i n g that resistance are culturally selected for, a n d so there is again a coevolutionary arms-race: hosts evolve i m p r o v e d censoring, m e m e s evolve e n h a n c e d propagation. This all suggests that in an advanced culture parasitic m e m e s should be able to proliferate. G e n e s are unlikely to be able to devise innate defences against each a n d every one of the m y r i a d s of biologically harmful m e m e m u t a n t s that arise in as variegated a culture as the h u m a n one. O n e has even to consider the possibility that parasitic memes, such as those responsible for e n v i r o n m e n t a l pollution, could eradicate their h u m a n hosts, even before the genes of AIDS m a n a g e to do so.

CULTURAL EVOLUTION Cultural evolution is the inevitable spin-off from the imperfect replicative properties of memes. Memes reproduce and mutate as they establish themselves in a given brain, a n d as they transmit themselves to other brains. The survival and the reproductive efficiency of different m e m e s is not identical as t h e y compete for a n d interact with their environmental niche. Some memes spread explosively, others are only mildly successful, while m a n y become extinct. Different m e m e s have differing cultural fitnesses, m u c h as different genes have differing biological fitnesses. In short, the memetic information lodged in the collective m e m o r y of a given cultural ensemble is subject to variation and selection. Memes have to be viewed as i n d e p e n d e n t l y evolving entities w h o s e core habitat h a p p e n s to be the brains of some higher animals a n d w h o s e p h e n o t y p o i c expression is the cultural behaviour of these same animals. In their essentials t h e y are not too different from, for example, influenza viruses that inhabit the naso-oral cavities of vertebrates and express themselves in the sneezing a n d c o u g h i n g behaviour of their hosts (Yamashita et al., 1988). The m u l t i t u d e of species and subspecies p o p u l a t i n g the earth is doubtlessly the most striking product of genetic evolution (Minkhoff, 1983; F u t u y a m a , 1986). Speciation consists of the emergence of assemblies of m u t u a l l y a d j u s t e d genes (genomes) a d a p t e d to survive and reproduce in different ecological niches. Subcultures and cultures can be similarly understood as distinct coadapted assemblies of memes, as populations of m e m o m e s , which thrive in different socioecological

Cultural evolution

93

niches. A n at least t e m p o r a r y isolation b e t w e e n p o o l s of g e n e s facilitates biological speciation. Restriction of m e m e flow for w h a t e v e r reason, b u t often d u e to geographical separation b e t w e e n host populations, is an important factor in cultural speciation. Media a n d mobility are the antithesis of cultural speciation, as t h e y facilitate the transport of m e m e s b e t w e e n previously isolated cultures. The almost universal spreading of the Coca-Cola subculture in the late 1940s, a n d the M a c D o n a l d ' s subculture in the early 1980s, are witness to this. O n the other hand, the t e n d e n c y for like to mate with like, that is assortive mating according to characteristics such as height, eye colour, personality, etc., helps to maintain biological distinctiveness. The t e n d e n c y for individuals of like culture to stick together, illustrated by both the isolation of immigrant c o m m u n i t i e s a n d the insulation of social classes, in turn aids the preservation of cultural specificities. W h e n only a few individuals are the f o u n d e r s of a large population then the latter's genetic composition reflects its restricted ancestry. The analogue of this f o u n d e r effect that favours the emergence of n e w species on islands also effects cultural evolution. It is k n o w n , for example, that only a few chaffinches colonized the C h a t h a m Islands in the South Pacific in about 1900. The present population of this bird, s o m e 35 generations hence, still has an aberrant and r e d u c e d song repertoire, a dialect that differs from that of the p a r e n t p o p u l a t i o n living in N e w Zealand. No d o u b t this reflects the few a n d individaul song styles that the f o u n d e r s b r o u g h t with t h e m and p a s s e d on to their d e s c e n d a n t s (Baker and Jenkins, 1987). Competition is a very salient characteristic of biological evolution. The replicative and instructive activities of genes are d e p e n d e n t on ~environmental resources. Finite resources limit reproduction and their partitioning leads to various forms of competition b e t w e e n genomes. In organisms capable of behaving, competitiveness frequently surfaces in the guise of agonistic behaviour. Aggression for food and space, strife about social rank and contests for sexual partners are examples. M e m e s also compete for limited resources, primarily for synaptic space in hosts, but also for the means that they need to reproduce themselves (principally a share of the hosts' behaviour). It is not surprising therefore that m e m e s should also instruct their hosts to behave competitively, even agonistically on their behalf. A m o n g h u m a n s at any rate, culturally driven aggressive behaviour is sadly often in evidence, even in its most extreme forms. Brawls a m o n g soccer fans, m u r d e r a m o n g political partisans, wars b e t w e e n religious sects, are events that challenge again and again our naive belief in h u m a n morality and rationality. Biological evolution, h o w e v e r , also yields cooperative behaviour. Each m e m b e r in a bird flock, for instance, benefits in fitness from the

94

The nature of culture

fact that the antipredator vigilance is e n h a n c e d b y socializing: m a n y eyes see m o r e than t w o (Tinbergen, 1953). Culturally d e t e r m i n e d b e h a v i o u r of this kind is extremely w i d e s p r e a d , at least a m o n g humans. Religious sects, learned societies, political parties, etc., clearly arise b e c a u s e the m e m e s c o n c e r n e d are more effective jointly than singly in s p r e a d i n g themselves. The simple fact that b l o o d relatives share varying p r o p o r t i o n s of g e n e s generates selective p r e s s u r e for the e m e r g e n c e of an accordingly g r a d e d altruistic disposition a m o n g t h e m (Hamilton, 1964). Analogously, individuals can share many, f e w or no m e m e s , yielding a gradation of memetic kinships. In a d v a n c e d cultures with institutions such as schools and universities, large n u m b e r s of m e m e s are transmitted a m o n g unrelated persons. Altruistic b e h a v i o u r of a m a r k e d l y parental quality b y professors t o w a r d s their 'best' pupils (i.e. those that have a d o p t e d m a n y of their memes) is not u n c o m m o n . Culturally b a s e d helping b e h a v i o u r a m o n g genetically unrelated people that have some beliefs or traditions in c o m m o n is w i d e s p r e a d : Muslims help Muslims, f r e e m a s o n s aid freemasons, fraternity m e m b e r s assist fraternity members, etc. In fact, cultural altruism m a y often simply reinforce or formalize the other biologically viable form of altruism, n a m e l y reciprocal altruism that, a m o n g animals at least relies on only a rather indefinite fellowship (Trivers, 1985). Competition b e t w e e n biological kin g r o u p s can, h o w e v e r , also enhance strife. Capuchin monkey bands c o m p o s e d mainly of relations, for example, engage in quite warlike aggression against other b a n d s about trees in fruit or stray females (Delius, unpublished observations). To an even greater extent, the same applies to cultural kin groups. Indeed, all too frequently Protestants and Catholics, Sikhs and H i n d u s and m a n y other such g r o u p s choose to kill each other. M e m e selfishness m a y on occasions even override gene altruism. Differing political allegiances for instance can make mortal foes of e v e n close blood relatives, as d o c u m e n t e d by several tragic Spanish Civil War episodes. Every culture seems to contain items that are in some w a y extravagant, involving effort, e x p e n s e or inconvenience that appears disproportionate relative to the pay-off, return or advantage the items provide. Megalithic stone circles, pyramids, gothic cathedrals, tulipomania, operatic performances, fanciful fashions are some examples. Can these be c o m p a r e d to biological extravaganzas such as elk antlers, bird of paradise plumage, manakin dances or orchid flowers? In the biological context it is coevolution that most often brings about extraordinary traits. W h e n e v e r the evolution of t w o or more kinds of organisms is closely i n t e r d e p e n d e n t , in the sense that each kind is a selection agency affecting the evolution of the other, then

Cultural evolution

95

there is scope for unpredictable, sometimes spectacular d e v e l o p m e n t s (Futayama a n d Slatkin, 1983). Males and females of one species are often involved in such r u n a w a y games t h r o u g h sexual selection. Within each sex there is competition for the best sexual partners. Females, w h o invest heavily during reproduction, can gain m u c h b y choosing males with characteristics that p r o m i s e offspring of quality. This generates selection for males that have such characteristics, but also leads to breeding females having ever stronger preferences. The e n s u i n g feedback spiral can give rise to unusual features such as the peacock's tail or the b o w e r b i r d ' s b o w e r (Borgia, 1986). Mutualistic m e m e s that are like extensions of g e n e s are b o u n d to get caught u p in this sort of game. The w h o l e birdsong culture is strongly s u s p e c t e d to be a memetic offshoot of g e n e - b a s e d sexual selection (Catchpole, 1987). A m o n g humans, sex-differentiated dress fashions have p r o b a b l y originated in the s a m e way. M e m e reproduction itself at first sight s e e m s to be of an asexual kind, much as the simple b u d d i n g or cloning typical of such organisms as virus and bacteria (Jackson et al., 1986). According to detailed questionnaire investigations by Cavalli-Sforza et al. (1982) on the cultural traits of American college students, the m e m e occasioning art m u s e u m visits for instance, appears to derive solely from the m e m e b o r n e by just one other model p e r s o n (father). H o w e v e r , the p r o p a g a t i o n of the m e m e motivating churchgoing a m o n g this population a p p e a r s to require the fusion of appropriate m e m e s carried by t w o p e r s o n s (the parents). O t h e r memes, for instance that eliciting jogging, usually descends from several m e m e s born by friends, celebrities, etc., but not the parents. It was argued earlier that host g e n o m e s m a y in fact tend to bias memetic reproduction t o w a r d s a multifusional m o d e involving several source m e m e s ('do w h a t e v e r y b o d y does'). It is uncertain, h o w e v e r , w h e t h e r this primitive isogamic 'sexuality' of m e m e s can s u p p o r t anything like cultural sexual selection. Cultural trait luxuriation is m o r e likely to be p r o d u c e d b y the same kind of coevolutionary tangles effective in complex biological communities which occupy elaborate niches such as the h u m i d tropics. There the survival and reproduction chances of a n y organism are mainly d e t e r m i n e d by the ecological context created b y the other organisms, rather than by the physical conditions of the habitat. The intricate a n d d y n a m i c w e b of organismal interactions characterizing such communities has led to the evolution of innumerable freaks, such as flowers that look like bees, caterpillars that look like snakes, m o t h s that look like hummingbirds, butterflies that look like other butterflies, and so forth. Analogously, h o w well a m e m e succeeds d e p e n d s largely on the cultural context in which it finds itself. For example, once a set

96

The nature of culture

of Muslim or Catholic m e m e s has established itself in a brain, it generates a strong bias for the acceptance of further m e m e s of Muslim or Catholic type, but also for the rejection of a n y B u d d h i s t or H i n d u m e m e s . A r u n a w a y process leading to exaggeration a n d fanaticism b e c o m e s a strong possibility in such a context. From there to p y r a m i d and cathedral building m a y be just a step further. M o r e generally, the selection of m e m e s b y m e m e s m u s t d o u b t l e s s l y be a major factor in cultural evolution. The arbitrary d e v e l o p m e n t s that such an inherently unstable a r r a n g e m e n t can p r o d u c e are intuitively boundless. If m e m e s select m e m e s , can m e m e s also select genes? In certain circumstances they u n d o u b t e d l y do. Different socially learned songs, for example, definitely p r o m o t e a n d sustain the genetical differences b e t w e e n several sympatric bird species (Thielcke, 1973). That is of course precisely what Tinbergen and Lorenz h a d a s s u m e d during that remarkable 1959 conversation mentioned at the beginning of this essay. Given that culturally transmitted song dialects also influence intraspecific mating preferences of songbirds, they are also b o u n d to have subtle effects on their population genetics, even if the effects are difficult to pinpiont (Barker and C u n n i n g h a m , 1985). During the Ravenglass discussions Niko Tinbergen often considered w h e t h e r cultural processes such as language, birth control or m o d e m medicine, were not importantly affecting the course of h u m a n biological evolution. A few years later he s e e m e d to be certain about it. His w o r r y was then that cultural evolution in several respects w a s outstripping biological evolution at a d a n g e r o u s l y accelerating pace (Tinbergen, 1977). H e wrote: 'It is an illusion to believe . . . that cultural evolution (entails) unmitigated progress'. The overall course of cultural evolution, he concluded, n e e d e d a rational and urgent correction. 'Time is r u n n i n g out', Niko w a r n e d us, a n d that is no less true t o d a y than it w a s then.

ACKNOWLEDGEMENTS While preparing this chapter the a u t h o r ' s research w a s s u p p o r t e d by the D e u t s c h e Forschungsgemeinschaft. J. Delius, J. E m m e r t o n , M. D a w k i n s and R. D a w k i n s are t h a n k e d for critical c o m m e n t s and stylistic i m p r o v e m e n t s . J. Delius also p r o v i d e d the Butler quote. M. S i e m a n n and A. N i e m u t h assisted with patient and expert manuscript preparation. The chapter is an extensively r e w o r k e d version of an earlier and longer text (Delius, 1989).

References

97

REFERENCES Alderks, C.E. (1986) Observational learning in the pigeon: effects of model's rate of response and percentage of reinforcement. Animal Learning Behaviour, 14, 331-35. Anderson, R.M. and May, R.M. (eds) (1982) Population biology of infectious diseases, Springer, Berlin. Baker, A.J. and Jenkins, P.F. (1987) Founder effect and cultural evolution of songs in an isolated population of chaffinches, FringiUa coelebs, in the Chatham Islands. Animal Behaviour, 35, 1793-1803. Bajema, C.J. (1972) Transmission of information about the environment in the h u m a n species: a cybernetic view of genetic and cultural evolution. Social Biology, 19, 224-26. Ball, I.A. (1984) Memes as replicators. Ethology and Sociobiology, 5, 145-61. Barker, M.C. and Cunningham, M.A. (1985) The biology of bird song dialects. Behavioural and Brain Sciences, 8, 85-133. Baudoin, M. (1975) Host castration as a parasitic strategy. Evolution, 29, 335-52. Biederman, G.B., Robertson, H.A. and Vaughan, M. (1986) Observational learning of two visual discriminations by pigeons: a within-subject design. Journal for the Experimental Analysis of Behaviour, 46, 45-9. Bonner, J.T. (1980) The evolution of culture in animals, Princeton University Press, Princeton. Borgia, G. (1986) Sexual selection in bowerbirds. ScientificAmerican, 256, 70-79. Boyd, R. and Richerson, P.J.V. (1985) Culture and the evolutionary process, Chicago University Press, Chicago. Campbell, D.T. (1969) Variation and selective retention in sociocultural evolution. General Systematics Yearbook, 14, 69-85. Cann, R.L., Stoneking, M. and Wilson, A.C. (1987) Mitochondrial DNA and human evolution. Nature, 325, 31-36. Catania, C. (1985) Rule governed behaviour and the origins of language, in Behaviour analysis and contemporary psychology, (eds C.F. Lowe, M. Richelle, D.E. Blackman and C.M. Bradshaw), Erlbaum, London, pp. 135-156. Catchpole, C.K. (1986). The biology and evolution of bird songs. Perspectives in Biology and Medicine, 30, 47-62. Catchpole, C.K. (1987) Bird song, sexual selection and female choice. Trends in Ecology and Evolution, 2, 94-97. Cavalli-Sforza, L.L. and Feldman, M.W. (1981) Cultural transmission and evolution, a quantitative approach, Princeton University Press, Princeton. Cavalli-Sforza, L.L., Feldman, M.W., Chen, K.H. and Dornbusch, S.M. (1982) Theory and observation in cultural transmission. Science 218, 19-27. Chesler, P. (1969) Maternal influence in learning by observation in kittens. Science 166, 901-903. Changeaux, J.-P., Heideman, T. and Patte, P. 1984. Learning by selection, in The biology of learning (eds P. Marler and H.S. Terrace), Springer, Berlin, pp. 115-133. Christie, A.B. (1981) Rabies. Journal of Infection, 3, 201-218. Curio, E., Ernst, E. and Vieth, W. (1978) Cultural transmission of e n e m y recognition: one function of mobbing. Science, 202, 899-901. Davies, B.D., Dulbecco, R., Eisen, H.N. and Ginsberg, H.S. (eds) (1980) Microbiology, Harper and Row, Philadelphia. Dawkins, R. (1976) The selfish gene. Oxford University Press, Oxford

98

The nature of culture

Delius, J.D. (1989) Of mind memes and brain bugs, a natural history of culture, in The nature of culture, (ed W.A. Koch), Brockmeyer, Bochum, pp. 26-79 Delius, J.D. (1990) Sapient sauropsids and hollering hominids, in Geneses of language, (ed W. Koch). Brockmeyer, Bochum, pp. 1-29. Devoogd, T.J., Nixdorf, B. and Nottebohm, F. (1985) Synaptogenesis and changes in synaptic morphology related to acquisition of a new behaviour. Brain Research, 329, 304-308. Dudai, Y. (1989)The neurobiology of memory: concepts, findings, trends. Oxford University Press, Oxford. Falk, J.L. and Feingold, D.A. (1987) Environmental and cultural factors in the behavioral action of drugs, in Psychopharmacology: the third generation of progress, (ed H.Y. Meltzer), Raven Press, New York, pp. 1503-1509. Fenner, F. and Ratcliffe, F.N. (1965)Myxomatosis, Cambridge University Press, Cambridge. Futuyma, D.J. (1986) Evolutionary biology, 2nd edn, Sinauer, Sunderland, Mass. Futuyma, D.J. and Slatkin, M. (1983) Coevolution, Sinauer, Sunderland, Mass. Ewer, R.F. (1969) The 'instinct to teach'. Nature, 222, 698. Gould, J.L. and Marler, P.(1987) Learning by instinct. Scientific American, 256, 62-73. Hamilton, W.D. (1964) The evolution of social behavior. Journal of Theoretical Biology, 7, 1-52. Harris, M. (1987) Cultural anthropology, Harper and Row, New York. Hewlett, B.S. and Cavalli-Sforza, L.L. (1986) Cultural transmission among Aka pygmies. American Anthropologist, 88, 922-34. Hogan, D.E. (1986) Observational learning of a conditional hue discrimination in pigeons. Learning and Motivation, 17, 40-58. Hohorst, W. (1981) Parasitologie, in Biologie, (eds D. Starck, K. Fiedler, P. Harth and J. Richter), Verlag Chemie, Weinheim, S. 765-808. Horn, G. (1986) Imprinting, learning, and memory. Behavioral neuroscience, 100, 825-32. Jackson, J.B.C., Buss, L.W. and Cook, R.E. (eds) (1986) Population biology and evolution of clonal organisms, Yale University Press, New Haven. Klopfer, P.H. and Hailman, J.P. (1965) Habitat selection in birds. Advances in the Study of Behavior, 1, 279-303. Kohonen, T. (1984) Self organization and associative memory, Springer, Berlin. Kroodsma, D.E. and Miller, E.H. (eds) (1982) Acoustic communication in birds, Academic Press, New York. Lefebvre, L. (1986) Cultural diffusion of a novel food-finding behaviour in urban pigeons: an experimental field test. Ethology, 71, 295-304. Lumsden, C.J. and Wilson, E.O. (1981) Genes, mind and culture, the coevolutionary process, Havard University Press, Cambridge, Mass. Margulis, L. (1981) Symbiosis in cell evolution, Freeman, San Fransisco. Medawar, P.B. (1976) Does ethology throw any light on h u m a n behaviour? in Growing points in ethology, (eds P.P.G. Bateson and R.A. Hinde), Cambridge University Press, Cambridge, pp. 497-506. Meire, P.M. and Ervynick, A. (1986) Are oystercatchers (Haemotopus ostralegus) selecting the most profitable mussels (Mytilus edulis)? Animal Behavior, 34, 1427-35.

References

99

Minkhoff, E.C. (1983) Evolutionary biology, Addison Wesley, Reading, Mass. Moore, J. (1984) Parasites that change the behaviour of their host. Scientific American, 250, 82-89. Morris, R.G.M., Kandel, E.R. and Squire, L.R. (1988) Learning and memory. Trends in Neuroscience, 11, 125-79. Murton, R.K., Coombs, C.F.B. and Thearle, R.J.P. (1972) Ecological studies of the feral pigeon. Flock behaviour and social organization. Journal of Applied Ecology, 9, 875-89. Nishida, T. (1987) Local traditions and cultural transmission, in Primate societies (eds B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham, and T.T. Struhsaker), Chicago University Press, Chicago, pp. 462-474. Norton-Griffiths, M. (1967) Some ecological aspects of feeding behaviour of the oystercatcher Haematopus ostralegus on the edible mussel Mytilus edulis. Ibis, 109, 412-24. Palm, G. (1982)Associative memory. Springer, Berlin. Pringle, J.W.S. (1951) On the parallel between learning and evolution. Behaviour, 3, 174-215. Rummelhardt D.E. and McClelland, J.L. (1986) Parallel distributed processing. Exploration in the microstructure of cognition. MIT Press, Cambridge, Mass. Schmidt-Koenig, K. (1965) Current problems in bird orientation. Advances in the Study of Behavior, 1, 217-78. Smith, D.C. and Douglas, A.E. (1987) The biology of symbiosis, Arnold, London. Staddon, J.E.R. (1983) Adaptive behaviour and learning, Cambridge University Press, Cambridge. Subowski, M.D. (1989) Recognition in ethology. Perspectives in Ethology, 8, 137-71. Thielke, G. (1973) Die Wirkung erlernter Signale auf die Artbildung, Universit/itsverlag, Konstanz. Tinbergen, N. (1953) Social behaviour in animals, Methuen, London. Tinbergen, N. (1976) Ethology in a changing world, in Growing Points in Ethology, (eds P.P.G. Bateson and R.A. Hinde), Cambridge University Press, Cambridge, pp. 507-27. Tinbergen, N. (1977) Time is running out, unpublished manuscript. Trivers, R. (1985) Social evolution, Cummings, Menlo Park, CA. Wallh/iusser, E. and Scheich, H. (1987) Auditory imprinting leads to differential 2-deoxyglucose uptake and dendritic spine loss in the chick rostral forebrain. Developmental Brain Research, 31, 29-44. Yamashita, M., Krystal, M., Fitch, W.M. and Palese P. (1988) Influenza B virus evolution: co-circulating lineages and comparison of evolutionary patter with those of influenza A and C viruses. Virology, 163, 112-22. Zentall, T.R. and Galef, B.G. Jr (eds) (1988) Social learning: psychological and biological perspectives. Erlbaum, Hillsdale.

--7 Niko Tinbergen, comparative studies and evolution MICHAEL H. ROBINSON

INTRODUCTION All sciences have an o n t o g e n y , a n d ethology is no exception. W h e n I joined the Animal Behaviour Group in 1963, Niko Tinbergen was talking about 'a science as y o u n g as ours' (Tinbergen, 1963). At that time I think it is fair to say that British ethology was in its adolescent phase. It h a d certainly passed youth, which, like senescence, is characterized by innocence. We were then full of adolescent passion and idealism, but perhaps lacking some degree of judgement and adult cynicism. We believed in an attainable state of revelation about the mysteries of behaviour, a n d that somehow we were standard-bearers. Much of the language of those days centred on the function a n d evolution of behaviour and in fact, Niko's ~ i m s a n d M e t h o d s in Ethology' was a kind of state of the Union docum e n t that assessed progress, problems, a n d in some ways redefined the mission of Oxford ethology. It contained a reiteration of the definition of ethology as the biological s t u d y of behaviour and, importantly for my present purpose, p u t evolutionary studies as one of its four key components. If we were truly evolutionary ethologists at that time, then the comparative m e t h o d was one of the m a i n devices in our armoury. I shall herein attempt a s o m e w h a t idiosyncratic review to show w h y I think comparative studies are extraordinarily important.

C O M P A R A T I V E STUDIES IN EVOLUTIONARY BIOLOGY Before m o v i n g on to discuss the comparative m e t h o d in ethology, it is w o r t h stepping back to look at its role in evolutionary biology as

Comparative studies in evolutionary biology

101

a whole. (This is not the place to discuss the p h i l o s o p h y of science or such issues as w h e t h e r biology has a special flavour in terms of methodology. Ernst Mayr (1982, 1988) is a good source of detailed a n d beautifully balanced treatments of the f u n d a m e n t a l p r o b l e m s involved.) It is safe to say that there is absolutely no d o u b t that m a n y evolutionary questions are not susceptible to experimental investigation. Darwin's entire approach to evolution was based on comparative studies. Even n o w the revisionists Eldredge and Gould have developed their p u n c t u a t i o n i s t c r u s a d e entirely f r o m c o m p a r i n g fossil assemblages, and thus from comparative studies (Gould, 1980; G o u l d a n d Eldredge, 1977; Eldredge, 1985a, b, 1989). P u n c t u a t i o n i s m could be derived only from the fossil record. This is obvious because fossil assemblages are our only basis for tracing patterns of change in the history of biological systems, but comparisons within living forms also yield important evolutionary insights. These are w o r t h examining because behaviour, like soft parts, leaves no fossils.

Origins and functions C o m p a r i s o n s b e t w e e n living forms - apart from b e h a v i o u r - can involve m o r p h o l o g y , anatomy, e m b r y o l o g y , physiology, nutrition, biochemistry, genetics, i m m u n o l o g y and so on. C o m p a r i s o n s can be u s e d to elucidate a variety of biological problems. For me, some uses of the comparative method rank far ahead of others, in simple reflection of m y preferences and addictions within the science of biology. First and foremost for me are the interlinked questions of origins a n d functions. These are the issues that Dawkins (1986) raised so elegantly and so eloquently in the 'The Blind W a t c h m a k e r ' . Essentially, w e naturalists burn to k n o w h o w structures of marvellous perfection reach that perfect state. The n u b of the problem is answering Paley's famous question, which he could only a n s w e r by postulating a grand designer of all life. To the evolutionary biologist the challenge is to discover, b y comparison, w h a t forms of intermediate structures could p r e c e d e present specialized ' e n d ' products. Important as is defining the predecessors, determining their p r e s u m p t i v e adaptive function is equally important. Niko (1959a), with characteristic clarity, called the entire two-part process 'the descriptive reconstruction of the course of evolution that has led to the present situation'. Since b e c o m i n g a zoo director, I have learned of a gloriously Kiplingesque example of evolutionary fine-tuning. It concerns the hairs on the tail of the p y g m y h i p p o p o t a m u s . These are aborescent, the only mammalian hairs to branch, and their function involves territorial

102

Niko Tinbergen, comparative studies and evolution

marking (Kranz, 1982). H i p p o s mark their territories with faeces which they scatter by whizzing their tails a r o u n d while defaecating. Arborescent hairs fling faeces more efficiently than straight ones. H o w could such hairs evolve? W h a t a c o n f o u n d i n g question. If w e are to dismiss grand design, we m u s t recognize that there are t w o questions involved in the a n s w e r to Paley: w h a t are the steps in the process, and w h a t w a s the function of the structures as t h e y evolved? Comparative studies are the only source of answers.

Relationships Of course, the most obvious use of comparative studies for the great majority of biologists, i.e. those not o b s e s s e d b y the origin of intricate mechanisms/devices/structures/characters, is in elucidating relationships. Building grand phylogenies admittedly is fun; building accounts of relationships at the smaller scale of genera, families, orders and so on, can be immensely satisfying. W h e t h e r w e do it b y external characters - the p r e p o n d e r a n t m e t h o d , because eyes a n d microscopeaided eyes w e r e the only technologies available to Linnaeus and most of his d e s c e n d a n t s - or w h e t h e r w e n o w plug in chemical technologies, comparisons are p a r a m o u n t . They can be statistically based, intuitive, or both, b u t most frequently they are built on evolutionary interpretations. This is not always true. There are taxonomists w h o s t u d y patterns of resemblance in their o w n right, without a s s u m i n g any evolutionary implications. The term that Dawkins (Dawkins, 1986) uses for this trend, ' p u r e resemblance measurers' should, I hope, stick.

Convergences, parallelisms, homologies and analogies Comparative studies are also the basis of the study of the convergences and parallelisms which enrich evolutionary theory. H o m o l o g i e s and analogies also emerge from this field and can provide a high degree of intellectual excitement. A simple-to-describe example concerns the evolution of the camera-like eye convergently in the c e p h a l o p o d s and the vertebrates. As I watch our nautiloids s w i m clumsily a r o u n d the National Z o o ' s Invertebrate Exhibit I realize that their very conservative design, dating back to the Mesozoic, still works. They also s h o w us h o w an ectodermal pit could b e c o m e an eye. O n e could a p p l y the same process to convergent eyes in polyphyletic arthropods. For me as an airplane enthusiast, the 'discovery' of lift in the ' w i n g s ' of rays

Comparative studies in ethology

103

a n d skates, a n d its utilization for flight in insects, reptiles, birds a n d mammals raises the question of whether the Wright brothers (and other claimants) w o u l d have t h o u g h t flight possible w i t h o u t the example of birds. W o u l d they have d e v e l o p e d the physics quicker if t h e y ' d studied the flight of n o n - b u o y a n t fishes, or w o u l d t h e y have arrived at the helicopter before the airplane if t h e y h a d s t u d i e d the flight of the dipterocarp fruits?

Evolutionary insights W h e t h e r one believes that biologists p r o c e e d b y induction or by the so-called hypothetico-deductive m e t h o d (or both) there is little d o u b t that, as Niko so often insisted, asking the right questions n e e d s a background of observations. The observations do not need to be o n e ' s own, but a b r o a d k n o w l e d g e of animal biology, derived from comparative studies, can certainly provide the insights necessary for hypothesis formation. It can provide insights into the existence of selection p r e s s u r e s both broad and narrow. In a sense, as Roberta Rubinoff p o i n t e d out to me, s o m e kinds of c o m p a r i s o n enable one to utilize data from the experiments carried out by the effects of stochastic natural processes, geological history, and evolution itself. Darwin's insights, derived from s t u d y i n g the G a l a p o g o s flora and fauna, were in fact derived from the results of a long-term exclusion experiment. The 'chance' geographical separation of the islands from the mainland p r o d u c e d the kind of situation that a p r e s e n t - d a y ornithologist might wish to contrive, one w h e r e he w o u l d be able to seed uninhabited areas with one family of birds, a n d exclude their competitors. Of course he w o u l d want to live long e n o u g h to observe the results. Darwin had the insight to interpret the results of this experiment partly because he had the comparative base acquired by a good and well-travelled naturalist. In his narrative of the Beagle voyage he remarked: 'Reviewing the facts here given, one is astonished at the a m o u n t of creative force, if such an expression m a y be used, displayed here on these small barren islands'. Australia is a great experiment for the marsupials, South America for the edentates, and so on. There are also great 'experiments' that result from closely related species occupying very different habitats.

COMPARATIVE STUDIES IN ETHOLOGY Niko's attitude to comparative studies was itself evolutionary. It is interesting that in the 'Authors N o t e s ' to his first v o l u m e of 'The

104

Niko Tinbergen, comparative studies and evolution

animal in its w o r l d ' (1972) he says 'It w a s K o n r a d Lorenz's relentless prodding which m a d e me turn to comparative studies. Having studied the herring gull in s o m e d e p t h , I naturally t u r n e d (finally convinced b y Lorenz's p a p e r on dabbling ducks) to other gulls'. Of his (1959b) p a p e r on comparative studies in gulls he says, 'it has a d i m e n s i o n hardly f o u n d in m y earlier papers: inter-species comparison. More precisely, w h a t w a s lacking in all those one-species papers w a s a n y serious a t t e m p t to apply the comparative m e t h o d for the p u r p o s e of interpreting diversity a n d similarity as the o u t c o m e of adaptive divergence a n d convergence; as such t h e y s h o w a failure to take in the lessons I could have learned from Whitman, Heinroth, Huxley, V e r w e y and Lorenz' (my italics). This is a very frank evaluation. The fact is that Niko himself never carried out a broad comparative study, but his s t u d e n t s certainly carried that b a n n e r for him. From cichlid fishes, Baerends and Baerends (1950), to c e p h a l o p o d s (Moynihan, 1985) and b e y o n d , the list is long and honourable. M y close association with N i k o ' s pupil Martin M o y n i h a n , during 20 years b a s e d in the tropics, has convinced m e that he is primus inter pares in this field. Most of the later examples that I use are from his work. N o n e of this m e a n s that Niko did not realize the importance of comparative studies in ethology. "The study of instinct' (1951) contains a major section on evolution and s o m e provocative thinking on homologization and comparison. From that point on, regularly in the 1950s and 1960s Niko p r o d u c e d a succession of papers on b e h a v i o u r evolution (1954, 1959a, 1959b, 1960, 1962, 1963, 1964, 1965a, 1965b, H i n d e and Tinbergen, 1958). M a n y of these w e r e concerned with experimental investigations of the survival of behaviour patterns, but s o m e were treatments of the entire field and the role of comparative studies in the reconstruction of evolutionary pathways, in systematics, and in the elucidation of function and causation. Noteworthy are Hinde and Tinbergen (1958) and Tinbergen (1959a). In H i n d e and Tinbergen (ibid) the authors define the limits and p r o b l e m s of the comparative method. They mention 39 comparative studies, then either completed or in progress, spanning spiders, grasshoppers, mantids, flies, wasps, fiddler crabs, cichlid fishes, sticklebacks, three families of finches, buntings and gulls. This m a y have been a fairly c o m p r e h e n s i v e list for the time. Anticipating the future e m p h a s i s of m u c h of the Oxford g r o u p ' s research is an important paragraph: 'A k n o w l e d g e of the probable course of evolution p r o m p t s further enquiry as to w h y evolution has taken that course and not some other. It is thus desirable to k n o w w h e t h e r the changes are adaptive and can have been brought about by selection. This involves a s t u d y of the survival value of the behaviour e l e m e n t s . . . ' . In his 1959 p a p e r 'Behaviour, systematics

Comparative studies in ethology

105

and natural selection' Niko examined the subject critically, giving some i m p o r t a n t recipes for using the comparative m e t h o d . These are well worth rereading, although they m a y n o w be largely s u b s u m e d in more recent treatments of comparative methodology (Ridley, 1983). Distilling this original w i s d o m , a n d other protocols from H i n d e a n d Tinbergen (ibid) we get: 1. 'As in m o r p h o l o g y , successful use of the comparative m e t h o d d e p e n d s on the selection of characters to be c o m p a r e d ' . (H and T) 2. 'It is not desirable to use characters which change rapidly and could have been acquired i n d e p e n d e n t l y in different g r o u p s ' . (H a n d T) 3. ' M a n y of the difficulties involved in the use of behavioural characters can be avoided by a broad approach; the importance of a k n o w l e d g e of the natural history of the animal a n d the causation a n d function of the behaviour c a n n o t be overe m p h a s i z e d ' . (H a n d T) 4. 'In order to translate differences b e t w e e n contemporary forms into changes of time, one step further is required; an interpretation of the direction of change. To do this it is essential as in comparative a n a t o m y to combine data derived from the comparison of species with data about the function of both the original a n d the derived character'. (T) 5. 'The most convincing examples of evolutionary changes of function have been f o u n d in signal function'. (T) 6. The two most fruitful types of approach are (a) the s t u d y of divergent forms derived from c o m m o n stock, a n d (b) that of distantly related convergent forms.' (T) This is a selection that one can evaluate 30 years later. Tinbergen's t r e a t m e n t (1959a) also contains a crucial section on 'Interaction of selection pressures'. This is an idea he was to return to again and again. In essence he argued that behaviours m a y be evolutionary compromises. Thus w h e n one is studying selection pressures, 'one cannot help seeing that selection pressures must often be in conflict with each other. One e n d s up by discovering that each character has not only been i m p r o v e d with regard to its o w n particular function but has u n d e r g o n e indirect effects which . . . are recognized as effects of selection w h e n seen as parts of a s y s t e m . ' At this stage it is w o r t h giving some examples that I have selected principally from m y o w n work a n d studies by m y colleagues at the S m i t h s o n i a n Tropical Research Institute. I m a d e this choice mainly for two reasons, quite apart from the intrinsic content of the studies. First, I am more familiar with this research than with work elsewhere (my ten-year stint as an administrator 1980-1990 h a v i n g isolated me

106

Niko Tinbergen, comparative studies and evolution

from comparative research). Second, I think that t h e y m a k e points about tropical research c o m p a r e d with the state of university-based science. Tropical biology is u n i q u e l y rich in o p p o r t u n i t i e s for comparative studies because there almost certainly are, for m a n y major groups of animals, more related species p r e s e n t in any tropical area than a n y w h e r e else on earth. This is true of both rainforest faunas and those of coral reefs. This makes it easier to study very large speciessamples in relatively small areas. In this respect, e v e n zoos do not come near to the species richness of, say, Barro Colorado Island. The other factor relates to ethos and style. Research institutes can, if properly led, avoid the almost inevitable 'Rat-race effect' f o u n d at universities. In m o d e r n academia the probability of c o m m i t m e n t to broad lateral studies, u n d e r t a k e n over long periods, is frequently low. This kind of c o m m i t m e n t is essential for most comparative studies. (The universities most particularly affected b y rat-racery are those w h e r e conditions of tenure involve a s s e s s e m e n t s of p a p e r productivity.) There is yet another reason for choosing s o m e of these studies to exemplify the comparative approach: m a n y were p u b l i s h e d in journals not necessarily read a s s i d u o u s l y by ethologists. Criticisms of the c o n d u c t and results of comparative studies will be raised later.

DESCRIPTIVE RECONSTRUCTIONS B E H A V I O U R EVOLUTION

OF THE COURSE OF

Camouflage, mimicry and defensive adaptations W h e n I joined the Behaviour G r o u p , David Blest had just c o m p l e t e d his s t u d y of the function of eye-spot patterns in Lepidoptera (1957a). This led him to s o m e b r o a d scale comparative studies, and the consequent evolutionary insights (1957b; 1963a; 1963b). Investigations of defensive systems in insects were not entirely a n e w v e n t u r e for Niko's students. De Ruiter (1952; 1955) had previously studied countershading and stick-mimicry in caterpillars. Oxford in the days of H o p e Professor E.B. Poulton h a d a long tradition (papers from 1884-1934!) of camouflage studies and Niko had w o r k e d with Bernard Kettlewell in experiments on industrial melanism. Later there w a s to be an extensive investigation of camouflage in the eggs of black-headed gulls (Tinbergen et al., 1962). I started a s t u d y of the adaptive function of rocking m o v e m e n t s in stick- and leaf-mimicking insects which w a s to lead me into a lifelong interest in p r e d a t o r - p r e y interactions. This thesis topic, with great serendipity, led me to Panama, w h e r e the diversity of insects is overwhelming. This was long before the studies

Descriptive reconstructions of the course of behaviour evolution

107

of Erwin (1982) s u g g e s t e d that there w e r e p e r h a p s 30 million species of insects in the world, most of t h e m in the rainforests, rather than the 1.5 million previously estimated. In Panama, and later in Colombia, Venezuela, Sri Lanka a n d P a p u a N e w G u i n e a I s t u d i e d the defensive adaptations of p h a s m i d s , mantids, tettigoniids, acridiids, and, eventually, spiders. In these g r o u p s w a s a w h o l e range of, visual defences, ranging from relatively simple camouflage to the most complex a n d detailed forms of stick, leaf and faeces mimicry. As I accumulated examples of the complex p o s t u r e s a s s u m e d by both eucryptic and mimetic insects (Robinson, 1964; 1968a, b, c, d; 1969a, b,; 1970a, b; 1973; 1977; 1978; 1979; 1981; 1985; Robinson and Pratt, 1976), the comparisons across g r o u p s a n d b e t w e e n groups, together with the mine of information contained in the comparative studies of mantids b y Crane (1952) for Venezuela, and E d m u n d s (1972, 1976) for West Africa, eventually clicked together. I w a s led to visualize a scheme that a c c o u n t e d for the evolution of stick mimicry and, coincidentally, raised hypotheses about the prey-recognition processes of sophisticated visually hunting predators (1969a; 1970b; 1985). If one wishes to reconstruct possible steps in the evolution of specializations, one needs to discover a good range of probable intermediates and also to find a d e q u a t e inferences or evidence a b o u t the selection p r e s s u r e s involved in the changes. From m y o w n w o r k and a w i d e variety of other studies I eventually had both of these essential elements. As my experience of diverse tropical faunas has expanded, convergences b e t w e e n unrelated groups, and b e t w e e n the same g r o u p s in widely separated geographic regions s e e m n o w to fit within the original scheme and pile more and more examples into it (Figures 7.1 and 7.2). The insight that p r o v e d to be a turning point came from the discovery of a remarkable stick insect in Panama. This w a s Pterinoxylus spinulosus, which has an u n u s u a l l y specialized resting p o s t u r e (Robinson, 1968c), s h o w n in detail in Figure 7.3. Not only are the first pair of legs held in line with the b o d y axis and apposed, as in all sticklike phasmids, but the second and third pairs of legs are held in complex postures, folded on themselves in highly specialized ways. The immediate inference is that these are leg-concealing postures. The reciprocal conclusion is that such devices imply that predators m a y attend to such giveaway features of insect prey as the possession of legs. Once one assumes that legs m a y be a disadvantage to concealment, disguise and deception, then each n e w species of camouflaged or mimetic animal one finds b e c o m e s a source of anticipation. A d d e d to the excitement of collection and discovery (perhaps an atavism from hunting-gathering) is a n e w curiosity b a s e d on the question ' w h a t will it do with its legs?' Despite the fact that fewer than 5% of the

C~

° O

O.

1i

o'O.~

_

.~

"~ ~

~

0'..~

~,.o

~

0

u~

0

~

~

~

o

~

,-,>

0

r~

,.,,

~ ..~ ,-'..~ ~

,.0

-~

~

~

..~

!::;

~a

~

,~

~'.-~

~

,~,

~

~ •~

.~-,

~

•

.

0

~ ' "C

~

~,~, ~

~

~

v

~b~"

,-.~

~"~

~ ~

I::~,-~_

.

0,.~ ,"

•

~

"~ ~

~ ~

~

~,,~

;'~ ,'r"l ~ ~

"-~

~

I~

~

C

v) (1; ~-

~"~

C ~

t~

t'~

~

N

"~

.~

m

~

~

~

(~

(~

¢~

'

~

,,,

r,

~

~

~

~ ~ .~ - ~

C. ~

~

~ ~

u~

V) a~

~ ~ ~

0

~

~'uO

~

u

~

..~

__

~

~

. 0

~

C

I:::

~

--

C ~D ~'

~

0

.~

.

~

~).~ ,-~

~

~

~ ~ . ~ ~--~

.~

0

.o

.,

)~ ~ ~

~

;~.a

0

_

~

..,

.4-,

0

~

r~

~

~

I~,.~

o

~

.

~

~~ . ~ ' ~

0

',-'

~

,

~0

•

.

~0 ..,~ , . ~

0 ~ ~C ~~

~

.~ ,~ ~

~

~

0-'-' ..~ ~

,z:~ ._., ,_~

~

o

0

~

~

~

- __

..-. U

X

~'~

X

:;~

~'.~

~ _ ~.~

~

~',.,., -~

~ - - . ~ =1 ~~

c~ c O

~

"~

0

,-~

--" ~,.)

"~ ~ ~

-'~. (1; ,,~

~ .,-,

~ ~

L ~(1~ ,--~-

~ 0

,4..,

~

(~

~

~

~,

~, . ~ . ,

0

~

I=

~

.,.C; ,~

~r~

~ ~

~"~'-~

C

,-- " ~

~.-

.= ~ ~ 0

~ ~=_

~ .~ "~

~.

,.~

~

.~

-,..,.,

--

~

~

~.C

~

,-'--

~

.-

. . . . .

~

~

"~

c~

~,.-,

110

Niko Tinbergen, comparative studies and evolution

Figure 7.2 Photographs of the dead-leaf mantid Acanthops falcata and the prostrateresting cryptic tettigoniid Acanthodis curvidens, shown in Figure 7.1 stages MIII and OII respectively. Note the postures of legs I.

Descriptive reconstructions of the course of behaviour evolution

111

3

Figure 7.3 The phasmid Pterinoxylus spinulosus referred to in the text (page 107). This insect assumes a posture that effectively conceals all six legs in positions consistent with the overall stick mimicry. living insects I collected could be n a m e d , I w a s never d i s a p p o i n t e d . Their behaviours were a revelation: one w a s constantly a m a z e d b y the variety of concealing 'inventions" involved. Instances of these have accumulated with time (Robinson, 1970b, 1985). Clues come from other people's photographs, where the significance of the postures they have recorded h a d not been recognized, at least overtly. For instance, quite b y chance while surveying the recent b e h a v i o u r literature for this paper, I came u p o n a d r a w i n g (Cloarec, 1988) of the mimetic p o s t u r e of the water stick-insect Ranatra sp., a hemipteran, far i n d e e d from the p h a s m i d s . This p o s t u r e is strikingly similar to that of a p r a y i n g mantis from P a n a m a that I described over 20 years ago (Robinson, 1969b). O n e of the most satisfying things for me as a naturalist, despite the absence of taxonomists capable of identifying the beasts, w a s to find three species of elusive leaf insect (Phyllidae) in P a p u a N e w Guinea, each of which folded its legs to merge totally with its b o d y . Things illustrated in classic b o o k s are a glory to see in the wild. The use of the comparative m e t h o d to identify widespread selection p r e s s u r e s for concealing characteristic insect parts eventually led to the final satisfaction of being able to p r o p o s e a reconstruction of h o w stick mimicry could have b e e n evolved. This was m a d e easier b y the fact that both the mantids and the p h a s m i d s (two widely mimetic g r o u p s of insects) h a d p r e s e n t - d a y forms that s e e m e d likely to be

112

Niko Tinbergen, comparative studies and evolution

similar to probable stages in the evolutionary sequence leading from camouflage to stick or leaf mimicry. My reconstruction started from insights gained from studying camouflaged insects resting in twigs and leaves. These align themselves along the twig or leaf vein (in Papua New Guinea, along the concave upper surfaces of Pandannis sp. leaves). In their cryptic postures they protract their anterior legs in line with the long axis, fold their intermediate legs against the b o d y o r substrate, and position the posterior legs behind the body in line with its axis (Robinson, 1969b). This posture effectively conceals the legs, antennae and head, and reduces the profile of the insect. It also, in effect, increases the insect's length by adding the length of legs I and III to the body length. Of course, if the camouflage works, none of this extension is apparent. However, the postures can be regarded as a step towards potential mimicry. There are several phasmids that rest in this position. They are simply cryptic, background-matching species (Robinson, 1969b). If the insect does not choose to rest on a background appropriate to its body colour it could be at risk, or at least provoke further scrutiny. Any cryptic insect resting on an elongate structure could, from this posture, evolve toward further profile reduction (concealment) as a result of further elongation (Figures 7.1, 7.2). Interestingly enough there are two other solutions to the leg concealment problem. Both are 'dead ends' that cannot lead directly to stick mimicry. One leg-concealing variant is to tuck the hind legs u n d e r wing covers. This solution is accomplished in two different ways, depending on wing posture, seen in two genera of New Guinea katydids (Robinson, 1973). Yet another variant is to fold legs II and III against the body, a device found in New World tettigoniids of the family Pseudophyllidae (Robinson, 1969a). The possible steps from an elongate, prone resting posture are shown in Figures 7.1 and 7.2. They are represented in the mimetic postures of existing species. To reiterate, this hypothetical pathway involves the assumption that legs and other characteristic animal structures are concealed because they are giveaway clues to the detection of otherwise concealed or disguised animals. The primary reason for assuming this is that there is an amazing range of behaviours and structures that seem to conceal legs and other structures. These adaptations are found in spiders of at least two families (Robinson, 1985, and unpublished data), lizards and even birds. Some of these are shown as adjuncts to Figure 7.1 in Figure 7.2. Despite the range and complexity of such presumptive leg concealment, the argument may seem to be circular: legs are concealed therefore legs are preydetection clues. I believe that what this really constitutes is not circularity but the inductive base for a testable hypothesis. We can

Descriptive reconstructions of the course of behaviour evolution

113

simply ask: do visually h u n t i n g predators actually use legs to detect prey? I have some very suggestive results from experiments on this problem (Robinson, 1970b). A m o n g these results is the fact that sticks with cricket legs glued onto them were attacked and bitten by tamarins; similar sticks without legs were ignored. A detailed s t u d y of arthropod antipredator adaptations leaves one with an indelible picture of a complex arms race between predators and prey. The detailed perfection of defensive devices delighted Niko over and over again. He argued strongly against the prevalent opinions that m a n y defensive devices were too good to be true, or that in some sense t h e y were better t h a n necessary to fool the perception of predators (Tinbergen, 1963). I think he was right to do this. For me the complex perfection of defences seems to argue against the kinds of rapid macroevolutionary c h a n g e implied in some treatments of punctuationism.

Behavioural evolution in orb-weaving spiders Araneid spiders are a very n u m e r o u s part of the arthropod faunas of tropical rainforests (Elton, 1973). A considerable b o d y of research has accumulated on their behaviour in the last 25 years (see for instance, Shear, 1986). Students have concentrated on p r e d a t o r y behaviour, courtship and mating behaviour, web structure and w e b building. These studies have led to reconstructions of evolutionary p a t h w a y s and to the construction of phylogenies. M y o w n studies of p r e d a t o r y behaviour, and those of Eberhard, and our n u m e r o u s colleagues, co-workers and students have allowed us to reconstruct possible stages in the evolution of the complex attack and immobilization elements of araneid predatory behaviour. These studies have also provided us with functional explanations of the reconstructions. Robinson (1975) gives an overview of these reconstructions and the evidence for them. Later e n h a n c e m e n t s of that review can be found in Coddington (1986), Eberhard (1986) and Stowe (1986). The focus of this story is on p r e y - w r a p p i n g behaviour by w h i c h orb-weavers enswathe their prey in silk. Eberhard (1967) drew attention to the fact that not all web-building spiders (a term that includes several families, not only the d o m i n a n t orb-weavers) w e r e capable of using silk at the first stage of their attack. He p r o p o s e d a s c h e m e based on comparisons b e t w e e n families to account for the origins of attackwrapping. Later, I s h o w e d that all the stages for a hypothetical sequence of the evolution of attack wrapping exist within the one most diverse family of web-builders: the Araneidae (Robinson, 1969c). This scheme, s h o w n in Figure 7.4, is s u p p l e m e n t e d by details of the

Niko Tinbergen, comparative studies and evolution

114 1

2

3

oo.-°~~s''ss"

pathways exist. The three vertical lineages 1, 2, and 3 combined, represent the behavioural repertoire of stage 3 of Robinson (ibid). Sections I + 2 plus the broken lines represent stage 2a; 1 + 2 minus broken lines represent stage 2b; line 1 alone represents stage 1.

Descriptive reconstructions of the course of behaviour evolution

115

?

Figure 7.5 Evolution of orb-web structures. Arrows show the direction of specialization. Upper left: regular, more or less symmetrical orb. Lower left: ladder webs from New Guinea and Colombia. The detail shows the ladderlike viscid element. Upper right: horizontal orb of Poecilopachys sp. from Australia and New Guinea. The viscid elements are slack and hang down in loops; when an insect strikes one of them it shears at one end and absorbs the impact. Below this is shown the Pasilobus web, an orb reduced to one sector that functions in the same way. Bottom right: the bolas spiders Mastophora and Ordgarius make a single thread with one or two drops of viscid material (see text, pages 113-16).

functional a d v a n t a g e of e a c h stage in s u c h a r e c o n s t r u c t e d e v o l u t i o n a r y p a t h w a y . T h e s t u d i e s e v e n i n c l u d e d e x p e r i m e n t a l e v i d e n c e of t h e a d v a n t a g e of e a c h a d d i t i o n to t h e ' p r i m i t i v e ' state. E b e r h a r d ' s r e c e n t (1982) p h y l o g e n i e s for t h e f a m i l y a r a n e i d a e e m p h a s i z e t h e a p p e a r a n c e of a t t a c k w r a p p i n g w i t h i n t h e f a m i l y . P e r h a p s e v e n m o r e i n s i g h t - p r o v o k i n g for t h e p r o c e s s of r e c o n s t r u c t i n g p a t h w a y s of w e b - e v o l u t i o n are d i s c o v e r i e s a b o u t specializat i o n s of t h e o r i g i n a l l y w h e e l - l i k e o r b w e b . W e b s t r u c t u r e is a n e x p r e s s i o n of b e h a v i o u r a n d c a n b e r e g a r d e d as a n e x p r e s s i o n of t h e e v o l u t i o n of s p e c i e s - s p e c i f i c b e h a v i o u r . In 1970, w i t h B. R o b i n s o n I d i s c o v e r e d a r e m a r k a b l e specialization of the c o n v e n t i o n a l o r b in P a p u a

116

Niko Tinbergen, comparative studies and evolution

N e w G u i n e a (Robinson a n d Robinson, 1972). W e called this a ladder w e b b e c a u s e it consisted of a parallel-sided extension of a l o w e r s e g m e n t of an orb in w h i c h the viscid element, spiral in an orb, w a s side-to-side like the rungs of a ladder. Eberhard then discovered an equally specialized 'inverted' ladder w e b in Colombia (Eberhard, 1975). This remarkable piece of c o n v e r g e n c e (Figure 7.5) b e t w e e n t w o u n r e l a t e d spiders, s e p a r a t e d b y m o r e than 15 000 miles, is attributable to the operation of a c o m m o n selective factor. It is part of the continuing arms race b e t w e e n spiders a n d moths. Moths (and other lepidopterans) can escape readily from spiders w e b s (Eisner et al., 1964, Robinson, 1969d). The scales on their wings c o m e off onto the glue on the web, inactivate it, a n d they flutter free. The ladder w e b gives an exaggerated vertical extent of sticky surface to flutter against. Eberhard (1977, 1980a) w o r k e d out the p r e d a t o r y m e c h a n i s m s involved in the moth-catching behaviour of the bolas spider Mastophora dizzydeani, an araneid that uses as a capture device a single short thread with a terminal glue droplet. The m o t h secretes a chemical lure to attract male moths, and has almost certainly evolved a superglue. This device begs the question, w h a t are the stages b e t w e e n the ancestral orb and this highly r e d u c e d silk structure? The discovery in P a p u a N e w G u i n e a of the Pasilobus w e b (Robinson a n d Robinson, 1975) p r o v i d e d both a link in the evolutionary s e q u e n c e and the basis for reinterpreting the w e b of Poecilopachys described by Clyne (1973). The webs of both of these spiders are more or less horizontal and the viscid elements h a n g b e l o w the structural frame. Each sticky element has a low shear joint at one end, and this breaks on impact to absorb the shearing force exerted by the flying moth. The tethered insect is then killed by the spider. The Poecilopachys w e b is a complete orb; that of Pasilobus consists of only t w o sectors of an orb. The step from one to the other is one of reduction and concentration. The Pasilobus w e b can give rise to the bolas in m u c h simpler steps than can the conventional orb. Figure 7.5 s h o w s these structures. Further intermediates could await discovery. Robinson and Robinson (1978, 1980) carried out a s t u d y of the courtship and mating b e h a v i o u r of more than 50 species of araneid spiders. These studies revealed that courtship fell into three major categories according to both the position of the courting male in relation to the female's web, and to the type of primary s e n s o r y modalities involved. T h e y regarded these categories as representing an evolutionary progression from primitive to advanced, b u t Eberhard (1982) disagreed. There is a c o r r e s p o n d e n c e b e t w e e n classification b a s e d on p r e d a t o r y b e h a v i o u r and that b a s e d on courtship.

Descriptive reconstructions of the course of behaviour evolution

117

Behavioural comparisons and taxonomic relationships M o y n i h a n has contributed consistently to the elucidation of relationships through behaviour comparisons. In 1959 he p r o d u c e d a revision of the family Laridae; then in 1962 a major review of S o u t h American and Pacific larids. In that first major treatment M o y n i h a n d i s c u s s e d the kinds of b e h a v i o u r t h a t p r o v i d e 'reliable evidence of relationships', arguing that displays serve that function best. H e d e f i n e d display as ' a n y and all b e h a v i o u r patterns that have b e c o m e standardized or s t e r e o t y p e d in any way, in order to s u b s e r v e a social signal function.' The usefulness of displays in t a x o n o m y is, M o y n i h a n argued, ' d u e to the fact that they are less often or less thoroughly, affected by c o n v e r g e n t evolution than m a n y morphological features' a n d 'displays n e e d not be so closely a d a p t e d to as m a n y aspects of the external e n v i r o n m e n t ' . Later he w a s to a d d (Moynihan, 1975) 'the physical features which are characteristic of m o s t displays, that is stereotypy and exaggeration of form, are equally characteristic of some b e h a v i o u r patterns which are a d a p t e d to p r o m o t e crypsis'. It s e e m s to me that these j u d g e m e n t s still stand: displays are g o o d characters. However, good taxonomic judgements can be derived from other types of behaviour, as Eberhard has s h o w n . After a really extensive series of investigations into web-building behaviour, Eberhard (1982) combined data from these studies with extensive data from his o w n and other studies of predatory behaviour and courtship behaviour to use 'behavioural characters for the higher classification of orbweaving spiders'. He used data from 148 species, representing 'at least' 55 genera, to d e v e l o p a distribution of conservative characters that agrees 'in general' with classical taxonomic s c h e m e s b a s e d on adult m o r p h o l o g y . Eberhard concentrated his web-building studies on four p h a s e s of constructional behaviour. These were: 1. The construction of the radii (four distinct methods). 2. The construction of the temporary spiral of the w e b (three different styles). 3. The construction of the sticky spiral of the w e b (five distinct elements together totalling 13 different behaviours). 4. Construction of the h u b of the w e b (five distinct behaviours). This kind of behavioural analysis gives a lot of information to correlate. To illustrate the complexity of the behaviours, I can simplify just o n e of the sections of analysis, that on sticky spiral construction. To a d d the spiral, all o r b - w e a v e r s w o r k from the o u t s i d e of the w e b inwards, after building the non-sticky structural scaffolding of the web. Most spiders construct a t e m p o r a r y spiral of dry silk from the inside

118

Niko Tinbergen, comparative studies and evolution

o u t w a r d s before laying d o w n the sticky spiral. T h e y u s e this as a foothold during their construction walk. As the spider m o v e s from radius (spoke) to radius it attaches the spiral. H o w the spider gauges the attachment point is subject to very marked behavioural differences b e t w e e n genera. There are four different a n d distinct b e h a v i o u r s at this stage w h i c h are complex a n d difficult to describe in w o r d s alone. H o w e v e r , to describe just part of the m o v e m e n t illustrates the difference. In version (a) the spider reaches forwards with its left first leg; in version (b) it reaches forwards with its right first leg; in version (c) it reaches back with its left fourth leg, and in version (d) there is no reaching b e h a v i o u r at all. There are also b e h a v i o u r differences in which legs hold the radius just before the m o m e n t of attachment, and in contacts with the t e m p o r a r y spiral. This is probably as complex a comparative analysis of b e h a v i o u r as has ever b e e n d o c u m e n t e d . It revealed a n u m b e r of c o n v e r g e n c e s as well as illuminating relationships.

Comparative studies and the production of evolutionary insights M o y n i h a n ' s w o r k on c o m m u n i c a t i o n in squids, cuttlefish, nautiloids and o c t o p u s (1975; 1983a, b; 1985; M o y n i h a n and Rodaniche, 1977; 1982) follows his long series of other comparative studies that has greatly illuminated several dark corners. M o y n i h a n ' s work has ranged (in at least 25 substantial papers from 1955 to the present) from gulls, through birds of several other families, to N e w World primates, cephalopods and back to birds again. To me the most exciting aspect of the cephalopod work, out of many exciting features, is Moynihan's identification of the conservatism of certain displays. The c e p h a l o p o d s have a very ancient history and they are quite well represented by fossils, so we k n o w w h e n certain major groups separated: plus or minus a few million years, the three d o m i n a n t orders of m o d e r n c e p h a l o p o d s Teuthida (squids), Sepiida (cuttlefish), Octopida (octopus and argonauts) certainly separated in the early Mesozoic. But as M o y n i h a n has s h o w n they still share four major categories of display! These are: 1. A display called the dymantic, in which t w o black spots appear on the b o d y . 2. The zebra stripes, in which relatively close-packed transverse stripes appear on the body. 3. The upward vee curls in which t w o arms are raised and held back over the ' h e a d ' , almost bull's h o r n s fashion. 4. Longitudinal streaks, stripes d i s p o s e d fore to aft.

Descriptive reconstructions of the course of behaviour evolutions

119

Figure 7.6 Two octopus displays (from Moynihan, 1985). Eyes, eyespots and postures. Bottom left, the Dymantic display of Octopus vulgaris, and above, the display of Octopus hummalincki. M o y n i h a n argues that these displays must be ancestral b e c a u s e convergence on this scale is highly improbable. I find this a convincing argument. The 190 million year itch has not affected s o m e really basic behaviour patterns. This raises a why? question. His answers are worth reading.

120

Niko Tinbergen, comparative studies and evolution

M o y n i h a n has also (1985) u s e d c o m p a r i s o n s with the C e p h a l o p o d a to raise some fundamental questions in the field of animal communication. Until animals as capable of "instant' a n d complex visual communication were studied in the field some of these questions were in a sense almost unthinkable. C e p h a l o p o d s , particularly the social, free-swimming, non-cryptozoic squids a n d cuttlefishes, are e q u i p p e d with the organic equivalent of a video display tube. Patterns of great complexity (Figure 7.6) can flash on their skin, flicker and c h a n g e in instants. Nothing in the animal k i n g d o m matches this. M o y n i h a n and his co-worker Rodaniche (1977; 1982) have w a t c h e d h o u r s of 'continuous' pattern changes in the reef squid Sepioteuthis sepiodea. This mass of observations has led M o y n i h a n (1985) to examine this communication in terms of rules and syntax. This treatment is challenging a n d provocative, one might e v e n say 'far-out', b u t it is a true e m e r g e n c e of theory from a n e w line of comparative studies. It is the animals themselves that are 'far-out' a n d they m a y be the basis for o p e n i n g a n e w door. O n e of the things emerging from the c e p h a l o p o d studies is that these animals exceed the quantitative limits of display repertoires k n o w n from vertebrate studies. The idea of limits on display repertoires was d e v e l o p e d by M o y n i h a n (1970) in a p a p e r based on a comparative review. The theory and implications are interesting, but before dealing with t h e m it is worth returning to the relatively h u g e repertoires of s o m e c e p h a l o p o d s . W h y do s o m e of t h e m exceed the ' n o r m ' for vertebrates by as m u c h as half an order of m a g n i t u d e ? M o y n i h a n argues (1985) that s o m e of the complex ritualized patterns classified as displays may, in fact, be w h a t he has called anti-displays (1975). Anti-displays is a difficult term, but has b e e n u s e d to refer to complex adaptations that p r o m o t e crypsis of, m o r e generally, displays 'that are d e s i g n e d to i m p e d e the transfer of information to d a n g e r o u s perceivers'. This is a most interesting extension of antipredator theory. I have s u g g e s t e d (Robinson, 1969b; 1981; 1985) that eucrypsis (camouflage sensu stricto) d e p e n d s for its success in the suppression of signals, w h e r e a s all other systems d e p e n d on signalling either false information (plant-part and Batesian mimicry) or true information (aposematism). This scheme is r e p e a t e d b y E d m u n d s (1974) in his definitive 'Defence in animals'. M o y n i h a n ' s c e p h a l o p o d studies suggest a n e w extension of defence theory. An animal m a y p r o d u c e utter confusion in a predator by very rapid changes in colours, patterns, shapes and textures. In a sense such a succession of anti-displays w o u l d constitute image suppression. A further insight derived from comparative studies concerns the control, suppression, decay, d i s a p p e a r a n c e and replacement of

Descriptive reconstructions of the course of behaviour evolution

121

displays. After reviewing published accounts of the display repertoires of 62 species of vertebrate, m a m m a l s , birds a n d fishes, M o y n i h a n (1970) c o n c l u d e d that, despite great differences in habits a n d social structure, the n u m b e r of displays w a s remarkably similar. H e points out that 'the usual range of displays w o u l d s e e m to be from approximately 15 to approximately 35'. This conclusion leads to a w h y question. The interesting a n s w e r i n g suggestion is that repertoire ranges m a y be a d i v e r s i t y - d e p e n d e n t matter. The m o r e displays the more some will inevitably be rare a n d u n e x p e c t e d . H e also argues that the more diversity in the repertoire, the more diverse the form of each n e w display will have to be in order to be distinguishable, and therefore the more peculiar and disturbing it might be. This approach is full of possibilities for further s t u d y and analysis. It provides predictions about h o w and w h y displays s h o u l d decline in a species history, and a b o u t w h y a n d with w h a t they s h o u l d be replaced. It is possibly a reflection on o u r ability to r e s p o n d to rare, 'peculiar', and diverse ideas that its insights have b e e n less u s e d b y others of the species ethologist than t h e y s h o u l d have been. A n o t h e r delightful example of the revelatory value of comparative studies relates to horned beetles. There has long been a mystery about the function of horns in beetles. Darwin was intrigued by the function of the horns of stag beetles that he f o u n d in Chile during the Beagle voyage. O p i n i o n s have differed ever since with h y p o t h e s e s a b o u t horns as sex-attracting a d o r n m e n t s and e v e n functionless results of allometry. The problems involved in sorting out function were: 1. Lack of observations on living beetles. 2. The vast array of structures involved in ' h o r n ' p r o d u c t i o n (extensions of the head, mandibles, front legs, prothorax and so on). 3. The form of the ' h o r n s ' themselves, which is extraordinarily variable from the simple to the grotesque. 4. The fact that they occur in m a n y unrelated beetle families. Characteristically, the matter has b e e n t h o r o u g h l y dealt with b y Eberhard (1979; 1980b, 1981) on the basis of studies of 17 species of h o r n e d beetles. Once the first m y s t e r y is elucidated the insight n e e d e d for the solution to others is accumulated incrementally. Here, in this study, comparison facilitates. Quite simply 'it has b e e n established that far from being useless, beetle horns serve as effective w e a p o n s in contests b e t w e e n m e m b e r s of the same species over critical resources' (Eberhard 1980b). The horns are used in a remarkable variety of ways, some of which are s h o w n in Figure 7.7. This is a clever s t u d y s h o w i n g the p o w e r of ingenious, c o m p a r i s o n - m i n d e d , investigation.

122

Niko Tinbergen, comparative studies and evolution

Figure 7. 7 Horned beetles, after Eberhard. A1 shows the prothorax ventral horn of the beetle Doryphora punctissima, at first sight not a useable weapon because of its location and the fact that it does not extend beyond the head. A2 shows the use of this horn in combat. The unshaded individual is prying the other off the substrate. B1 shows the elongated antler-like horns of a darkling beetle close to the species Molion muelleri; since the beetle lives in tunnels it is difficult to guess at the utility of such jaws. B2 shows their use in combat. The more aggressive combatant turns through 180 ° and clamps its opponent behind the head.

CONCLUSION:

PROBLEMS

AND

PROSPECTS

Problems W h a t p r o b l e m s exist in c o m p a r a t i v e s t u d i e s ? S o m e are c o m m o n to all t h e e v o l u t i o n a r y a s s u m p t i o n s a n d i n t e r p r e t a t i o n s d e r i v e d f r o m c o m p a r i s o n s . C o m m o n l y , p r o b l e m s arise f r o m c o m p a r i n g t h e w r o n g c h a r a c t e r s . This is t r u e of t h e c o m p a r i s o n b e t w e e n m o r p h o l o g i c a l c h a r a c t e r s t h a t is the basis of m o s t p h y l o g e n y c o n s t r u c t i o n . S u c h c h a r a c t e r s differ c o n s i d e r a b l y in t h e i r v a r i a n c e f r o m o r g a n to o r g a n a n d species to species. In the 'old d a y s ' expert taxonomists w e r e e x p e r t b e c a u s e , after s t e e p i n g t h e m s e l v e s in t h e i r speciality for y e a r s , t h e y h a d a n i n d u c t i v e basis for a s s e s s i n g w h i c h c h a r a c t e r s w e r e ' g o o d ' . N o w a d a y s t h e y confirm their intuitions with statistics, or p e r h a p s e v e n test their j u d g e m e n t that way. It is i m p o r t a n t that the characters c h o s e n

Conclusion: problems and prospects

123

for c o m p a r i s o n s h o u l d be reliably species-specific. Since e t h o l o g y ' s adolescent days of the 1960s our faith in the fixity of behaviour patterns has been s o m e w h a t eroded. For instance, Martin and M a y (1982) claim that 'Animal behaviour, both within and b e t w e e n species, t e n d s to exhibit m u c h greater variability than does m o r p h o l o g y or physiology. This makes it difficult to reconstruct p h y l o g e n i e s from b e h a v i o u r patterns.' This echoes some w i d e s p r e a d scepticism. Recent e m p h a s e s on s t u d y i n g intraspecific difference in behaviour, a n d the occurrence within a species of different evolutionary stable strategies, have t e n d e d to reduce the e m p h a s i s on broad comparative studies. This is in part a product of the fashions that s w e e p through ethology as well as other branches of science. It is also p r o b a b l y a reflection of changes in academic p r o c e d u r e s and the state of the job market (these are n o t necessarily i n d e p e n d e n t variables). Clutton-Brock and H a r v e y ' s (1984) review of comparative approaches to investigating adaptation provides a detailed critique of methods and comments: ' O u r intention in reviewing the pitfalls of the comparative m e t h o d is not to discourage the use of comparisons: many important questions can only be approached in this way. Moreover, it is w o r t h r e m e m b e r i n g that while ideal c o m p a r i s o n s are u n c o m m o n , ideal experiments which control for all possible c o n f o u n d i n g variables are rare.' In conclusion, I am sure that w e cannot afford to neglect the comparative m e t h o d . The examples cited above, alone, and selective as they are, s h o w w h a t insights it can provide. I think t h e y also s h o w that in the h a n d s of good naturalists, choices can be m a d e about the bases of comparison that circumvent m a n y of the problems that can otherwise bedevil the process. We can now, a priori, define some n e w caveats about the behavioural characters we use. For instance, the great revival of interest in sexual selection has b e e n heuristic in m a n y fields. We should n o w surely be convinced that w h e r e there is female choice there m u s t be differences to be c h o s e n b e t w e e n . This m e a n s that w h e n w e s t u d y courtship b e h a v i o u r w e must expect variability in those elements that can reflect, and be u s e d b y the female to detect, differences b e t w e e n males (and ultimately differences in their fitness). This m e a n s that, in phylogenic comparisons of courtship behaviour, w e should be s t u d y i n g differences in strategies, not tactics. In particular, w e should also c o m p a r e the differences in strategies that make differences in tactics possible. (Eberhard (1985) has a marvellous book a b o u t differences in the form of male sex organs and the extent to which this d e p e n d s on female preference. Vive la difference indeed!) It also seems to me that in general, behaviours associated with primary defence (preventing detection as prey, Robinson, 1969a) should be more reliably specific than those

124

Niko Tinbergen, comparative studies and evolution

involved in secondary defence (i.e. those that operate to t h w a r t attack after detection). The construction of prey-capture artefacts, a n d the types of p r e d a t o r y behaviour elicited by specific types of p r e y s h o u l d also be strongly invariable. I have not even m e n t i o n e d a n o t h e r field for comparative studies that seems to be of great potential, i.e. that of m a p p i n g the evolution of learning, intelligence, m e m o r y a n d consciousness. Griffin (1978, 1981, 1984) o p e n e d the doors to this for us. The prospects are exciting. We are, I hope, still curious naturalists all. The use of comparative m e t h o d s in studies of evolution, a n d particularly, for me at least, in studies of the Paley p h e n o m e n o n , is a great game (in the sense of Kipling's Kim), fascinating, tantalizing, exciting a n d ultimately satisfying. Niko Tinbergen delighted in the w o n d e r s p r o d u c e d by the evolutionary process a n d the great game of discovery. I h o p e we c o n t i n u e to play at it.

REFERENCES Baerends, G.P. and Barends-van-Roon, J.M. (1950) An introduction to the study of the ethology of cichlid fishes. Behaviour, Suppl 1, 1-242. Blest, A.D. (1957a) The function of eye-spot patterns in the Lepidoptera. Behaviour, 11, 209-56. Blest, A.D. (1957b) The evolution of protective displays in the Saturnioidea and Sphingidae (Lepidoptera). Behaviour, 11, 257-309. Blest, A.D. (1963a) Relations between moths and predators. Nature, Lond., 197, 1046-7. Blest, A.D. (1963b) Longevity, palatability and sound production in some New World arctiid and ctenuchid moths. Zoologica, 49, 161-81. Cloarec, A. (1988) Behavioral adaptations to aquatic life in insects, in Advances in the Study of Behavior, (eds. J.S. Rosenblatt, C. Beer, M-C. Busnel, P.J.B. Slater), Academic Press, New York, pp. 99-151. Coddington, J. (1986) The monophyletic origin of the orb web, in Spiders, webs, behavior and evolution, (ed W.A. Shear) Stanford University Press, Stanford, California, pp. 319-63. Clutton-Brock, T.H. and Harvey, P.H. (1984) Comparative approaches to investigating adaptation, in Behavioural Ecology, (eds J.R. Krebs and N.B. Davies), Sinauer Associates Inc., Cambridge, pp. 7-29. Clyne, D. (1973) Notes on the web of Poecilopachys australasia (Griffin and Pidgeon 1833) (Araneidae: Argiopidae). Australia Entomologist's Magazine, 1, 23-29. Crane, J. (1952) A comparative study of the innate defensive behaviour of Trinidad mantids (Orthoptera, Mantoidea). Zoologica, 37, 259-93. Dawkins, R. (1986) The Blind Watchmaker, W.W. Norton, New York and London. De Ruiter, L. (1952) Some experiments on the camouflage of stick caterpillars. Behaviour, 4, 222-32.

References

125

De Ruiter, L. (1955) Countershading in caterpillars. Archs. n~erlandaise de Zoologie, 11, 1-17. Eberhard, W.G. (1967) Attack behavior of diguetid spiders and the origin of prey-wrapping in spiders. Psyche, 74, 173-81. Eberhard, W.G. (1975) The 'inverted ladder' orb web of Scoloderus sp, and the intermediate orb of Eustala sp. (Araneae: Araneidae). Journal of Natural History, 9, 93-106. Eberhard, W.G. (1977) Aggressive chemical mimicry by a bolas spider. Science, 198, 1173-75. Eberhard, W.G. (1979) The function of horns in Podischnus agenor and other beetles, in Sexual selection and reproductive competition in insects, (eds M. Blum and N. Blum), Academic Press, New York, pp. 231-58. Eberhard, W.G. (1980a) The natural history and behavior of the bolas spider, Mastophora dizzydeani sp. N. (Araneidae). Psyche, 87, 143-69. Eberhard, W.G. (1980b) Horned beetles. Scientific American, 242, 166-82. Eberhard, W.G. (1981) The natural history of Doryphora sp. (Coleoptera, Chrysomelidae). and the function of its sternal horn. Annals of Entomological Society of America, 74, 445-48. Eberhard, W.G. (1982) Behavioral characteristics for the higher classification of orb-weaving spiders. Evolution, 36, 1067-95. Eberhard, W.G. (1985)Sexual selection and animal genitalia, Harvard University Press, Cambridge, Mass. Eberhard, W.G. (1986) Effects of orb-web geometry on prey interception and retention, in Spiders, webs, behavior and evolution, (ed W.A. Shear)Stanford University Press, Stanford, Calif. pp. 70-100. Edmunds, M. (1972) Defensive behaviour in Ghanaian praying mantids. Zoological Journal of the Linnean Society, 51, 1-32. Edmunds, M. (1974) Defence in Animals, Longman, London. Edmunds, M. (1976) The defensive behaviour of Ghanaian praying mantids with a discussion of territoriality. Zoological Journal of the Linnean Society, 58, 1-37. Eisner, T., Alsop, R., Ettershank, G. (1964) Adhesiveness of spider silk. Science, 146, 1058-61. Eldredge, N. (1985a) Time frames: The rethinking of Darwinian evolution and the theory of punctuated equilibria. Simon and Schuster, New York. Eldredge, N. (1985b) Unfinished synthesis: Biological hierarchies and modern evolutionary thought. Oxford University Press, New York. Eldredge, N. (1989) Macro-evolutionary Dynamics. McGraw-Hill, New York. Elton, S.S. (1973) The structure of invertebrate populations inside neotropical rainforest. Journal Animal Ecology, 42, 55-104. Erwin, T. (1982) Tropical forests: their richness in coleoptera and other arthropod species. The Coleopterist's Bulletin, 34, 305-22. Griffin, D.R. (1978) Prospects for a cognitive ethology. Behavioral and Brain Sciences, 1, 527-38. Griffin, D.R. (1981) The Question of Animal Awareness. Rockefeller University Press, New York. Griffin, D.R. (1984) Animal Thinking. Harvard University Press, Cambridge, MA, USA; London, England Gould, S.J. (1980) Is a new and general theory of evolution emerging? Paleobiology, 6, 119-30.

126

Niko Tinbergen, comparative studies and evolution

Gould, S.J. and Eldredge, N. (1977) Punctuated equilibria: The tempo and mode of evolution reconsidered. Paleobiology, 3, 115-51. Kranz, K.(1982) A note on the tail hairs from a pygmy hippopotamus (Choeropsis liberiensis). Zoo Biology, 1, 237-41. Hinde, R.A. and Tinbergen, N. (1958) The comparative study of speciesspecific behaviour, in Behaviour and Evolution, (eds A. Roe and G.G. Simpson, Yale University Press, Hartford, pp. 251-68. Mayr, E.(1982) The Growth of Biological Thought. Harvard University Press, Cambridge, MA, USA, London, England. Mayr, E. (1988) Towards a new philosophy of biology, Harvard University Press, Cambridge, Mass. Martin, R.D. and May, R. (1982) Outward signs of breeding, in Evolution now, (ed J.M. Smith) Freeman, San Francisco. Moynihan, M.H. (1959) A revision of the family Laridae (Ayes), American Museum Novitates, 1928, 1-42. Moynihan, M.H. (1962) Hostile and sexual behavior patterns of South American and Pacific Laridae. Behaviour, Suppl, 8, 1-365. Moynihan, M.H. (1970) The control, suppression, decay, disappearance and replacement of displays. Journal of Theoretical Biology, 29, 85-112. Moynihan, M.H. (1975) Conservatism of displays and comparable stereotyped patterns among cephalopods, in Function and evolution in behaviour, (eds G. Baerends, C. Beer, A. Manning), Oxford University Press, Oxford, pp. 276-91. Moynihan, M.H. (1983a) Notes on the behavior of Europrymna scolopes (Cephalopoda, Sepiolidae). Behaviour, 85, 25-41. Moynihan, M.H. (1983b) Notes on the behavior of Idiosepius pygmaeus (Cephalopoda, Idiosepiidae). Behaviour, 85, 42-57. Moynihan, M.H. (1985) Communication and noncommunication in cephalopods, Indiana University Press, Bloomington, Indiana. Moynihan, M.H. and Rodaniche, A.F. (1977) Communication, crypsis and mimicry among cephalopods, in How animals communicate, (ed T. Sebeok) Indiana University Press, Bloomington, Indiana, pp. 293-302. Moynihan, M.H. and Rodaniche, A.F. (1982) The behavior and natural history of the Caribbean reef squid Sepioteuthis sepioidea. Zeitschrifl fiir Tierpsychologze Advances in Ethology, 25, 1-150. Ridley, M. (1983) The explanation of organic diversity, Oxford University Press, Oxford. Robinson, M.H. (1964) The Javanese stick insect, Orxines macklotti De Haan (Phasmatodea, Phasmidae). The Entomologist's Monthly Magazine, 100, 254-59. Robinson, M.H. (1968a) The defensive behavior of the Javanese stick insect Orxines macklotti De Haan, with a note on the startle display of Metriotes diocles Westw. (Phasmatodea, Phasmidae). The Entomologist's Monthly Magazine. 104, 46-51. Robinson, M.H. (1968b) The startle display of Balboa tibialis (Brunner), (Orth., Tettigoniidae). The Entomologist's Monthly Magazine, 104, 88-90. Robinson, M.H. (1968c) The defensive behavior of Pterinoxylus spinulosus Redtenbacher, a winged stick insect from Panama (Phasmatodea). Psyche, 75, 195-207. Robinson, M.H. (1968d) The defensive behavior of the stick insect Oncotophasma martini (Griffini). (Orthopotera: Phasmatidae). Proceedings of the Royal Entomological Society, London, 43, 183-87.

References

127

Robinson, M.H. (1969a) Defenses against visually hunting predators. Evolutionary Biology, 3, 225-59. Robinson, M.H. (1969b) The defensive behavior of some orthopteroid insects from Panama. Transactions of the Royal Entomological Society, London, 121, 281-303. Robinson, M.H. (1969d) The predatory behavior of Argiope argentata (Fabricius). American Zoologist, 9, 161-73. Robinson, M.H. (1970a) Animals that mimic parts of plants. Morris Arboretum Bulletin, 21, 51-58. Robinson, M.H. (1970b) Insect antipredator adaptations and the behavior of predatory primates. Act. IV Congr. Latin Zool, 2, 811-36. Robinson, M.H. (1973) The evolution of cryptic postures in insects, with special reference to some New Guinea tettigoniids (Orthoptera). Psyche, 80, 159-65. Robinson, M.H. (1975) The evolution of predatory behaviour in araneid spiders, in Essays on the evolution and function of behaviour, (eds G. Baerends, C. Beer, and A. Manning), Oxford University Press, Oxford, pp. 292-312. Robinson, M.H. (1977) Informational complexity in tropical rain forest habitats and the origins of intelligence. Actas del IV Symposium Internacional de Ecologia Tropical Panama, 1, 148-68. Robinson, M.H. (1978) Tropical biology; is it real? Tropical Ecology, 19, 30-50. Robinson, M.H. (1979) By dawn's early light: matutinal mating and sex attractants in a neotropical praying mantis. Science, 205, 825-27. Robinson, M.H. (1981) A stick is a stick is a stick: on the definition of mimicry. Biological Journal of the Linnean Society of London, 16, 1-6. Robinson, M.H. (1982) Courtship and mating behaviour in spiders. Annual Review of Entomology, 1-20. Robinson, M.H. (1985)Predator-prey interactions, informational complexity, and the origins of intelligence. Journal of the Washington Academy of Sciences, 75, (4), 91-104. Robinson, M.H., Mirik, H. and Turner, O. (1969c) The predatory behavior of some araneid spiders and the origin of immobilization wrapping. Psyche, 76, 487-501. Robinson, M.H. and T. Pratt (1976) The phenology of Hexacentrus mundus at Wau, Papua New Guinea (Orthoptera- Tettigoniidae). Psyche, 82, 315-23. Robinson, M.H. and Robinson, B. (1972) The structure, possible function and origin of the remarkable ladder-web produced by a New Guinea orb-web spider. Journal of Natural History, 6,687-94. Robinson, M.H. and Robinson, B. (1975) Evolution beyond the orb-web, the web of Pasilobus sp.: its structure, construction and function. Zoological Journal of the Linnean Society of London, 576, 301-14. Robinson, M.H. and Robinson, B. (1978)The evolution of courtship systems in tropical araneid spiders Symposium of the Zoological Society of London, 42, 17-29. Robinson, M.H. and Robinson, B. (1980) Comparative studies of the courtship and mating behavior of tropical araneid spiders. Pacific Insects Monographs, 36. Shear, W.A. (ed) (1986) Spiders, webs, behavior and evolution, Stanford University Press, Stanford, CA.

128

Niko Tinbergen, comparative studies and evolution

Stowe, M.K. (1986) Prey specialization in the Araneidae, in Spiders, webs, behavior and evolution, (ed W.A. Shear), Stanford University Press, Stanford, Calif., pp. 101-132. Tinbergen, N. (1951) The study of instinct, Oxford University Press, Oxford. Tinbergen, N. (1954) The origin and evolution of courtship and threat display, in Evolution as a process, (eds. A.C. Hardy, J.S. Huxley and E.B. Ford) Allen and Unwin, London, pp. 233-50. Tinbergen, N. (1959a) Behavior, systematics and natural selection. Ibis, 101, 418-30. Tinbergen, N. (1959b) Comparative studies of the behaviour of gulls (Laridae): a progress report. Behaviour, 15, 1-70. Tinbergen, N. (1960) The evolution of behavior in gulls. Scientific American, 203, 118-30. Tinbergen, N. (1962) The evolution of animal communication, Symposium of the Zoological Society, London, 8, 1-8. Tinbergen, N. (1963) On aims and methods in ethology. Zeitschrifl fiir Tierpsychologie, 20, 410-33. Tinbergen, N. (1964) On adaptive radiation in gulls (Tribe Larini). Zool. Meded. Leiden, 34, 209-23. Tinbergen, N. (1965a) Behavior and natural selection, in Ideas in modern biology, Proceedings XVI International Congress Zool., (ed J.A. Moore) Natural History Press, New York, pp. 521-42. Tinbergen, N. (1965b) Some recent studies of the evolution of sexual behavior, in Sex and behavior, (ed F.A. Beach), Wiley, New York, pp. 1-34. Tinbergen, N. (1972) The animal in its world, Vol. 1. Allen and Unwin, London. Tinbergen, N., Broekhuysen, G.J., Feekes, F. et al. (1962) Egg-shell removal by the black-headed gull, Larus ridibundus L., a behaviour component of camouflage. Behaviour, 9, 74-117.

--8

The Tinbergen legacy in photography and film LARY SHAFFER

Niko Tinbergen always felt that something w a s w r o n g because he was able to spend much of his professional life doing things that he enjoyed enormously: watching and photographing animals, and trying to work out the interaction b e t w e e n b e h a v i o u r a n d evolution. H e wrote an elegant justification of his activities near the end of 'Curious naturalists' (Tinbergen, 1958): 'It seems to me that no man need be ashamed of being curious about nature. It could even be a r g u e d that this is w h a t he got his brains for and that no greater insult to nature and to oneself is possible than to be indifferent to nature. There are occupations of decidedly lesser standing.' In return for the excitement a n d fun he w a s having, Niko felt that he had an obligation to the public who, ultimately, paid for his work. T h r o u g h o u t his professional life, he placed a very high value on c o m m u n i c a t i n g the results of his studies to the general public. H e said 'I try to impress on m y s t u d e n t s that half their w o r k is communication. Science is a social effort, a n d scientists m u s t adjust to the public. If people d o n ' t w a n t to read y o u r work, y o u r w h o l e effort, and all the m o n e y that w e n t into it has b e e n lost.' (Hall, 1974). He felt it was an important responsibility to present research in forms which w o u l d attract and engage people. Having disdain for the stilted style of the scientific journals, he always e n c o u r a g e d his s t u d e n t s to write in the first person and to minimize jargon. An important aspect of the Tinbergen legacy in animal b e h a v i o u r is the example he set in using film a n d p h o t o g r a p h y to describe his findings.

130

The Tinbergen legacy in photography and film

Niko was an artist as well as a scientist. Although he rarely indulged himself, w h e n he took the time, he s h o w e d considerable talent at pencil sketching. This skill w a s a useful technical tool for him as he w o r k e d in the field because he w o u l d often make simple sketches of behaviours to illustrate his notes. These quick d r a w i n g s displayed the essence of the b e h a v i o u r with a remarkable e c o n o m y of line. Niko's drawings scattered t h r o u g h o u t 'Curious naturalists' (Tinbergen, 1958) and 'The Herring Gull's World' (Tinbergen, 1953) are s p l e n d i d examples of this. Niko described h o w , as a boy, he y e a r n e d to p r o d u c e p h o t o g r a p h s w h i c h could accurately capture m u c h more detail than the d r a w i n g s he was making. Niko had a lifelong interest in p h o t o g r a p h y and his artistic gifts are evident in the w o n d e r f u l p h o t o g r a p h s which illustrate his books. His lifetime s p a n n e d a time of rapid change and i m p r o v e m e n t in p h o t o g r a p h y and Niko did his best - with very limited f u n d s at first to take a d v a n t a g e of n e w d e v e l o p m e n t s as they came along. For much of his life his photographic skill s e e m s to have b e e n h a m p e r e d by the e q u i p m e n t which w a s available to him. H e was r e a d y to fly before his e q u i p m e n t k n e w h o w to walk. His earliest p h o t o g r a p h s were taken on clumsy 61/2 x 81/2 inch glass plates, called ' w h o l e plates'. H e often amusingly talked about the struggles involved in trying to p h o t o g r a p h animals with the primitive plate cameras which a c c o m p a n i e d the fragile glass negatives. The n u m b e r of negatives which could be e x p o s e d on a given d a y w a s limited by the n u m b e r of plate holders Niko o w n e d . By careful saving he finally m a n a g e d to acquire three double holders which took a plate in each side, permitting six exposures. O n c e he had e x p o s e d these plates, it was necessary to return h o m e to d e v e l o p them and reload the plate holder. It always s e e m e d to Niko that the most exciting photographs were on the plates which w o u l d get broken on the bicycle ride h o m e . There w e r e other p r o b l e m s related to trying to p h o t o g r a p h natural history, and particularly herring gulls, with a plate camera. P e r h a p s first a m o n g these problems w a s trying to use such a bulky camera in a hide. Because the viewfinder w a s on top of the camera and it was necessary for both viewfinder and lens to have a view from the hide, it was almost impossible to disguise the camera without alarming the gulls. Most of Niko's plate camera pictures from hides were taken by simply waiting until s o m e t h i n g h a p p e n e d in front of the camera then snapping the shutter. The greatest d r a w b a c k of the plate camera was that it w a s not reflex - the p h o t o g r a p h e r did not look t h r o u g h the lens b u t rather t h r o u g h a separate viewfinder. Because this viewfinder only approximated the scene that w o u l d be photographed, -

The Tinbergen legacy in photography and film

131

focus was a matter of g u e s s w o r k . Even for those pictures w h i c h h a p p e n e d to be properly focused important parts of the action w o u l d sometimes occur b e y o n d the edge of the negative. The plate camera could be focused t h r o u g h the lens by r e m o v i n g the plate holder, but by the time the plate h o l d e r was reinserted a n d its cover r e m o v e d , the reason for the p h o t o g r a p h w o u l d often be gone. Niko developed an additional strategy for p h o t o g r a p h i n g the gulls with the plate camera, which involved camouflaging the camera u n d e r an old basket or s o m e t h i n g similar near to the probable site of action. The remote camera was watched from a hide. At just the right m o m e n t , w h e n the right behaviour was h a p p e n i n g , in w h a t s e e m e d to be the right distance in front of the camera, Niko w o u l d release the s h u t t e r with a long bulb-operated release. This yielded larger pictures of the gulls, allowing better prints to be m a d e , but it h a d the d r a w b a c k that only one picture could be taken at a time. Following the exposure, Niko w o u l d have to get out of the hide, disturb the animals, a n d go to the camera to insert another plate. Niko used his detailed knowledge of the gulls in order to successfully set up the camera just w h e r e the animal was likely to be at the m o m e n t that s o m e t h i n g interesting was about to h a p p e n . A problem for him however, was that the gulls liked to use the camera basket as a lookout post and m u c h of the interesting action took place on top of the camera. Niko s h o w e d great determination in those days a n d a l t h o u g h most of the old glass plate negatives did not result in a n y t h i n g useful, a few are remarkable illustrations of behaviour. Before the war, large boxy Soho reflex-type cameras became available a n d Niko u s e d one of these for a short time. This camera used film which was 31/4 by 41/4 inches. This machine h a d at least three advantages over the plate camera. It could use unbreakable celluloid cut film and it came with a 'bookform' film holder which allowed more exposures to be carried to the field a n d more rapid reloading for the taking of the next exposure. More important, as a single lens reflex camera it allowed Niko to focus a n d compose the scene t h r o u g h the lens that was taking the picture. This solved some of the problems of use in a hide because all but the lens of the camera could be obscured by camouflage and slow, careful m o v e m e n t s of the camera became possible. The drawback was that before a picture could be taken, the larger mirror which directed the image to the viewfinder h a d to be w i n c h e d up m a n u a l l y by pulling a string to move it out of the p a t h b e t w e e n the lens a n d the film. It was necessary for Niko to anticipate the pattern of behaviour so that the mirror winching could be initiated before the desired behaviour h a p p e n e d . Niko often r e m a r k e d that he learned a great deal about the patterns of behaviour by trying to

132

The Tinbergen legacy in photography and film

p h o t o g r a p h t h e m with this primitive camera. At the e n d of the exposure, the reflex mirror w o u l d drop to the viewfinding position on its o w n with a clang that w o u l d u p s e t the animals for several minutes. For the expedition that Niko a n d his wife Lies took to G r e e n l a n d in 1932, Niko u s e d a Rolleiflex. This w a s a twin lens reflex camera having t w o m a t c h e d lenses: one for v i e w f i n d i n g a n d o n e for photographing. The Rolleiflex was much more portable than the earlier reflexes and had the a d d e d advantage that it u s e d roll film which could easily be reloaded in the field. The relative ease of using this camera, as well as its sharper lenses a n d higher resolution film e n a b l e d Niko to return with hauntingly beautiful p h o t o g r a p h s of G r e e n l a n d a n d its inhabitants, s o m e of which are r e p r o d u c e d in 'Curious naturalists' (Tinbergen, 1958). The tameness of the s n o w buntings and red-necked phalaropes in virtually u n i n h a b i t e d parts of G r e e n l a n d allowed Niko to take g o o d close-up pictures w i t h o u t a hide, using the short lenses of the Rolleiflex. After the w a r Niko b r o u g h t an Alpa reflex which w a s o n e of the early small 35 m m single lens reflexes. The lens on the Alpa w a s interchangeable b u t Niko did not have sufficient f u n d s to b u y the expensive telephoto lenses which were available. H o w e v e r , at this time, there were a n u m b e r of war department surplus telephoto lenses available which had b e e n part of aerial p h o t o g r a p h y cameras. Niko obtained t w o of these magnificently sharp lenses, a 280 m m a n d a 340 m m and had them adapted to the Alpa in the Zoology Department w o r k s h o p in Leiden. Robust, variable length barrels were fabricated from heavy 3-inch brass pipe and fitted to the lenses to permit focusing. The laboratory technicians u s e d a 11/2 inch pipe thread (the only large diameter threading e q u i p m e n t in the w o r k s h o p ) to attach the enormously heavy lenses to a brass clamp which w r a p p e d around the Alpa b o d y . These m a m m o t h lenses w e r e attached to the tripod with the tiny Alpa hanging on at the back. The adaptation was crude b u t the results were not. M a n y of the memorable pictures of gulls in 'The Herring Gull's World' (Tinbergen, 1953) and m a n y of the w o n d e r f u l animal pictures, such as those of the kittiwakes in 'Curious naturalists' (Tinbergen, 1958) were taken with these brass cannons. After he m o v e d to Britain, Niko eventually retired the Alpa and p u r c h a s e d one of the early N i k o n F single lens reflexes. With this camera, several Nikkor lenses a n d a 400 m m Novoflex, Niko took m a n y of the pictures for 'Tracks' (Ennion a n d Tinbergen, 1967) and for 'Signals for survival (Tinbergen et al., 1970). At last Niko h a d the e q u i p m e n t required to reach out into the world of gulls a n d other animals and the result is that the 'Signals' b o o k tells the story of the gulls with f e w w o r d s but with m a n y excellent pictures.

The Tinbergen legacy in photography and film

133

Perhaps because of his early training with glass plates, Niko always shot film economically. He w o u l d return from a hide session with three rolls of e x p o s e d film saying that he h a d 'just blasted a w a y at everything.' In the darkroom, he h a d a g o o d eye for finding the right negative and m a d e excellent prints with casual abandon. After making only one small exposure test strip u n d e r the enlarger, he only rarely m a d e the prints which n e e d e d to be rejected b e c a u s e of total quality. In the darkroom he w o u l d grab prints from the developing trays with his hands, e s c h e w i n g print tongs as being too c u m b e r s o m e . I a l w a y s f o u n d it alarming to watch him leaning over the d e v e l o p i n g trays with a long and delicate ash hanging from the hand-rolled cigarette clenched in his lips. While I n e v e r actually s a w one of these a s h e s fall into the developer, or, in the field, into an o p e n camera back, I always expected to. Niko w a s a pioneer in the making of natural history films w h i c h tell a research story. While biologists have been making natural history films about their o w n research since motion pictures first a p p e a r e d , until recently very few of these films were sufficiently polished to bring the research stories to a wide public. A n o t e w o r t h y early exception w a s Julian H u x l e y ' s 1937 A c a d e m y A w a r d winning gannet film. Niko started taking motion pictures while still in H o l l a n d a n d p r o d u c e d a film about the courtship of the three-spined stickleback, as well as a film giving a composite view of research and field c a m p life in Hulshorst. Niko also tried to film herrring gulls, but j u d g i n g from the surviving scraps of film, camera limitations m a d e it uneconomic to attempt a gull film at this point. As far as I can ascertain, these earliest films were p h o t o g r a p h e d with a Kodak 16 mm, nonreflex, spring-driven camera with a single short lens. The v i e w f i n d e r w a s on the top of this camera and so difficulties with the v i e w f i n d i n g s h o w e d t h e m s e l v e s in the vertical dimension, with the t e n d e c y of heads or feet to be cut off. The difficulty in getting moving, n o n - h u m a n animals in focus was very great and much of the stickleback film avoids close-up shots, in which this difficulty w a s magnified. The black and white, silent stickleback a n d H u l s h o r s t films w e r e given a professional polish b y the addition of title cards to help tell the story. They were used extensively as teaching films in the Zoology d e p a r t m e n t at Leiden. W h e n Niko m o v e d to Oxford, the stickleback film was h a n d e d over to the British Film Institute for educational distribution to schools. By the time they w e r e retired, the BFI prints of the stickleback film were w o r n ragged, attesting to the n u m b e r s of s h o w i n g s they m u s t have had. U p o n N i k o ' s arrival in Oxford, Alister H a r d y h e l p e d to m a k e possible the purchase of a Bell & H o w e l l HR-1 which w a s a s t u r d y

134

The Tinbergen legacy in photography and film

s p r i n g - w o u n d 16 m m camera w h i c h h a d the a d v a n t a g e of h a v i n g a three-lens turret. In these d a y s before z o o m lenses, this turret permitted three different focal l e n g t h lenses to be u s e d in succession by rotating the turret until a n o t h e r lens came into the breech. The range of the t u r r e t - m o u n t e d lenses was limited because a t e l e p h o t o lens m o u n t e d on the turret w o u l d be part of the scene being p h o t o g r a p h e d by wider angle lenses. Although the Bell & Howell was not a reflex camera, its makers had provided a small focusing peephole near the edge of the lens turret. A lens was rotated until it was adjacent to this peephole, t h r o u g h which it could be focused on the subject. T h e n it was rotated back to the talking position before filming could begin. The viewfinder h a d an a d e q u a t e a d j u s t m e n t for parallax. Niko was d e t e r m i n e d to m a k e a series of films for use in t e a c h i n g at Oxford. He realized the potential which film offered to bring the excitement of m e t h o d s a n d results of the field camp work back to the u n f o r t u n a t e s w h o h a d been left b e h i n d in the lab. He started to w o r k on this project shortly after arrival in Oxford. Surviving scraps of film s h o w the attempts to s t u d y gulls on Scolt-Head Island, w h e r e the spring tide was so high that it covered m u c h of the b r e e d i n g colony, leaving gulls s w i m m i n g above their nests, waiting for the tide to recede. The earliest of Niko's Oxford teaching films stressed the results of the research, rather than the process of research. A m o n g the first were a film about Esther Cullen's kittiwakes on the Farne Islands, a n d a film s h o w i n g Bernard Kettlewell's classic experiments on industrial m e l a n i s m in the P e p p e r e d Moth. According to Niko, the P e p p e r e d Moth film was m a d e as a result of doubts, in some quarters, that birds could possibly be responsible for the differential p r e d a t i o n of black or pale-chequered moths. Working together, Niko and Kettlewell were able to produce convincing film evidence with good close-up shots of birds grabbing poorly c a m o u f l a g e d m o t h s from tree t r u n k s (Tinbergen, 1958). The kittiwake a n d the m o t h s were ideal subjects for filming with the Bell & Howell, because the action occurred in quite restricted areas (small ledges or small sections of tree trunk) w h i c h could be focused u p o n in advance using the little peephole. Niko h a d acquired a 150 m m telephoto lens with which he was able, for the first time, to get good motion picture close-ups of wild animals (Figure 8.1). The Bell & Howell w e n t with Niko to the Ravenglass field camp w h e r e he m a d e a series of teaching films. The earliest of these was a descriptive film about the courtship of the black-headed gull but his subsequent efforts were what he called 'research-in-action' films. These showed the researchers and details of their experimental manipulations as well as the responses of the animals involved. This tactic h a d been

The Tinbergen legacy in photography and film

135

Figure 8.1.

presaged in the old Hulshorst film, b u t at Ravenglass it became the major focus of Niko's film-making efforts. At the time that Niko was making these research-in-action teaching films, he met H u g h Falkus. H u g h w a s w o r k i n g for Border Television making a little series called 'Five Minutes with H u g h Falkus' in which he drifted a r o u n d the border country finding stories of local interest which could be told in five minutes. While travelling around, H u g h had heard about the w o r k of the Oxford Behaviour g r o u p at Ravenglass. H e visited, talked and ultimately m a d e four of the little p r o g r a m m e s a b o u t research there. Niko w a s fascinated by the extent to w h i c h television could bring animal b e h a v i o u r research to a very large audience, and he agreed to w o r k with the BBC to make three research-in-action programs for the 'Look' series. These half-hour, black and white programmes ('The sign readers', 'The b e a c h c o m b e r s ' a n d 'The gull watchers') contain quite a bit of Niko's animal b e h a v i o u r film as well as some interview material filmed by the BBC. At the same time, Niko was turning out m e m o r a b l e silent teaching films in colour on eggshell removal in the black-headed gull, search image in the carrion crow, and the breeding biology of the oystercatcher

136

The Tinbergen legacy in photography and film

Figure 8.2 Niko Tinbergen filming oystercatcher chicks in 1971.

(Figure 8.2). Niko also travelled to the Bass Rock to film the gannet studies of Bryan Nelson. These films b r o u g h t field w o r k alive for a generation of students. In 1966 Niko began another collaboration with H u g h Falkus to film the life story of the lesser black-backed gull on W a l n e y Island. This film, 'Signals for survival', w a s c o m m i s s i o n e d by the BBC for the 'World about us' series. By this time Niko had acquired a 16 mm, reflex Bolex motion picture camera. A r m e d with the telephoto lenses he had u s e d with his Nikon, as well as a little Pan Cinor z o o m lens he had the capability to catch the fast-moving action which p u n c t u a t e s this film. With the 'Signals' film the e q u i p m e n t ceased to limit his talent and the resulting p r o g r a m m e is a film of u n u s u a l b e a u t y as well as lasting educational value (Figure 8.3). Niko learned about the syntax of films while filming 'Signals' with H u g h Falkus. H u g h taught Niko about the use of long shots, closeu p s and establishing shots to tell the story visually. N i k o ' s previous films h a d told their story clearly, but the story was told with film clips which were, effectively, animated slides. Because of the limitations of the non-reflex cameras, m u c h of the early film that Niko took consisted of multiple shots of the same animal against the same

The Tinbergen legacy in photography and film

137

Figure 8.3 Niko Tinbergen filming 'Behaviour and survival' in 1972.

b a c k g r o u n d at the same magnification in the film frame. It is very difficult for a film editor to make a s m o o t h visual story with this kind of material. W h e n one s e g m e n t e n d s and a n o t h e r begins the animal on the screen seems to j u m p s u d d e n l y because the b a c k g r o u n d a n d magnification are the same but the animal has m o v e d b e t w e e n one shot a n d another. This kind of film edit is called, with justification, j u m p cut. If the editor has a variety of different magnifications or different camera angles with which to work, then the film can be fitted together like a linear jigsaw puzzle. Two segments which w o u l d jump if hitched together directly can be u s e d near to each other w i t h o u t the disruptive visual jump, if separated by a close-up. Niko k n e w the gulls a n d he k n e w their story. H u g h k n e w h o w to build a film. Their collaboration h a d its r o u g h edges, but it w o r k e d because each h a d respect for the expertise of the other. For the two seasons d u r i n g which 'Signals' was being made, Niko trooped out to the hides with H u g h ' s lists of specific shots which would be needed: close up h e a d and shoulders of gull facing left; m e d i u m shot of mated pair with grass background; and so on. Talking of this time, Niko often said that it was very difficult for h i m to concentrate on getting the specific shots which were n e e d e d w h e n , at the same time, other

138

The Tinbergen legacy in photography and film

exciting things w o u l d be going on w i t h i n camera range. He gave in at times a n d some of these u n s c r i p t e d h a p p e n i n g s greatly enriched the film. 'Signals' was first t r a n s m i t t e d in 1968 a n d in 1969 it w o n the prestigious Italia Prize for television documentaries. O n the heels of this international recognition, Niko was a p p r o a c h e d by the BBC a n d Time/Life w h o w a n t e d to make a series of half-hour television programmes on animal behaviour to be called 'Behaviour and survival'. They w a n t e d Niko to supervise the series a n d m a k e as m a n y of the p r o g r a m m e s as he could. In the end, Niko did little filming for this series, a l t h o u g h some of the films u s e d old material d a t i n g back to the Ravenglass days. Niko wrote, edited a n d directed the filming of three of these p r o g r a m m e s , 'The mussel specialist', 'Tracking', a n d an i n t r o d u c t o r y p r o g r a m m e . For the other ten p r o g r a m m e s he was involved in the original t r e a t m e n t a n d plan a n d t h e n came in again after filming to polish off the editing and the script. These programmes have w o r n well a n d nearly t w e n t y years later t h e y are still r u n n i n g in some television markets. They also have seen very wide educational distribution. There were two t h e m e s to which Niko frequently r e t u r n e d w h e n talking about natural history p h o t o g r a p h y a n d film making. First, he h a d a deep c o m m i t m e n t to k n o w i n g the animal well, so that his films a n d p h o t o g r a p h s , which m u s t be selective, s h o w e d an accurate picture of animal behaviour. Second, a l t h o u g h Niko h a d an extraordinary sense of pictorial b e a u t y and composition, he disdained natural history films or books which were, in his w o r d s 'pretty-pretty', with no substance. In this category he placed films which were n o t h i n g more t h a n m o n t a g e s of pictures of animals with no a t t e m p t to build a story. In all his work, the story was the important thing. His films a n d his books are scientific a n d artistic works, but they are also deftly told stories and it is for this reason that t h e y are so memorable.

REFERENCES Ennion, E. and Tinbergen, N. (1967) Tracks, Oxford University Press, Oxford. Hall, E. (1974) A conversation with Nobel Prize winner Niko Tinbergen. Psychology Today, 7, 65-80. Tinbergen, N. (1953). The herring gull's world, Collins, London. Tinbergen, N. (1958) Curious naturalists, Country Life, London. Tinbergen, N., Falkus, H. and Ennion, E. (1970) Signals for survival, Oxford University Press, Oxford.

Afterword AUBREY MANNING

This m e e t i n g h a d a strong family feeling about it. Most people attending k n e w Niko Tinbergen a n d there was a u n i q u e gathering of his old students, a l t h o u g h we sadly missed Mike Cullen w h o was such a key figure in the group for m a n y years. Our thanks go to Marian Dawkins, Tim Halliday a n d Richard Dawkins for arranging this celebratory reunion. It was particularly nice for us to be joined by members of the real Tinbergen family. It cannot always have been easy to have f a m o u s parents. The children m u s t have been gullo r p h a n s from time to time and they also h a d to put with a stream of visitors competing for their parents' attention. However, they could not fail to have recognized the esteem a n d deep affection that all our e x t e n d e d ethological family have always felt for Niko a n d Lies. Most of the papers read here included some personal reminiscence along with science. We w o u l d all acknowledge that the Tinbergen legacy had a distinctive style about it, as well as its distinctive biological content. There was the marvellous a t m o s p h e r e of 'Friday evenings' at the Tinbergens' house, for example, which provided a mixture of informality a n d rigour. Rigour m e a n t that Niko obstinately refused to let discussion move on until he h a d fully u n d e r s t o o d the a r g u m e n t a lesson I have tried h a r d to live up to w h e n the t e m p t a t i o n is just to let things go and h o p e you'll be able to work it out later. The manifestation of his style which I shall most cherish derives from vivid memories of one or two walks in Wytham, w h e n Niko came to visit my study area. He offered a spontaneous r u n n i n g commentary on the natural world a r o u n d - the timing of nectar secretion from a flower, the flight intention m o v e m e n t s of a bird, the nesting b u r r o w of a solitary bee - everything caught his eye a n d he could fit into a -

140

A fterword

p a t t e r n of life; I can call it no less. Once or twice I could s h o w him s o m e t h i n g n e w with m y bumble-bees a n d share his utter delight for a n e w insight into the w a y their world is organized. We can all underst a n d w h y he called his essay of scientific autobiography* ' W a t c h i n g a n d w o n d e r i n g ' - this latter w o r d to be taken in both senses. As we k n o w , he was m o d e s t in a most extreme way, a n d he r e m a i n e d g e n u i n e l y a m a z e d at the prestige he c o m m a n d e d in the world of science. D e s m o n d Morris recounts h o w w h e n the Nobel Prize was a n n o u n c e d , his first response was a s t o n i s h e d m o d e s t y but with an immediate a f t e r t h o u g h t - 'it'll be g o o d for e t h o l o g y ' . Of course it was, but t h r o u g h Niko himself, for it was he w h o led the ethological approach into its fullest maturity. So m a n y of his ideas have entered into our w a y of t h i n k i n g as all the papers in this v o l u m e bear evidence. We were s a d d e n e d by the d e a t h of Lies just a few days before our meeting. All of us r e m e m b e r t h e m together. Lies w o r k e d with h i m in the early days in Greenland, she was there at every Friday evening (often with the most telling interjections) a n d t h e y collaborated for their later research on childhood autism. W h e n e v e r I visited them over these past few years we always talked about this work which t h e y did together. Their c o m m e n t a r y was as lively (and often acerbic!) as ever a n d this is h o w I shall r e m e m b e r them. In that autobiographical essay, Niko wrote 'But w h a t m e n in m y position can truly say is that they have been privileged to have lived in such an interesting time and to have witnessed a n d assisted both in the birth, or rather the rebirth, and the coming-of-age of a fascinating n e w branch of biology.' Here is the characteristic m o d e s t y again, but people in our position recognize h o w privileged we have been to be m e m b e r s of that generation w h i c h has learnt from h i m directly. We are all beneficiaries of The Tinbergen Legacy.

* Tinbergen, N. (1985) Watchingand wondering, in Studying animal behavior: autobiographies of the founders (ed D.A. Dewsbury) University of Chicago Press, Chicago and London, pp. 431-63.

Index

Acanthodis curvidens 110 Acanthops falcata (dead-leaf

Arachnura melanura (flower-

mantid) 110 Adaptation 9 Addictive drugs 91

Aspiridia galli, courtship signals

Agelychnis callidryas (red-eyed tree frog) 109 Aggression causation of 40-4 external stimuli 41-2, 45 interactions between other motivational systems and 43-4, 47~9 internal organization 42-3, 45-9 in man 33-4, 35 in spiders 53 territorial, exaggerated 91 AIDS 92 ambivalent behaviour 61 Ammophila (digger wasp), reproductive behaviour 12 Amphibia, calls in 66 Analogies 102-3 Andersson, M. 20 Angmagssalikmut Eskimos 9 Anti-displays 120 Aposematism 120 Apus apus (swift) 21

mimicking spider) 109 in 67 Assessment 56 Attack and escape behaviour 14, 61 Autism, childhood 31, 33, 35, 36, 140 Autonomic responses 61 Batesian mimicry 120 Behavioural comparisons and taxonomic relationships 117-18 Behavioural culture 76 Behavioural ecology, difference from ethology 27-8 Behavioural evolution, descriptive reconstructions 106-22 Bioevolution and culture 75-8 Biological kin 94 Bird of paradise 94 Black-box analysis 14, 17 Black-headed gull 20 choking in chicks 52-3 egg camouflage 106 eggshell removal 19, 21, 23, 135

142

Index

film of courtship 134 lesser 136 Blackbirds, mobbing behaviour 80 Blest, David 106 Blurton Jones, N. 31 Boschma, Professor H. 8 Bowerbirds 66, 95 Brooke, Michael 28 Caerostris tuberculata (stick-

mimicking araneid spider) 109 Camouflage 106-13 Carrion crow, search image in 135 Caterpillars, counter shading and stick mimicry 106 Cats 79 Causation 9, 19 and function 55-7 modern studies of 51-7 of displays 43 Cebus monkeys 94 Cephalopods display 118-20 eye in 102 Cervus elaphus (red deer), maternal behaviour 22 Chaffinches 93 Child behaviour 32 Cichlid fishes agonistic behaviour in 52 fights between 51 pre-spawning behaviour, model for 48 Cocks, fighting, displacement pecking in 47 Coevolution 64, 65, 69 Commensalism 85, 89 Communication modern view of 64-72 Tinbergen/Lorenz view of 61-4 Comparative studies in ethology 103-6 in evolutionary biology 100-3 and evolutionary insights

118-22 evolutionary, problems 122-4 Competition 93 for best sexual partners 95 Conditioning 77, 80, 87 Conflict theory 15, 52 of the causation of agonistic displays 43-4 criticism of 47 Conflicts of interst 23-4 Convergences 102-3 Cooperation 23 Cooperative behaviour 93 Cooperative signals 23, 65 Courtship signals 63 Covert learning 88 Crying response of babies 84 Crypsis 21, 117, 120 Cuculus canorus (cuckoos) 28, 64, 65, 67 Cullen, Esther 134 Cullen, Mike 139 Cultural evolution 92-6 Cultural kin 94 Culture behavioural 76 and bioevolution 75-8 and social learning 78-81 Culturegenes 84 Dabbling ducks 104 Darwin, Charles 101, 103, 122 Dawkins, Richard 64, 102 Blind Watchmaker, The 101 De Levende Natuur 2 Defensive adaptations 106-13 Derived activities 61 Description by consequence 33 Design 64 Development 19 Direct fitness 25 Disinhibition hypothesis 47 Displacement activities 15, 47, 61 Display 14 causation of 43 evolution 62 limited repertoire of 118-20

Index suppression of 120-1 threat 67 Doryphora punctissima 121 Ducks, dabbling 104 Eastern meadowlark 70 Edmunds, M.: Defence in Animals 120 Education, h u m a n 35, 36-7 Elk 94 Energy models 45-6 Erithacus rubecula (robin) 21 Eskimos 9, 37 Ethology comparative studies 103-6 difference from behavioural ecology 27-8 Eucrypsis 107, 120 Euplectes progne (widowbirds) 20 Evolution 19 behavioural 106-22 cultural evolution 92-6 Evolutionary biology, comparative studies 100-3, 122-4 Evolutionary change 64 Evolutionary stable strategies, theory of 20 Exploratory play 35 Fabre 12 Faeces mimicry 107 Falkus, H u g h 135, 137 Ferton 12 Fireflies 64 Fitness consequences of behaviour 20, 23 direct 25 indirect 25 Fixed action patterns (FAP) 13, 14 Flight 102-3 Founder effect 93 Frequency dependence 65 Function 19, 64

143

Game theory models 14, 51, 56, 67, 68 Gannet 136 Gazelles, stotting in 66 Genes 83-4 and learning 78 meme symbioses 84-9 selection and culture 77 Great tits, signals in 68 Greylag goose, egg-retrieving activity 13 Group formation in man 34 Group selection 23 Haan, Beirens de 12 Hamilton, W.D. 20 Handicap principle 67 Hardy, Alister 133 Heimans, E. 1, 2, 3 Heinroth 104 Helping at the nest 23, 24-7 Herring gull 9, 104 chicks, food pecking in 12 egg-shell removal 19 films of 133 Hierarchical model 55 Hinde, R.A.: Animal Behaviour 56 Hippopotamus, pygmy, tail hairs in 101-2 Homologies 102-3 Honest signals 66, 67, 72 H o n e y bees, homing behaviour 8 Horned beetles 122 Howard 12 Hulshorst 5, 12 H u m a n s see Man Huxley, Julian 9, 12, 61, 104, 133 Hypothetico-deductive method 103 Indirect fitness 25 Individual differences 21-2 Industrial melanism 106, 134 Influenza viruses 92 Innate behaviour 77 Innate releasing mechanism (IRM) 13, 15, 32

144

Index

Insight learning 78, 88 Instinct 9, 14, 31 Instrumental learning 77 Intention movements 61 Jungle fowl, courtship 63 Kettlewell, Bernard 106 Kittiwakes 20, 132, 134 Kiihn 12 Lack, David 21, 31 Language 81 Larus ridibundus see Black-headed gull Leg concealment 111-13 Lehrman 15 Lesser black-backed gull 136 Linnaeus 102 Lorenz, Konrad 13-14, 19, 31, 75-6, 104 Macaque, Japanese 79 Man aggression 33-4 celibacy in 91 child behaviour 32-3 commensal memes in 90 cultural altruism 93-4 cultural evolution and behaviour 75 education 35, 36-7 instinct in 31 language 81 memes, success of 95-6 social learning 80-1 territorialism 34 warfare 35 Mankin 94 Mastophora sp. 115 Mastophora dizzydeani (bolas spider) 116 McFarland 55-6 Feedback Mechanisms in Animal Behaviour 50 Meadowlark, eastern 70 song perception 71

Melanerpes formicivorous (acorn woodpeckers) 25-6 Melanism, industrial 106, 134 Meme definition 83 gene symbioses 84-9 and menobiology 81-4 parasitic 89-92 Memory, long-term 82 Menobiology and memes 81-4 Merops bullockiodes (white fronted bee-eater) 25 Mimicry 106-13 Batesian 120 faeces 107 in insects 107-12 plant-part 120 stick 106, 107, 109-12 Mitochondria 85 Molion muelleri 121 Morris, Desmond 31, 140 Moynihan, Martin 104 Muslims 94 Mutualism 85 Myxomatosis 91 Nederlandse Jeugdbond voor Naturrstudie (NJN) 2, 3, 11 Nelson, Bryan 136 Octopus displays 119 Orb-weaving spiders, behavioural evolution in 113-16, 117-18 Orchids 94 Ordigarius 115 Oystercatcher 79, 135-6

Paelyphenomenon 124 Pannadannis sp. 112 Parallelisms 102-3 Parasitism 85-6 Parrots 80 Parus major (great tit) 21 Pasilobus sp. 115, 116 Peacock 63, 95 Pelkwijk, Jan Joost ter 10-11

Index Peppered moth 134 Phalaropes, red-necked 9, 132 Philanthus triangulum (digger wasp), nest-orientation 5, 10 Phyllium 109 Phylogeny 14 Physalaemus colorandum, song 69 Physalaemus pustulosis, song 69 Pigeons brain and memory in 82 learning 79 learning of breeding sites 78 Plant-mimicry in insects 109, 120 Poecilopachys sp. 115, 116 Portielje, Frits 12 Potoo 109 Poulton, Professor E.B. 106 Predator-prey interaction 106 Prisopus berosus 109 Protective responses 61 Protocultures 77 Provisioning rules 24 Prunella modularis (dunnocks) 26-7, 28 Pterinoxylus spinulosus (stick insect) 107, 111 Ptilinoryhchus violaceus (satin bower bird) 66 Punctuationism 101 Pygmy hippopotamus, tail hairs in 101-2 Rabbits, myxomatosis 91-2 Rabies virus 85-6, 91 Ranatra (water stick-insect) 109, 111 Ray wings 102-3 Receiver psychology 69, 70 Red deer, threat signals in 68 Red jungle fowl 67 Red-necked phalaropes 9, 132 Redirected activities 61 Reed-warblers 64 Resource holding potential 67 Rissa tridactyla see Kittiwakes Ritualization 63, 65 Rutten, Elisabeth see Tinbergen, Lies

145

Scatophaga stercoraria (dungfly) 21 Schierbeek, Dr A. 3 Selfish gene altruism principle 64, 89-90 Selous 12 Sepiotheuthis sepiodea (reef squid) 120 Sequential Assessment Game 56 Serengeti Research Institute, Tanzania 17 Sevenster 14 Signals 63-4 cooperative 23, 65 courtship 63 design 69 function of 67 honest 66, 67, 72 non-cooperative 65 threat 63, 67, 68 Signals for Survival (film) 136, 138 Skates 103 Snow bunting 9, 132 Social behaviour 23-4 Song cultural nature of 80 design in 68-9, 70 imprinting 88 memory 76 perception 71-2 repertoire 70-1 as species-isolating mechanism 75-6 Space-State model of motivation 54, 55 Speciation 93 Spiders aggression in 53 courtship and mating behaviour 116 orb-weaving 113-16, 117-18 prey-wrapping behaviour 113-15 web structure 115 Stage beetles, horns in 122 Stick mimicry 106, 107, 109-12 Sticklebacks see Three-spined sticklebacks

146

Index

Suckling reflex 84 Survival value of behaviour 20 Symbiosis 87, 89 Territorialism in humans 34 Thijsse, Jac P. 1, 2, 3 Threat signals 63, 67, 68 Three-spined stickleback 9, 14 aggression in 41-2 films of courtship 133 sand digging in 44 Thrush nestlings, begging in 12 Tijmstra, G.J. 3 Tilapia mariae (reef fish) 46 Tinbergen, Niko Aims and Methods in Ethology 49, 100 Animal in its World, The 104 'Behaviour, systematics and natural selection" 105 Curious Naturalists 130, 132 'Functional ethology and the h u m a n sciences' (Croonian lecture) (1972) 31, 36, 37 Herring Gull's World, The 18, 19, 130, 132 'On war and peace in animals and man' 31, 33, 40 Signals for Survival 132

Social Behaviour in Animals 20 Study of Instinct, The 41, 104 Tracks 132 Watching and Wondering 140 Tinbergen, Lies 9, 132, 140 Tinbergen, Lukas 3, 5, 11 Trade-offs 21 Unitary drive theories 45, 46 Van der Klaauw, Professor C.J. 9, 13 Van Iersel 14 Van Veen, Karel 16 Variety 64 Verkade 2 Verwey, Albert 5 Verwey, Jan 4-5, 104 Viruses influenza 92 rabies 85-6, 91 Vogelwarte Rossitten 4 Von Frisch, Karl 8, 12-13 Von Uexkiill 12 Wagtails, mobbing action 23 Whitman 104 Woodpeckers, chick feeding by male 25-6, 27