Advances in the Study of Behavior, Volume 9

Advances in

THE STUDY OF BEHAVIOR VOLUME 9

Contributors to This Volume MARY D. SALTER AINSWORTH MEI-FANG CHENG F. REED HAINSWORTH LYSA LELAND GASTON RICHARD R. V. SHORT THOMAS T. STRUHSAKER LARRY L. WOLF

Advances in

THE STUDY OF BEHAVIOR Edited by JAY S. ROSENBLATT Institute of Animal Behavior Rutgers University Newark, New Jersey

ROBERTA. HINDE Medical Research Council Unit on the Development and Integration of Behaviour University Sub-Department of Animal Behaviour Madingley, Cambridge, England COLINBEER Institute of Animal Behavior Rutgers University Newark, New Jersey MARIE-CLAIRE BUSNEL Laboratoire de Physiologie Acoustique Institut National de la Recherche Agronomique Minist2re de 1’Agriculture Jouy en Josas (S. et O.),France

VOLUME 9

ACADEMIC PRESS

New York San Francisco London

A Subsidiary of Harcoun Brace Jovanovich, Publishers

1979

COPYRIGHT @ 1979, BY ACADEMIC PRESS, INC. ALL RIGHTS RESERVED. N O PART O F THIS PUBLICATION MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM OR BY ANY MEANS, ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING, OR ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITING FROM T H E PUBLISHER.

ACADEMIC PRESS, INC.

11 I Fifth Avenue, New York. New York 10003

Uirited Kitrgdoin Editiori prrblished by ACADEMIC PRESS. INC. ( L O N D O N ) LTD. 24/28 Oval Road, London'NW1 7DX

LIBRARY OF CONGRESS CATALOG CARD NUMBER: 64-803 1 ISBN 0-12-004509-5 PRINTED IN THE UNITED STATES OF AMERICA

79808182

9 8 7 6 5 4 3 2 1

Contents .............................................. Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Contents of Previous Volumes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lisr of Contributors

vii

ix xi

Attachment as Related to Mother-Infant Interaction MARY D . SALTER AINSWORTH I.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I1. Procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

111. Findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 6 10 38 49

Feeding: An Ecological Approach F . REED HAINSWORTH AND LARRY L . WOLF I. I1. 111. IV . V. VI .

Introduction: Feeding as an Economic Problem . . . . . . . . . . . . . . . Some Determinants of Costs and Benefits .................... The Economics of Food Choice ............................ Feeding Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Economics of Patch Exploitation ........................... Synopsis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

53 56 60 68 73 88 89

Progress and Prospects in Ring Dove Research: A Personal View MEI-FANG CHENG I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1. Major Features of Reproductive Behavior in the Ring Dove . . . . . 111. Hormones and Behavior: Lehrman’s Hypotheses . . . . . . . . . . . . . . V

97 98 98

vi

CONTENTS

IV . New Directions ......................................... V . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References .............................................

118 123 124

Sexual Selection and Its Component Parts. Somatic and Genital Selection. as Illustrated by Man and the Great Apes R . V . SHORT I. I1. I11. IV . V. VI .

The Concept of Sexual Selection ........................... Reproduction in the Gorilla ............................... Reproduction in the Orangutan ............................. Reproduction in the Chimpanzee ........................... Reproduction in Man . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . General Conclusions ..................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

131 135 139 143 147 152 155

Socioecology of Five Sympatric Monkey Species in the Kibale Forest. Uganda THOMAS T . STRUHSAKER AND LYSA LELAND I. I1. I11. IV . V. VI . VII .

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Summary of Ecology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Time Budget . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Social Organization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Social Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . General Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

159 162 162 166 177 201 218 223

Ontogenesis and Phylogenesis: Mutual Constraints GASTON RICHARD I. I1. I11. IV . V.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Toward a Model of Ontogenesis ........................... Toward a Model of Phylogenesis ........................... Mutual Constraints between Ontogeny and Phylogeny . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Subjectlndex

..................................................

229 234 249 264 267 269 279

List of Contributors Numbers in parentheses indicate the pages on which the authors’ contributions begin.

MARY D. SALTER AINSWORTH, Department of Psychology, University of Virginia, Charlottesville, Virginia 22901 ( 1 ) MEI-FANG CHENG, Institute of Animal Behavior, Rutgers-The sity, Newark, New Jersey 07102 (97)

State Univer-

F. REED HAINSWORTH, Department of Biology, Syracuse University, Syracuse, New York 13210 (53) LYSA LELAND,* New York Zoological Society and The Rockefeller University, New York, New York (159) GASTON RICHARD, Formerly, Laboratoire d Ethologie, Universite de Rennes, Rennes-Cedex, France (229) R. V. SHORT, MRC Unit of Reproductive Biology, 2 Forrest Road, Edinburgh, Scotland ( I 31) THOMAS T. STRUHSAKER, * New York Zoological Society and The Rockefeller University, New York, New York (159) LARRY L. WOLF, Department of Biology, Syracuse University, Syracuse, New York 13210 (53)

*Present address: P.O. Box 409, Fort Portal, Uganda, East Africa. vii

This Page Intentionally Left Blank

Preface The study of behavior is attracting the attention of ever-increasing numbers of zoologists and comparative psychologists in all parts of the world, and is also becoming increasingly important to students of human behavior in the psychiatric, psychological, and allied professions. Widening circles of workers, from a variety of backgrounds, carry out descriptive and experimental studies of behavior under natural conditions, laboratory studies of the organization of behavior, analyses of neural and hormonal mechanisms of behavior, and studies of the development, genetics, and evolution of behavior, using both animal and human subjects. The aim of Advances in the Study of Behavior is to provide workers on all aspects of behavior an opportunity to present an account of recent progress in their particular fields for the benefit of other students of behavior. It is our intention to encourage a variety of critical reviews, including intensive factual reviews of recent work, reformulations of persistent problems, and historical and theoretical essays, all oriented toward the facilitation of current and future progress. Advances in the Study ofBehavior is offered as a contribution to the development of cooperation and communication among scientists in our field.

ix

This Page Intentionally Left Blank

Contents of Previous Volumes

Volume 1

Vdume 3

Aspects of Stimulation and Organization in ApproacWithdrawal Processes Underlying Vertebrate Behavioral Development T. C. SCHNEIRLA

Behavioral Aspects of Homeostasis D. J. McFARLAND Individual Recognition of Voice in the Social Behavior of Birds C. 0. BEER

Problems of Behavioral Studies in the Newborn Infant H. F. R. PRECHTL

Ontogenetic and Phylogenctic Functions of the Parent-Offspring Relationship in Mammals LAWRENCE V. HARPER

The Study of Visual Depth and Distance Percep tion in Animals RICHARD D. WALK

The Relationships between Mammalian Young and Conspecifics Other Than Mothers and Peers:A Review Y.SPENCER-BOOTH

Physiological and Psychological Aspects of Selective Perception GABRIEL HORN

Tool-Using in Primates and Other Vertebrates JANE VAN LAWICK-GOODALL

Current Problems in Bird Orientation KLAUS SCHMIDT-KOENIG

Author IndexSubject Index

Habitat Selection in Birds P. H. KLOPFER and J. P. HAILMAN Author IndexSubject Index

Vdume 4

Volume 2

Constraints on Learning SARA J. SHETTLEWORTH

Psychobiology of Sexual Behavior in the Guinea h3 WILLIAM C. YOUNG

Female Reproduction Cycles and Social Behavior in Primates T. E. ROWELL

Breeding Behavior of the Blowfly V. G. DETHIER

The Onset of Maternal Behavior in Rats, Hamsters, and Mice: A Selective Review ELAINE NOIROT

Sequences of Behavior R. A. HINDE and J. G. STEVENSON

Sexual and Other Long-Term Aspects of Imprinting in Birds and Other Species KLAUS IMMELMA”

The Neurobehavioral Analysis of Limbic Forebrain Mechanisms: Revision and Progress Report KARL H. PRIBRAM Age-Mate or Peer Affectional System HARRY F. HARLOW

Recognition Processes and Behavior, with Special Reference to Effects of Testosterone on Persistence R. J. ANDREW

Author IndexSubject Index

Author Index-Subject Index

xi

xii

CONTENTS OF PREVIOUS VOLUMES

Volume 5

Volume 7

Some Neumnal Mechanismsof Simple Behavior KENNETH D. ROEDER

Maturation of the Mammalian Nervous System and the Ontogeny of Behavior PATRICIA S. GOLDMAN

The Orientational and Navigational Basis of Homing in Birds WILLIAM T. KEETON The Ontogeny of Behavior in the Chick Embryo RONALD W. OPPENHEIM Processes Governing Behavioral States of Readiness WALTER HEILIGENBERG

Functional Analysis of Masculine Copulatory Behavior in the Rat BENJAMIN D. SACHS and RONALD J. BARFIELD Sexual Receptivity and Attractiveness in the Female Rhesus Monkey ERIC B. KEVERNE

Time-sharing as a Behavioral Phenomenon D. J. McFARLAND

Prenatal Parent-Young Interactions in Birds and Their Long-Term Effects MONICA IMPEKOVEN

Male-Female Interactions and the Organization of Mammalian Mating Patterns CAROL DIAKOW

Life History of Male Japanese Monkeys WKIMARU SUGIYAMA

Author Index-Subject Index

Feeding Behavior of the Pigeon H. PHILIP ZEIGLER

Volume 6 Specificity and the Origins of Behavior P. P. G. BATESON The Selection of Foods by Rats, Humans, and Other Animals PAUL ROZIN

Subject Index

Volume 8 Comparative Approaches to Social Behavior in Closely Related Species of Birds FRANK McKINNEY

Social Transmission of Acquired Behavior: A Discussion of Tradition and Social Learning in Vertebrates BENNETT G. GALEF, JR.

The Mluence of Daylength and Male Vocalizations on the Estrogen-Dependent Behavior of Female Canaries and Budgerigars, with Discussion of Data from Other Species ROBERT A. HINDE and ELIZABETH STEEL

Care and Exploitation of Nonhuman Rimate Infants by Conspecifics Other Than the Mother SARAH BLAFFER HRDY

Ethological Aspects of Chemical Communication in Ants BERT HOLLWBLER

Hypothalamic Mechanisms of Sexual Behavior, with Special Reference to Birds J. B. HUTCHISON

Filial Responsiveness to Olfactory Cues in the Laboratory Rat MICHAEL LEON

Sex Hormones, Regulatory Behaviors, and Body Weight GEORGE N. WADE

A Comparison of the Properties of Different Reinforcers JERRY A. HOGAN and T. 1. ROPER

Subject Index

Subject Index

Advances in

THE STUDY OF BEHAVIOR VOLUME 9

This Page Intentionally Left Blank

.

ADVANCES IN THE STUDY OF BEHAVIOR VOL . Y

Attachment as Related to Mother-Infant Interaction MARYD . SALTER AINSWORTH DEPARTMENT OF PSYCHOLOGY UNIVERSITY OF VIRGINIA CHARLOTTESVILLE. VIRGINIA

1. Introduction . . . . . . . . . . . A . Attachment The0 B . Aims of the Study . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I1 . Procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . Subjects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Data Collection . . C . Data Analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D . The Strange Situation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E . Statistical Procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . Developmental Changes . . . . . . . . . . . . . . . . . B . Individual Differences in Infant Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . C . Individual Differences in Maternal Behavior ....................... D . Within-Quarter Interrelationships among Infant Behaviors . . . . . . . . . . . . E . Within-Quarter Interrelationships among Maternal Behaviors . . . . . . . . . . F . Within-Quarter Interrelations between Maternal and Infant Behaviors . . . G . Cross-Quarter Correlations of Maternal and Infant Behaviors . . . . . . . . . . H . Relationship of Infant Behavior at Home to Attachment Patterns in the Strange Situation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I . Relationship of Maternal Behavior at Home to Infant Attachment Patterns Assessed in the Strange Situation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . J . Interpretative Summary of Findings .................... IV . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . Three Views of Direction of Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B . Direction of Effects i n a Limited Time Period C . Direction of Effects over Several Periods of Time . . . . . . . . . . . . . . . . . . . D . Discussion of Findings in Light of the Above Considerations . . . . . . . . . . E . Practical Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 2 5 6 6 6 7 8 9 10 11

14 15

17 20 20 26 31 34 36 38 39

40 41 44 47 49

.

Copyright @j 1Y7Y by Academic Press Inc . All lights of reproduction in any form reserved . ISBN 11- 12-004509-5

2

M A R Y D. SALTER AlNSWORTH

I.

INTRODUCTION

For many years 1 have been investigating the development of a baby’s attachment to his mother and the ways in which this development is related to the kinds of interaction he has experienced with her. The study upon which this chapter is based was begun in 1963, and deals with a sample of white, middle-class families living in the Baltimore area. It has been a short-term longitudinal study, based on naturalistic observation of the mother-infant dyad in the familiar environment of the home, supplemented by one session in a controlled laboratory situation. The project as a whole was designed both to elucidate general trends of development of infant-mother attachment during the first year of life and to explore individual differences in this development. In this chapter we shall be concerned chiefly with individual differences in attachment and attachment behavior as they are related to differences in maternal behavior in interaction with the infant. Before stating our aims in more detail we need briefly to consider the theoretical background of the study. A.

ATTACHMENT THEORY

In general, the theoretical background of our work has been Bowlby’s (1958, 1969, 1973) ethological-evolutionary theory of attachment to which, indeed, our own empirical findings and theoretical discussions have contributed ( A h w o r t h , 1969, 1972, 1973, 1977a; Ainsworth P I d., 1978). Infant-mother attachment is conceived as an affectional tie that a baby forms to his mother figure, binding them together in space and enduring over time. Such bonding is not present at birth, but develops during the first year of life. The process of becoming attached is supported by a number of species-characteristic behaviors that have emerged in the course of evolution because they afforded survival advantage in the “environment of evolutionary adaptedness.” These behaviors have in common the predictable outcome of promoting and/or maintaining contact and/or proximity to conspecifics, and particularly to the principal caregiver who indeed is most usually the mother. Because of this common, predictable outcome such behaviors may be classed together as “attachment behavior.” Indeed. it is useful to consider behavior thus classed together as constituting a behavioral systemin this case the attachment behavioral system. The biological function of both attachment behavior and attachment is hypothesized to be protection. Some attachment behaviors are present at or soon after birth. Among these Bowlby distinguished two classes: signaling behaviors, such as crying and smiling, that promote proximity by attracting an adult to approach, and other more active behaviors, such as sucking, rooting, and grasping, through which the infant on his own account gains or maintains contact. These early behaviors are conceived as fixed-action patterns, each with its own causes of activation and termination.

ATTACHMENT AND MOTHER-INFANT INTERACTION

3

Attachment behavior undergoes four main kinds of change in the course of development. (1) The range of stimuli activating and/or terminating the behavior in question becomes progressively narrowed, so that attachment behavior becomes increasingly focused on one or a few familiar figures rather than being emitted without discrimination as to figure. (2) The behavior itself is altered in form, becoming increasingly complex and differentiated. (3) Some speciescharacteristic proximity/contact promoting behaviors, not present in the newborn, emerge in the course of development, for example, reaching, clinging, and locomotor approach. (4) Attachment behavior, initially consisting of several more or less separate fixed-action patterns, comes increasingly to act as an organized system. One feature of this system is that attachment behavior becomes increasingly "goal-corrected, " i.e., directed by the infant intentionally toward his "set-goal" of proximity to or close contact with his attachment figure, and continuously corrected by feedback during the course of action until the setgoal is attained. Bowlby (1969) suggested that there are at least five classes of conditions that may combine to cause a behavioral system to become active, some of these specific and some general. Among the specific causal conditions are specific environmental stimuli, and equally important, the way in which the behavioral system is organized in the central nervous system. Hormonal state may also have a fairly specific effect. Among the more general causal conditions are the level of activation of the CNS and the total stimulation impinging on the organism at the time. In the earliest months, each separate attachment behavior seems to have its own specific conditions for activation, but later, as the attachment system becomes more organized centrally, it tends to be activated as a whole. When this degree of internal organization has been achieved, it is possible to list conditions likely to affect the activation of the attachment system, some intraorganismic and some external. Among the intraorganismic conditions are illness, pain, fatigue, and hunger. Among the external conditions are the locus and behavior of the attachment figure (whether present or absent, departing or returning, responsive or unresponsive, accepting or rejecting), the locus and behavior of other persons including strangers, the presence or absence of alarming stimuli, and the degree of familiarity versus strangeness of the situation in general. Furthermore, our research has led us to hypothesize (Ainsworth et al., 1978) that the specific behaviors that are deployed when the attachment system is activated are related to the intensity of the activation. This intensity is also elated to the current setting of the set-goal of the system. Thus it is congruous with a low intensity of activation to have the set-goal merely to establish or to maintain interaction with an attachment figure across a distance, for example, by smiling or vocalizing. In contrast, when the system is activated at a high level of intensity, the set-goal is likely to shift to a specification of close bodily contact, so that a baby may scurry quickly to his mother, clamber up, and cling tightly, or scream urgently, signaling her to come to him. Which of these two alternatives is selected

4

MARY D. SALTER AINSWORTH

would seem to depend on the baby’s confidence in being able quickly in this situation to reach his mother under his own “steam. Whereas the various attachment behaviors of the very young infant are but loosely organized together, even as early as the second half of the first year attachment behavior begins to become organized in a hierarchical pattern in accordance with “plans” (Miller et al., 1960). This increasing organization has several implications. (1) Different proximity-promoting behaviors may serve as alternative means of achieving the set-goal which guides the plan. (2) Specific behaviors become, like Piaget’s (1936) “mobile schemata,” available to serve as means to a variety of ends. Thus a behavior may come to serve a variety of behavioral systems. For example, locomotor approach obviously serves several other systems, as well as the attachment system, and signaling behavior, such as smiling, may promote interactions with persons other than attachment figures. (3) Individual differences in the way in which the attachment system becomes organized are influenced by differences in experience, especially differences in the feedback or consequences of the various deployments of attachment behavior. Thus the ways in which attachment in any given individual becomes organized with reference to a specific attachment figure largely depends on the history of that individual’s interaction with that figure. It is implicit‘in the concept of behavioral systems that no one system is in a continuous state of activation. On the contrary, the activity of such systems alternates. At one time one system may be active and thus determine overt behavior, and another at another time, depending on the relative conditions of activation of the systems in question. Of particular interest in infancy is the balance between the attachment and exploratory system. When conditions for activation of attachment behavior are absent or at a low level and conditions for activation of exploratory behavior are present, the infant is very likely to turn fmm his mother figure to engage in exploratory play. We have referred to this as “the use of the mother as a secure base from which to explore” (Ainsworth, 1967). It is nevertheless implicit in this concept that any conditions that activate attachment behavior more strongly than exploratory behavior is activated will result in cessation of exploration and efforts to establish proximity to or contact with the mother. It is generally acknowledged that the relatively long period of infantile helplessness characteristic of humans provides the conditions necessary for adaptation to a wide range of environmental variation-for flexibility and learning. At the same time it implies a long period during which the young child is vulnerable and needs protection. It may thus be seen that the protective functior. of attachment behavior and reciprocal maternal behavior dovetails with the flexibility associated with a long infancy. Furthermore, it may be seen that ‘t would be maladaptive for attachment behavior to be continuously at a high lev of activation. It is only when attachment behavior is terminated, i.e., the set-goal for proximitykontact attained, that the infant is open to stimuli instigating exploration. ”

b

ATTACHMENT AND MOTHER-INFANT INTERACTION

5

One of Bowlby’s theoretical points is that in the course of evolution a system of maternal behavior developed that is reciprocal to infant attachment behavior; Hinde (1976) would call it complementary. It too has the predictable outcome of proximity promotion or maintenance and the function of protection of the infant. It is reasonable to assume that infant attachment behavior and reciprocal maternal behavior are preadapted to each other. Thus, we suggest, one major aspect of the environment of evolutionary adaptedness for infant attachment behavior is not merely a mother figure but one who is sensitively responsive to infant behavioral cues. Bowlby suggested that, to the extent that the present environment of rearing departs from the environment to which a baby’s behavior is preadapted, behavioral anomalies may be expected to occur. It is within theoretical framework that we view the role that an infant’s interaction with his mother plays in influencing the qualitative nature of his developing attachment to her.

B.

AIMSOF THE STUDY

The project as a whole had five major aims, which may be summarized as follows; (1) to identify the various behaviors that may be classed together as attachment behavior and to trace their development, (2) to describe how these behaviors become organized together and focused on the mother figure, thus determining the nature of the infant’s attachment to her, (3) to describe individual differences in the development of attachment behavior and the organization of attachment, (4) to ascertain how environmental influences, and in particular the behavior of the mother figure, affect this development, and (5) to investigate the relationship between infant-mother attachment and other aspects of development, both cognitive and social. In this chapter, the focus is on aims (3) and (4), although it is impossible entirely to omit consideration of findings relevant to the other aims of the study. Let us here consider in somewhat more detail the two aims to which we shall direct most of our attention. Because of our emphasis upon the organization of behavior, we are concerned not merely with the behaviors that compose the attachment system considered separately but also with the identification of stable patternings of behavior. This interest in patterns of attachment behavior is reflected not only in the ways in which we chose to analyze the relationships among the behavioral measures, but also to some extent in the measures that were themselves chosen in an early stage of data reduction. One of the first sets of data analysis to be completed was that concerned with behavior in a laboratory situation at the end of the first year, a situation we termed “the strange situation.” Individual differences in the way in which strange-situation behavior was patterned were very conspicuous, and led to the classification of infants in accordance with these patterns. As our analysis of infant behavior at home gradually proceeded, it became apparent that behavior

6

MARY D. SALTER AINSWORTH

also was patterned. Furthermore it became evident that patterns of home behavior were related in such a way to the strange-situation classifications that one could interpret both as reflecting patterns of the organization of the infant’s attachment to his mother. The analyses of maternal behavior at home proceeded concomitantly with the comparable analyses of infant behavior at home. As might be expected, maternal and infant behavior at any one time in our data analysis were found to be closely related. Furthermore, individual differences in behavior of the mothers in interaction with their babies throughout the first year appeared to be closely related to individual differences in the nature of babies’ attachment to their mothers at the end of this period. In Section IV we shall discuss the issue of direction of effects, that is, the effect of the baby on his mother’s behavior versus the effect of the mother on her baby’s behavior and develoment, and the belief will be asserted that the effects are reciprocal, each influencing the other. Nevertheless, data will be presented that support the conclusion that deep-seated patterns of maternal behavior do indeed have a strong influence on the way in which an infant’s attachment to his mother becomes organized. 11. PROCEDURES Although this chapter is based upon the findings reported in other publications, it seems helpful here briefly to summarize and to comment upon the main

features of our procedures. The reader is referred to the other publications for details. A.

SUBJECTS

The subjects were 26 mother-infant pairs from white, middle-class families i n the Baltimore area, originally contacted through pediatricians in private practice, usually before the baby’s birth. Sixteen of the babies were boys; 10 were girls. Ten of the babies were first born, all of them boys. All but four of the infants were bottle-fed from the beginning. Only four of the mothers had employment outside the home at any time during the baby’s first year, and only one of these worked fulltime. B.

DATACOLLECTION

Data were collected in the course of visits to the home occurring at three-week intervals from 3 to 54 weeks after the baby’s birth, each visit lasting approximately 4 hours. When the baby was 51 weeks old, the infant and his mother were introduced to a laboratory situation, the strange situation, which will be de-

ATTACHMENT AND MOTHER-INFANT INTERACTION

7

scribed later. During the home visits the visitor-observer made detailed notes of the behavior of the infant, especially when in interaction with his mother or with others, and in addition recorded as much as possible of what the mother and other members of the household did and said. These notes were subsequently transcribed into a typed narrative account. The length and frequency of the visits tended to minimize the interference implicit in the presence of an observer, as the mother (and also, later the baby) became accustomed to the visitor and behaved naturally. This effect was enhanced by the fact that the visitor was responsive to overtures from both mother and baby in such a way that he or she evinced friendly interest in the persons in the household rather than seeming merely to observe and to record what they did and said. Furthermore, the frequency and length of the visits promoted the derivation of relatively stable measures from the data, by normalizing day-to-day and even hour-to-hour variations in behavior. C.

DATAANALYSIS

Although narrative reports, such as those that constitute our raw data, preserve fairly detailed sequences of interaction, they do not yield ready-made measures of behavior. A major task has been to devise ways in which the narrative data might be reduced into manipulable, quantitative terms. One solution, anticipated from the outset, was to identify certain commonly recurring everyday situations in which attachment behavior was most likely to be activated, and in which the absence of such behavior might be noteworthy. These “critical” situations included: situations in which the baby is picked up, and perhaps held, and then put down (Ainsworth et al., 1972; Blehar et al., 1978); face-to-face encounters (Blehar et a l . , 1977); and situations in which a person leaves the room in which the baby is situated, and subsequently reenters it (Stayton et al., 1973, Stayton and Ainsworth, 1973). In each of these situations behavior of both partners was coded. In addition, some behaviors were coded whenever they occurred, for example, crying (Bell and Ainsworth, 1972; Ainsworth and Bell, 1977) and locomotor approach behavior (Tracy e f al., 1976). Finally, in the course of these analyses further behavioral variables, whether of mother or infant, suggested themselves as worthy of special coding and derivation of measures, for example, maternal behavior in the feeding situation (Ainsworth and Bell, 1969), maternal commands and infant obedience (Stayton et al., 1971), and a variety of maternal and infant behaviors especially relevant to the distinction of mother-avoidant babies from securely attached infants and from mother-resistant infants (see below) (Main, 1977; Blehar e f al., 1978). These analyses provided a large number of measures of behavior. Many of these are straightforward measures of frequency or duration of easily identified behaviors, for example, how often and how long an infant cries, or how often a

8

MARY D. SALTER AINSWORTH

mother picks her baby up, and for how long she holds him. Other measures focus on qualitative aspects of the behavior, for example, how contingently the mother responds to infant behavior in face-to-faceencounters, how tender and careful she is in handling her baby when in physical contact with him, or to what extent a baby responds to the return of his mother after an absence with greeting behavior that can be identified as positive or negative. Some of the qualitative measures reflect the fact that attachment behaviors may to some extent be interchangeable. Thus, for example, a baby may greet his mother upon her return after an absence by smiling, vocalizing, bouncing, reaching or leaning toward her, or approaching her; any of these, separately or in combination, was identified as positive greeting behavior. Even these qualitative behavioral categories were translated into frequency or duration measures, for example, the percentage of mother-entersroom episodes in which a baby greeted her positively, or the percentage of total holding time in which the mother handled her baby tenderly and carefully. In addition to coding of behaviors, a number of 9-point rating scales were devised for the assessment of maternal behavior, a notable feature of which was detailed behavioral identification of the five odd-numbered anchor points. For both ratings and measures derived from the codings, data were pooled so that all visits occurring in any one quarter on the first year yielded one score. D. THESTRANGESITUATION

As a supplement to longitudinal observation of mother-infant interaction in the home environment, a laboratory situation was devised. This situation provided situational control of the intensity of activation of the attachment-behavioral system. It consisted of eight episodes, all but the first of which lasted three minutes. After a brief introductory episode, mother and baby were alone in a room featuring a massive display of toys. Attachment behavior which might have been aroused by an unfamiliar environment was opposed to exploratory behavior activated by the attractive toys. In the next episode a stranger entered, thus possibly activating attachment behavior at a somewhat higher intensity, but also introducing a conflict between warinesdfear of the stranger and friendly, affiliative behavior directed toward her. Then followed a separation episode, in which the mother left the baby with the stranger: this was intended to activate attachment behavior still more intensely. It was expected that this high level of activation would carry over into the reunion episode which followed, before proximity or contact with the mother could terminate attachment behavior. Then followed a second separation, in which the baby was first left alone and then was again with the stranger, before the mother finally returned. It was expected that the effect of this sequence of episodes would be cumulative, with the highest level of intensity of activation of attachment behavior occumng during the second separation and reunion.

ATTACHMENT AND MOTHER-INFANT INTERACTION

9

Individual differences in behavior in this standardized situation were found to reflect individual differences in the nature of the infant’s attachment to his mother, an interpretation supported by the discovery of systematic and significant relationships between the infants’ patterns of strange-situation behavior and both infant and maternal behavior at home during the first year of life and subsequent social and cognitive development. [Ainsworth et al. (1978) not only reported the relevant findings of this study, but also reviewed the investigations of a number of others most of which confirmed andor extended the former.] Infants were classified into three main groups on the basis of the patterning of their strange-situation behavior. The objectivity of the classification together with the behavioral dimensions that figured prominently in the classificatory system were confirmed by a multiple discriminant function analysis. Originally the groups had been labeled A, B, and C, but after an examination of the nature of the differences between these groups both at home and in the strange situation, more descriptive labels were also assigned. The infants of Group B were identified as securely attached. In the strange situation high-intensity activation of attachment behavior, as expected, resulted in increased efforts to gain and to maintain interaction, proximity, andor contact with the mother, especially in the reunion episodes, accompanied by little or no avoidant or resistant behavior. The infants of Group C also showed intensified proximitykontact seeking, but simultaneously displayed angry, resistant behavior in the reunion episodes. They were identified as anxiously attached and resistant. The infants of Group A were particularly interesting. In the reunion episodes they showed little or no proximity/contact seeking, but instead actively avoided interaction with or proximity to the mother, and hence were identified as anxious and avoidant. How these strange-situation patterns are related to behavior at home constitutes one of the sets of findings that will be discussed in this chapter.

E. STATISTICAL PROCEDURES Correlational techniques, including multivariate correlational techniques, are the chief resource of naturalistic studies for assessing the degree of relationship between conditions of rearing and subsequent infant development, especially when the sample of infants studied has not been specifically chosen to represent two or more conditions of rearing. The well-known defect of correlation is that neither a simple coefficient of correlation nor elaborate multivariate statistics indicate direction of effects. Thus, in the case of a significant correlation between maternal and infant behavior, it is not possible to assert whether maternal behavior influenced infant behavior, or infant behavior influenced maternal behavior, or they influenced each other reciprocally, or, indeed, whether both were influenced by some other factor not represented in the correlation itself.

10

MARY D. SALTER AINSWORTH

The issue of direction of effects in interactional research is further complicated by the fact that in any one episode of interaction between two individuals each is likely to affect the behavior of the other, at least to some extent. (The reciprocal influence cannot produce a perfect correlation, however, because the behavior of the partner is only one of the determinants of the behavior of each member of the dyad.) To complicate matters even more, the measures of maternal and infant behavior may themselves be confounded, as is inevitably the case in frequency and duration measures relevant to infant crying and maternal response to it (Bell and Ainsworth, 1972; Ainsworth and Bell, 1977). Nevertheless, it seems reasonable that the direction of effects might be sorted out if one could demonstrate that the behavior of the mother at time 1 was more closely related to the behavior of the baby at time 2 than the behavior of the baby at time 1 is related to the behavior of the mother at time 2. Cross-lag correlational methods have been applied for the solution of this kind of problem, but unfortunately they are unlikely to yield significant results except with samples very much larger than those characteristic of naturalistic studies (Kenny, 1975). Nevertheless, we have based part of our argument for direction of effects on matrices of cross-quarter correlations, despite the fact that cross-lag methods were not suitable for our data (Bell and Ainsworth, 1972; Blehar et al., 1978). However, we place our confidence for a solution to this problem not so much on statistical manipulation of any one given correlational matrix but in the kind of convergent research and analysis that is characteristic of construct validation (Cronbach and Meehl, 1955). This implies that no definitive answer may be found in any one piece of data analysis, nor indeed within any one research project, but rather that it is inference from a number of different data analyses and a number of different research projects, which, converging upon the same kinds of conclusions, builds up confidence in the probability that the combination of results may be attributed neither to chance nor to some common and overlooked variable. Experimental studies with other primate species, cross-cultural studies, or other experiments of opportunity, naturalistic or seminaturalistic studies with other samples, and analysis of a variety of aspects of mother-infant interaction within any one such study all offer grist for the construct validation mill. In this chapter the focus is only on a variety of aspects of mother-infant interaction analyzed for one sample of dyads. 111. FINDINGS In this section the findings of our various data analyses will be summarized, beginning with a brief consideration of developmental changes in infant behavior during the first year and with concomitant changes in maternal behavior. Then individual differences in infant and maternal behavior as manifested in the home

ATTACHMENT AND MOTHER-INFANT INTERACTION

11

environment, first separately and then as they relate to each other will be considered. Finally, the relationships of both infant and maternal behavior at home to the patterns of infant-mother attachment inferred from infant behavior in the strange situation will be discussed. A. DEVELOPMENTAL CHANGES Since this chapter is not primarily concerned with development, only brief mention will be made of those changes in infant and/or maternal behavior that seem necessary as a background for the other findings presented here.

I . Infant Crying and Maternal Response to It The frequency of infant crying remained constant on the average throughout the first year, although the duration of crying decreased, especially from the first to the second quarter. During the first quarter babies were most likely to cry when the mother was not nearby, but in the fourth quarter when the mother was in proximity but not in actual bodily contact. From this we (Bell and Ainsworth, 1972) concluded that crying is at first expressive, undiscriminating, and activated by the condition of being alone (as well as by conditions such as hunger and pain), but that toward the end of the first year crying may sometimes be a mode of communication directed specifically to the mother and hence most likely to occur when near to her. In regard both to the number of episodes ignored and the duration of maternal unresponsiveness to crying, mothers on the average became somewhat more responsive from the first to the fourth quarter. Bell and Ainsworth (1972) also examined the nature and effectiveness of various maternal interventions in response to infant crying. Throughout the first year the most common maternal response was to pick the baby up, and this intervention was effective in terminating crying in more than 80% of the instances. Feeding, although much less frequent, was almost equally effective. The least effective intervention, merely talking to the baby or attempting to interact with him, nevertheless terminated crying in about half its occurrences. 2. Behavior Relevant to Close Bodily Contact

We used categorical measures of infant behavior when in close bodily contact rather than attempting to deal with discrete behaviors (Blehar et al., 1978). We coded as positive response to being picked up and held: postural adjustment (i.e., cuddling or sinking in), smiling, and later on also more active behaviors such as clinging, embracing, and scrambling. Negative responses to being held included crying, restlessness, and later pushing away, hitting, and the like. Positive responses were relatively infrequent in the first quarter, but increased in the second and third quarters, only to decline somewhat in the fourth; whereas negative responses, initially occumng as often as positive responses, declined slightly in

12

MARY D. SALTER AINSWORTH

the course of the year. It was our impression that a substantial proportion of negative responses in the first quarter were due either to acute hunger or gastric distress. It seems that at first there is a period of mutual adjustment between mother and baby during which positive responses to close bodily contact are relatively infrequent, followed by a six-month period during which a number of mother-infant pairs achieve harmonious interaction in regard to contact (but by no means all do so), followed in turn by a period (the fourth quarter) in which close bodily contact seems less important to the baby than it was earlier. In the first quarter it was fairly common for a baby to respond negatively to being put down after having been picked up, crying, or later, otherwise signaling a protest. A positive response to being put down was very rare in the first quarter, increased to about 30% of the put-down episodes in the second and third quarters, and then showed a striking increase to over 60% in the fourth quarter. We checked what babies did after having responded positively to being put down in the fourth quarter, and found that in about half of the episodes they moved off into independent exploratory activity, one indication of an increasing tendency to move away from the mother to explore the environment. We also coded initiations of being picked up and being put down (i.e., active initiations rather than signals), but these were uncommon even in the fourth quarter. There were substantial changes in maternal behavior relevant to close bodily contact in the course of the first year; it appeared that these could, on the whole, be attributed to maternal response to developmental changes in the infant. The time that the average mother and baby spent in close bodily contact decreased from a mean of 20 minutes per infant waking hour in the first quarter to less than 6 minutes per hour in the fourth. Likewise the mean duration of contact reflected in the latter measure was largely attributable to a decrease in holding the baby while feedinghim. (The babies in this sample, none of whom were breast-fed in the fourth quarter, showed strong interest in feeding themselves, managing their own bottles and finger foods and resisting any attempt to hold them during feeding if this involved restraint of their self-feeding attempts.) Although the duration of holding decreased, the mean frequency of episodes of contact remained fairly constant throughout the first year, at approximately 3 episodes per hour. Let us turn to the qualitative aspects of maternal behavior, considering first what we have termed “tender, careful holding”-behavior characterized both by a gentle muting down of the mother’s usual speed and vigor of movement and by pacing of her handling to the infant’s tempo of responding. There were wide individual differences in the proportion of holding time in which the mother behaved tenderly and carefully, but on the whole this proportion had declined by the fourth quarter. There seems little doubt that the relative helplessness of the baby during his first few months tends to evoke slow and gentle handling in the case of the average mother, whereas the older, stronger, and more lively and competent the baby becomes the less often he evokes this kind of handling. (This

ATTACHMENT AND MOTHER-INFANT INTERACTION

13

constitutes an example of the way in which mothers respond to infants’ developmental cues.) Maternal holding behavior was identified as inept when it was particularly insensitive to the baby’s behavioral cues, involving, for example, picking him up abruptly, handling him roughly and without regard to his comfort, or handling him in a grossly inappropriate manner. This was relatively rare with most mothers, and declined on the average throughout the first year. Other qualitative measures were the percentages of pick-up episodes in which the mother behaved affectionately, playfully, or interferingly. Affectionate behavior, defined in terms of kissing, hugging, or caressing, did not occur often among most of the mothers in this sample and changed little in incidence in the course of the year. Playful behavior likewise was not very frequent, although it was more common in the second quarter than either earlier or later on. Interfering pick-ups were not even scored until the third quarter, for it is only when an infant is well-enough developed to be engaged in active manipulative or locomotor activity that he may be described as having a goal-corrected activity in progress, with which his mother can interfere. 3 . Behavior Relevant to Separation and Reunion

Here we were concerned with infant response to mother’s leaving the room and to her subsequent return (Stayton et al., 1973). We dealt only with the last three-quarters of the first year because, earlier, babies tend not to respond to mother’s coming and goings as such, but only to initiation or cessation of close bodily contact or face-to-face encounters. Mothers left the mom at a mean frequency of 3.4times per infant waking hour, with little change across time. We coded two infant responses to these brief everyday separations: crying and following. When we eliminated consideration of episodes in which a baby was left alone and those in which he was put down just before his mother departed, we found the median onset of crying in response to separation to be 22 weeks of age, a finding essentially the same as that for a sample of Ganda infants (Ainsworth, 1967, 1977b). After this onset, however, such protest at first occurred in a very small proportion of leave-room episodes. A peak occurred at 33 weeks of age when the mean frequency was close to 308,followed by a decline, which was in turn followed by a second peak at 45 weeks of age followed by a second decline. [Others, such as Schaffer and Emerson (1964) and Mahler et al. (1975) have found yet another peak in the second year of life.] One may assume that the departure of an attachment figure is interpreted differently by children at various stages of cognitive development. In all quarters, however, we found the baby more likely to protest when left alone rather than in the company of another person, even though that person was the relatively unfamiliar visitor-observer. We estimated the median age of the onset of following at 31 weeks, substantially later than the onset of crying. Following is obviously tied to the emergence of locomotion. Three weeks after the onset of crawling, babies who were free to

14

MARY

D.

SALTER AINSWORTH

follow did follow their mothers in 16% of leave-room episodes, but within another three weeks they did so in 49%, much more consistently than they cried. Responses to the mother’s return after an absence were classified into three categories (in addition to no response): positive greeting, crying, and mixed greeting. Responses characterized as positive included smiling, vocalizing, bouncing, reaching, leaning toward, approaching, and waving. The median age of onset of positive greeting was 16 weeks; substantially earlier than the onset of separation protest. In the last half of the first year, positive greetings occurred on the average in nearly one-third of enter-room episodes. During the second quarter, positive greetings were limited to smiling, vocalizing, and bouncing, with other forms emerging in the third quarter. Crying in greeting occurred but rarely, so it was combined with mixed greetings-those in which both crying and some form of positive greeting occurred. The median age of onset for such greetings was 27 weeks, followed by no significant developmental trend in frequency. As for maternal behavior relevant to separation and reunion episodes, we considered only two, neither of which showed any noteworthy change over time-frequency of leaving the room, and acknowledging the baby upon entering the room. DIFFERENCES IN INFANT BEHAVIOR B. INDIVIDUAL 1 . Crying

The range was very wide especially in the first quarter, from 21 minutes per waking hour to almost no crying at all, and from 10 episodes per hour to fewer than 2. Stability of individual differences was tested by a matrix of cross-quarter correlations. None of the coefficients was significant, except for that between the third and fourth quarters, for both frequency of crying episodes and for duration of crying ( r s = .43 and .39 respectively). The fact that the amount a baby cried in the first quarter bore no relationship to the amount he cried later on suggests that early differences in imtability fail to persist to a significant degree. It is not until the second half of the first year that the amount a baby cries seems to become a moderately stable individual characteristic (Bell and Ainsworth, 1972). 2.

Behavior Relevant to Close Bodily Contact

The range of individual differences in behavior relevant to close bodily contact was wide and remained wide throughout the first year. For example, one baby responded positively in 90% of the episodes in which his mother picked him up in the first quarter, whereas another was never observed to do so. (All infants were found capable of a positive response, however, to the visitor if not to the mother.) The range for negative response to being held was not quite as wide, but even so it was from 0 to between 41% and 60% across the four quarters. For positive response to being put down the range was relatively narrow in the first

ATTACHMENT AND MOTHER-INFANT INTERACTION

15

quarter but widened later on. For negative response to being put down the range was wide throughout. Again the matrices of cross-quarter correlations showed no stability from the first quarter to later quarters in regard to any of the above-mentioned measures. Positive response to holding did, however, become remarkably stable later on. (For example, the correlation coefficient between second- and third-quarter behavior was 30,and that between second- and fourth-quarter behavior .72). Both negative response to being picked up and positive response to being put down were fairly stable from the second to the fourth quarter. Responding negatively to being put down did not seem to become a stable individual characteristic however (Blehar et al., 1978). 3 . Behavior Relevant to Separation and Reunion

Second-quarter separation protest was not significantly related to third- or fourth-quarterdistress; this behavior does not appear to become even moderately stable until the second half of the first year. Positive greeting to the mother when she entered the room showed somewhat more stability, since fourth-quarter behavior was significantly related to both second- and third-quarter behavior. Crying and mixed greetings, probably because they occurred so rarely, yielded no significant cross-quarter correlations (Stayton and Ainsworth, 1973). 4 . Behavior in Face-to-Face Encounters Blehar et al. (1977) examined face-to-face interaction from 6 to 15 weeks, and tested for stability of individual differences by comparing scores for the visits at 6 and 9 weeks with those at 12 and 15 weeks. No significant correlations were found.

5 . Summary The trends are fairly consistent in regard to all of these measures of infant behavior, namely, that early individual differences do not tend to persist but that by the second half of the first year they become moderately stable. Exceptions tend to be behaviors that occur too rarely for an adequate sample of them to be obtained in any one quarter.

c.

INDIVIDUAL

DIFFERENCES IN MATERNAL BEHAVIOR

I . Response to Infant Crying

The range of individual differences in responsiveness to crying was very wide, especially in the baby’s first quarter. The least responsive mother ignored 97% of her baby’s cries in the first quarter, whereas the most responsive mother ignored only 3%. There was also a wide range in our durational measure of maternal unresponsiveness, which was the number of minutes per hour that a baby cried

16

MARY D. SALTER AINSWORTH

without or before any intervention from his mother. The stability of the measures of responsiveness-unresponsiveness was much greater than the stability of the measures of amount of infant crying. This was particularly so in the case of the durational measure. (see Table I; Bell and Ainsworth, 1972). 2. Behavior Relevant to Close Bodily Contact Again, the range of all measures of maternal behaviors was wide, and for most it changed but little in the course of the first year. In the case of five measures there was an impressive degree of stability throughout the first year, total holding time, mean duration of a pick-up episode, frequency of pick-ups, affectionate pick-ups, and inept holding. Maternal behavior characteristic of the baby's first quarter tends to persist throughout the first year. Three measures did not show the same degree of stability, however, and require comment. Tender, careful holding tended to be stable throughout the first three quarters, but there was no significant correlation between this behavior in the fourth quarter and any earlier quarters. We have already suggested that by the fourth quarter babies do not usually require this kind of handling. Mothers who were especially sensitive to infant developmental cues therefore tended to reduce the amount of tender, careful holding, although others continued their previous practice even though it was no longer especially appropriate; thus earlier behavior was inconsistent with fourth-quarter behavior in a number of instances. Playful behavior in the second quarter is substantially related to behavior in the third, but each is essentially unrelated to behavior in either the first or fourth quarters. In the first quarter most babies are relatively unresponsive to maternal playfulness while being held, and consequently mothers who are sensitive to developmental cues tend not to be playful then, even though they are playful later TABLE I

CONSISTENCY OF MATERNAL RESPONSIVENESS TO CRYING THROUGHOUT

FIRSTYEAR:

DURATION OF MOTHER'S UNRESPONgVENESS TO CRYING"

Quarters of first year Quarters of first year First Second Third

Second

Third

Fourth

.39b -

.33

.49" .69" .49"

.58"

-

aFrorn Bell and Ainsworth (1972). bp < .05. "p < .01.

ATTACHMENT AND MOTHER-INFANT INTERACTION

17

on. In the fourth quarter, much mother-infant play occurs in contexts other than close bodily contact, for example, chasing games and peek-a-boo; some mothers who played with the baby while holding him in earlier quarters continued to do so in the fourth quarter, whereas other mothers tended to stress play in other contexts. Finally, there was no significant stability in the percentage of pick-up episodes that were devoted to nonroutine interaction, probably because this measure included two quite independent kinds of nonroutine pick-ups-those undertaken to soothe a crying baby (predominant in the first half of the first year), and those undertaken for purely social interaction (more common in the second half) (Blehar et al., 1978). 3. Behavior in Face-to-Face Encounters Scores for visits atl6 and 9 weeks were correlated with scores for visits at 12 and 15 weeks. Of eight measures of maternal behavior, six showed significant stability, ranging from a coefficient of 3 9 for contingent pacing to infant behavioral cues to one of .80 for liveliness of stimulation. 4 . Summary

On the whole, measures of maternal behavior showed impressive stability throughout the periods examined, and thus differed from the measures of infant behavior which showed little stability until the second half of the first year.

D. WITHIN-QUARTER INTERRELATIONSHIPS AMONG INFANT BEHAVIORS Two analyses have been undertaken of the interrelationships among infant behaviors: (1) interrelationshipsamong behaviors relevant to close bodily contact within each of the four quarters (Blehar et al., 1978) and ( 2 ) interrelationships among crying, separation, and reunion behaviors, and behaviors relevant to close bodily contact in the fourth quarter (Stayton and Ainsworth, 1973). In addition some inferences about the interrelation of infant behaviors in face-to-face encounters may be made from a factor analysis of both maternal and infant behaviors for the period from 6 to 15 weeks (Blehar et al., 1977). 1 . Interrelations among Behaviors Relevant to Close Bodily Contact

Table I1 shows the intercorrelations of infant behaviors within the third and fourth quarters. The most noteworthy findings are that babies who respond positively to being held tend also to respond positively to being put down, rather than negatively. Indeed the same relationships tend to hold also for the first and second quarters. Thus, even early on, babies who “cuddle in” when held, adjusting their bodies to fit in with the mother’s body, tend not to protest when

18

MARY D. SALTER AINSWORTH

TABLE I1 INTERCORRELATIONSOF INFANT BEHAVIORS WITHIN

THE

THIRDAND FOURTH QUARTERS'

Positive Negative Positive Negative Initiation Initiation to holding to holding to put down to put down to pick UP of put down Positive to holding Negative to holding Positive to put down Negative to put down Initiation of pick up Initiation of put down

-.65d .74d -.5Id -.27

-.38'*'

-

-219~ .63d -.48d .SOd

.40c -.28 -.63d .36 -.37'

-.39c .05 -.6/ -.40c .35

.42 -.29

-.25 .65

.36

-.4gd

-.25 -.34

-.07 -.30

-

'Adapted from Blehar er al. (1978). bItalicizedcoefficients in the upper right hand half of the table refer to the fourth quarter; coefficients in the lower left hand half refer to the third quarter. ' p < .05. d p < .01.

contact ceases. It is as though this experience of truly close bodily contact tends to terminate attachment behavior, and thus soon (as mentioned in Section I) allows the baby to move off into independent exploratory activity. As might be expected, Table 11 shows significant inverse relationships between opposite measures, that is, between positive and negative responses to being held and to being put down. This is not artifactual because of the use of neutral scores, an acceptance of the mother's action without either a clear-cut, positive response or a protest. It may also be seen that babies who tend to initiate pick-ups tend also to respond positively to being held; whereas babies who tend to initiate being put down tend also to respond negatively to being held. It is noteworthy, however, that babies who initiate being put down tend not to respond positively to the put-down. As we shall attempt to show later their desire to be put down does not seem to be related to a wish to get on with other activities but rather to reflect conflict about close bodily contact with their mothers. 2 , Interrelationships among Various Fourth-Quarter Behaviors Stayton and Ainsworth (1973) presented a matrix of intercorrelations among 13 fourth-quarter variables, which were then subjected to a factor analysis, the two-factor solution of which is presented in Table 111. It may be seen that the highest loading on factor I was found for crying when the mother leaves the room (.875), and that other loadings in the same direction were: frequency and duration of crying, crying and mixed greeting when mother enters the room after an absence, and also negative response to being put down. Variables with loadings in the opposite direction were: positive greetings when mother enters the room, positive response to being put down, and also positive response to being held.

19

ATTACHMENT AND MOTHER-INFANT INTERACTION

FACTOR LOADINGS

OF

TABLE I11 FOURTH-QUARTER INFANT BEHAVIORAL VARIABLES"

Infant behavioral variable

Factor I

Crying when mother leaves room Following when mother leaves room Positive greeting when mother enters room Crying and mixed greeting when mother enters Frequency of crying Duration of crying Positive response to being held Negative response to being held Stops cry when picked up Positive response to being put down Negative response to being put down Initiation of being picked up Initiation of being put down

.875 -.234 -.593 .66I .733 .719 -.344 .277 - ,059 -.534 .379 .022 . I80

Factor I1 -.I71

-. I56 -.252 -.001

.280 ,427 -.541 .63 I -.635 -.439 .I77 -,596 ,605

"Adapted from Stayton and Ainsworth (1973).

Factor I was interpreted as representing an anxiety versus security dimension of the infant's attachment to his mother. Infants who receive high scores on those variables with substantial (positive) loadings on Factor I could be described as anxious about the mother's accessibility and responsiveness. Factor I1 is clearly related to response to close bodily contact. The variable with the highest loading in one direction is negative response to being held, whereas other variables in the same direction are initiation of being put down and duration of crying. The variable with the highest loading in the opposite direction is stopping crying when picked up, which reflects capacity to be comforted by physical contact with the mother. Other variables loaded in the same direction are initiations of being picked up, positive response to being held, and positive response to being put down. We interpret Factor I1 as reflecting the degree of conflict versus enjoyment and comfort that a baby experiences in the context of close bodily contact with his mother. 3 . Interrelations among First-Quarter Face-to-Face Behaviors

In the above-mentioned factor analysis of both maternal and infant behaviors the following infant behaviors received substantial loadings on Factor I: vocalizing, smiling, and bouncing with loadings in one direction, and merely looking at the mother which had a high loading in the other direction. Another pair of infant behaviors received substantial loadings in one direction on Factor II and hence may be inferred to be positively related-fussing and terminating the episode (Blehar et al., 1977).

20

MARY D. SALTER AINSWORTH

E. WITHIN-QUARTER INTERRELATIONSHIPS AMONG MATERNAL BEHAVIORS Stayton and Ainsworth ( 1973) reported fourth-quarter intercorrelations among three sets of measures of maternal behavior: response to infant crying, behaviors relevant to separation and reunion, and four ratings of maternal behavior. The four ratings were: sensitivity-insensitivity to infant signals and communications, acceptance-rejection, cooperation-interference, and accessibility-ignoring. [The first of these scales was appended in complete form to the chapter by Ainsworth et al. (1974). Brief descriptions of this and the other three scales were provided also by Ainsworth et al. (1971) and by Stayton and Ainsworth (1973).] The durational measure of maternal unresponsiveness to infant crying was significantlybut negatively related to all four sets of ratings, although the number of crying episodes ignored was significantly and negatively related only to sensitivity-insensitivity and to cooperation-interference. The consistency with which mothers acknowledged their babies upon entering the room after an absence was significantly and positively related to all four sets of ratings. The two measures of unresponsiveness to infant crying were positively related, as might be expected, but do not tap precisely the same variable ( r = .54). The frequency with which a mother left the room was significantly associated with rejection and interference;and also with the number of crying episodes ignored. The four sets of ratings were themselves highly intercorrelated, due to the fact that mothers who are sensitive to signals are neither rejecting, interfering, nor ignoring, but mothers rated as rejecting are not necessarily interfering and ignoring, and so on. Consequently, as shown by Stayton and Ainsworth (1973), they have different patterns of relationships with other maternal variables. Blehar et al. (1978) undertook for each quarter intercorrelations and factor analyses of maternal behavior relevant to close bodily contact. Blehar et al. (1977) did likewise for maternal behavior in face-to-face interaction. Those will not be reported here for they yielded essentially the same information as did the factor analyses of maternal and infant behavior which are discussed in the next section. INTERRELATIONS BETWEEN MATERNAL AND F. WITHIN-QUARTER INFANT BEHAVIORS 1 . Behavior Relevant to Close Bodily Contact

A two-dimensional plot of factor loadings for the first-quarter analysis are shown in Fig. 1. Factor I, represented on the horizontal axis, is a bipolar factor defined at one pole by maternal, tender, careful holding, the behavior that receives the highest positive factor loading. In the opposite direction the maternal behaviors that receive the highest loadings are: inept holding and frequency of

21

ATTACHMENT AND MOTHER-INFANT INTERACTION

-

Factor

.-VE

Factor I 1

TO P/D.INEPT .NEGATIVE

1

1

1

1

1

1

JI

HOLDING

.POSITIVE

TO HOLD 1

.

1

1

1

1

.

TO P/D

POSITIVE TO HOLD 1

1

m

a

,

EPISODES/HRO

.TENDER CAREFUL HOLDING .PLAYFUL

MEAN DURATION OF P/U.. DURATION OF HOLDING

P/U

.AFFECTIONATE

P/U

~

FIG. I . Factor loadings of first-quarter maternal and infant behaviors relevant to close bodily contact.

pick-up episodes. Factor 11, represented on the vertical axis, is defined by the two measures related to the duration of holding. Three measures reflecting qualitative differences in maternal behavior are also more or less heavily loaded on Factor 11: affectionate pick-ups, playful pick-ups, as well as tender, careful holding, showing that in this quarter maternal behavior of positive quality tends to be associated with longer durations of holding. It is noteworthy, however, that no infant behavior has substantial loadings on Factor 11. This suggests that individual differences in infant responses to being held and to being put down are not related primarily to differences in duration of being held. Indeed, all four measures of infant behavior fall close to the horizontal axis, and are thus closely associated with Factor I, with positive responses to being held and to being put down loaded in one direction and most closely related to tender, careful holding among all the maternal behaviors, and with negative responses to being held and put down loaded in the opposite direction, and thus related to the absence of tender, careful holding.

22

MARY D. SALTER AINSWORTH

We shall not show a plot for the second-quarter factor analysis since maternal and infant behaviors cluster much as they did before, with tender, careful holding being most closely associated with positive infant responses and inept holding being associated with negative infant responses. Frequency of pick-up episodes was associated with negative infant behaviors, more strongly than in the firstquarter analysis, and was inversely related both to the positive maternal and infant behaviors but also to duration of holding. These findings deserve comment. In this sample, mothers who picked their babies up most frequently tended also to put them down again quickly. These brief episodes tended to involve abrupt, jerky maternal behavior-the reverse of the slow, gentle behavior that we have labeled as tender and careful-and gave the baby little opportunity to adjust his posture to his mother before he was put down again. In the third quarter the interaction between qualitative and quantitative features of maternal behavior disappears, as may be seen in Fig. 2. It may be noted that almost all the qualitative maternal variables and all of the infant variables align Factor 1 '1

*INTERFERINQ P/U

Factor

I

POSITIVE O t V E TpYLq* ,

, ,

, ,

*PLAYFUL I

F P/U

*TENDER CAREFUL *INIT. P/U *AFFECTIONATE P/U

* I N I T . P/D

I

t

I

I

I

1

*EPiSOOES/MR 0-VE

I

,

,

INEPT *-VE TO HOLO T O P/D

t 0 DURATION OF HOLDINQ P/U DURATION

FIG.2. Factor loadings of third-quarter maternal and infant behaviors relevant to close bodily contact.

ATTACHMENT AND MOTHER-INFANT INTERACTION

23

themselves close to the horizontal axis which represents Factor I, and thus have negligible loadings on Factor 11, which is a quantitative factor defined at one pole by measures of duration of contact. The infant variables defined the bipolar Factor I, with positive response to being held receiving the heaviest loading toward one pole, and likewise negative response to being held at the other pole. Positive response to being put down as well as initiations of being picked up cluster with all the positive maternal behaviors, again with tender, careful holding receiving the heaviest loading among these. Negative response to being put down clusters with the same negative maternal behaviors as before-inept holding and frequency of pick-up episodes. We shall not report the fourth-quarter factor analysis in any detail. As in the first two quarters, the qualitative and quantitative aspects of maternal behavior interact to some extent, this time with the total duration of holding being somewhat associated with negative, rather than with positive, infant and maternal behaviors. It is suggested that this is because by the fourth quarter those mothers who hold their babies for long periods are those who are still holding them while feeding them-a practice that was obviously over-restraining and frustrating to the babies in the sample. Otherwise much the same kinds of relationships among behaviors hold for the fourth quarter as previously, except that tender, careful holding receives somewhat lighter loadings on the qualitative factor than it did before and that the mean duration of nonroutine pick-up emerges with substantial loadings both toward the positive pole of Factor I and the long duration pole of Factor 11. In summary, within each quarter of the first year, and especially from the second quarter onward, we find strong relationships between infant behavior relevant to close bodily contact and qualitative aspects of maternal behavior. Although there is some interaction between duration of holding and quality of holding, except in the third quarter, it seems to be more important how a mother holds her baby than how much she holds him, at least within the durational limits represented in this sample. Furthermore, there is a strong thread of consistency in the findings from one quarter to another, despite some change in the details of the interrelations (Blehar et al., 1978). 2 . Infant Crying and Maternal Responsiveness There are high positive correlations between infant crying and maternal unresponsiveness to it, in regard to both frequency and durational measures, in each quarter of the first year. These are spuriously high, however, since the measures themselves are confounded. For example, the length of time that elapses before a mother responds to a cry is included in the measure of duration of the infant’s crying. Bell and Ainsworth (1972) provided a correction for these confoundings of measures. When the corrections were employed, the within-quarter correlations between maternal and infant behavior still tended to be substantial, except

24

MARY D. SALTER AINSWORTH

for the first quarter, when they approached zero. The corrections changed the implications of the measures however. Ainsworth and Bell (1977) have concluded that there is no satisfactory way to correct for the confounding of the within-quarter measures of amount of infant crying and maternal responsiveness-unresponsiveness to it. Bell and Ainsworth did, however, assess the effectiveness of maternal interventions and its relationship to the amount of infant crying. Crying was judged to have terminated if 2 minutes elapsed without a renewal. The measure of maternal effectiveness was the inverse of the number of interventions offered before the criterion of termination was reached. The comparable infant measure was the number of crying clusters emitted, a cluster being defined as a series of crying episodes separated by gaps of less than 2 minutes. These measures are not confounded, for each can vary independently of the other. Nevertheless, within each quarter of the first year, it was found that the more interventions it took for a mother to terminate crying, the more crying clusters were emitted by the baby. This really implies that mothers who did not read their babies’ behavioral cues well enough to find an appropriate intervention tended to have babies who cried more than others. It also implies that even interventions that terminated crying for 2 minutes were not equally effective in preventing renewal of crying soon afterward.

3 . Behavior in Face-to-Face Interaction Blehar et al. (1977) reported a three-factor solution of a factor analysis of maternal, infant, and dyadic measures of face-to-face interaction for the period from 6 to 15 weeks inclusive. The factor loadings of the various measures are shown in Table IV. One pole of Factor I is defined by maternal “routine manner”, a matter-of-fact kind of behavior often characteristic of mothers when face-to-face with their babies during routine care. Other maternal behaviors loaded in the same direction are silent, unsmiling initiation of interaction and abruptness. Associated with these is the infant response of merely looking at the mother when she initiates interaction. The opposite pole of Factor I is defined by maternal playfulness. Contingent pacing by the mother is also loaded in the same direction, as is the dyadic measure of “ensuing interaction,” that is, interaction proceeding beyond the initial stimulus-response sequence. All of the positive infant behaviors, vocalizing, smiling, and bouncing, are associated with these maternal behaviors. Maternal variables with high loadings on Factor I1 are contingent pacing and “encouragement of further interaction,” which involved contingent pacing, but further involved the gradual increase of intensity and pace of stimulation as the baby became more responsive. The dyadic variable of ensuing interaction is also associated with these maternal behaviors. The one infant behavior with substantial loading in the same direction is bouncing, which may be viewed as an

ATTACHMENT AND MOTHER-INFANT INTERACTION

25

TABLE IV OFINFANT, MATERNAL, AND DYADIC MEASURES OF FACE-TO-FACE INTERACTION= FACTOR LOADINGS Factor loadings Type of measure

Behavioral measure

I

I1

Maternal Infant Maternal Maternal Dyadic Maternal Infant Infant Maternal Maternal Infant Dyadic Infant Infant Maternal

Routine manner Merely looking Silent, unsmiling initiation Abruptness Brief episode Mother terminates episode Fussing Baby terminates episode Encouraging interaction Contingent pacing Bouncing Ensuing interaction Smiling Vocalizing Playfulness

.70 .67 .53 .41 .34 .25 .I5 -.03 -.24 -.43 - .44 -.46 -.47 -.49 -.62

.47 .I9 .I6 .47 .52 .45 .64 .45 -.52 -.74 -.55 -.58 -.08 -.02 -.09

III

.25 .09

.25 .09 .5 I

-.03 .I5 -.09

-.57 -.01

- .09

-.28 -.36 -.38 -.I2

'From Blehar er al. (1977).

expression of excitement and delight. The opposite pole of Factor II is defined by infant fussing, with infant termination of the episode loaded in the same direction. Maternal behaviors associated with these are: routine manner, abruptness, and maternal termination of the episode. Not surprisingly, the dyadic measure brief episode is also substantially loaded in the same direction. Thus Factor I1 seems to be concerned with variables that make for a prolonged interaction in which the infant is delighted as contrasted with a brief episode in which affect is relatively negative. (We shall not discuss Factor 111 which seems solely concerned with the length of the interaction without considerations of affect.) 4 . Behavior Relevant to Separation and Reunion

Stayton and Ainsworth (1973) examined the relationships between infant responses to separation and reunion in the fourth quarter and the various maternal variables mentioned earlier (Section 111, E). Separation distress (i.e., crying when mother left the room) was positively related to both measures of maternal unresponsiveness to crying and negatively related to maternal sensitivity to infant signals. Following the mother when she left the room was positively related both to maternal accessibility (versus ignoring) and to sensitivity to infant signals. Positive greeting to the mother when she returned was positively related to maternal sensitivity to signals, cooperation (versus interference), and acceptance

26

MARY D. SALTER AINSWORTH

(versus rejection), and negatively related to both measures of maternal unresponsiveness to crying. Crying and mixed greetings were not significantly related to any of the maternal variables, possibly because they were too infrequent for reliable measures to have been obtained. It may be noted that neither the frequency with which the mother left the room nor the frequency with which she acknowledged the baby upon returning were related significantly to any of the infant separation and reunion behaviors. Since crying when mother left the room defined the anxious pole of the anxiety versus security dimension discussed in Section 111, D, 3, and positive greetings defined the secure pole, it seems justifiable to infer that maternal behavior associated with secure infant-mother attachment is characterized by sensitive responsiveness to infant signals, including crying, whereas unresponsiveness to such signals is associated with anxious attachment. 5. Behavior Relevant to Infant Obedience

Stayton et al. (197 1) identified two measures of infant obedience, compliance to mother’s verbal commands and internalized controls, which refers to selfinhibiting, self-controllingbehavior. The percentage of maternal commands with which the infant complied was significantly and positively correlated with maternal sensitivity to infant signals and communications, acceptance (versus rejection), and cooperation (versus interference), but not to the effort exerted by the mother to control the infant, as indicated by the frequencies with which she issued verbal commands or intervened physically to enforce them. Evidence of internalized control was rare in this sample of infants less than a year old, but those instances that did occur were also significantly related to the same three sets of maternal ratings. Internalized control differed from compliance to commands, however, in that it was also significantly (and more strongly) related to both infant IQ and the extent to which the mother permitted the baby to have floor freedom. Because of these relationships between maternal and infant behvior, we prefer to refer to infant cooperativeness and cheerful willingness to respond to maternal signals rather than to continue to use the terms obedience and compliance which imply a passive kind of conformity to parental controls. G. CROSS-QUARTER CORRELATIONS OF MATERNAL AND INFANT BEHAVIORS So far, we have undertaken cross-quarter correlations of maternal and infant behaviors in respect to two areas of mother-infant interaction, necessarily attending to one pair of behaviors at a time. The first of these was concerned with infant crying and maternal unresponsiveness to it, and the second with behaviors relevant to close bodily contact.

27

ATTACHMENT AND MOTHER-INFANT INTERACTION

TABLE V CROSS-QUARTER CORRELATIONS BETWEEN EPISODES OF CRYING IGNORED BY THE MOTHER AND FREQUENCY OF CRYINGO Frequency of crying

Episodes ignored by mother First quarter Second quarter Third quarter Fourth quarter

First quarter

Second quarter

Third quarter

Fourth quarter

-

.56*

.21 .39c -

.20 .36

.w

-

.34

-

.48'

.32 .29

.21

.w

"Adapted from Bell and Ainsworth (1972). bp < .Ol. 'p < .05.

1 . Infant Crying and Maternal Unresponsiveness

The cross-quarter correlations between infant frequency of crying (number of episodes per waking hour) and the number of episodes thereof ignored by the mother are shown in Table V. It may be seen that the more episodes the mother ignores in the first quarter, the more Frequently the baby cries in the second quarter, and similarly for the relationships between second and third, and between third and fourth quarters. In contrast, the frequency with which the baby cries in the first quarter is not significantly related to how many episodes the mother ignores in the second quarter, likewise for the relationships between the second and third quarters. The frequency with which the infant cries in the third quarter is, however, significantly related to the number of episodes his mother ignores in the fourth quarter. Bell and Ainsworth (1972) interpreted these findings to indicate that maternal ignoring of crying has more effect on how often an infant subsequently cries than the frequency of infant crying has on how much the mother subsequently ignores crying; an effect that appears to be confined to the first half of the first year however. By the second half of the first year, the influences between infant and mother seem to be reciprocal. This interpretation is supported by the facts earlier reported that maternal ignoring of crying shows fair consistency throughout the infant's first year whereas frequency of crying does not seem to become a stable infant characteristic until the second half of the year. These findings were generally confirmed by the matrix of cross-quarter correlations between the duration of infant crying (measured in minutes per waking hour) and the comparable maternal measure of duration of urlresponsiveness (the number of minutes per waking hour that a baby cried before or without an intervention from his mother; see Table VI). The more unresponsive the mother

28

MARY D. SALTER AINSWORTH

TABLE VI CROSS-QUARTER CORRELATIONS BETWEEN DURATION OF MOTHER’S UNRESPONSIVENESS TO CRYING AND DURATION OF CRYING‘ ~

Duration of crying Duration of mother’s unresponsiveness

First quarter

Second quarter

Third quarter

First quarter Second quarter Third quarter Fourth quarter

-

.45b

.37 .I2 .4Ib

-

.40b .42b

.5Ic .69c

.52‘

-

Fourth quarter .32 .6Y .51r

-

‘From Bell and Ainsworth (1972). bp < .05. ‘p < .01.

is to crying in the first quarter the more the baby cries in the second quarter, whereas the amount the baby cries in the first quarter is not significantly related to how unresponsive the mother is in the second quarter. In this matrix it may be seen, however, that the correlations between the second and third, and between the third and fourth quarters are significant in both directions, as though a vicious spiral had become established. Nevertheless, it would appear that the direction of effects in the earliest months is for the mother’s behavior to affect subsequent infant behavior more than the infant’s behavior affects subsequent maternal behavior. Bell and Ainsworth (1 972) presented a third set of cross-quarter correlations between maternal effectiveness-ineffectiveness in responding to crying and the number of crying clusters per waking hour. Although (as shown in Section 111, F, 2) within each quarter the more effective the mother’s interventions the less the baby cried, there were no significant cross-quarter correlations. Specifically, the effectiveness of the mother’s interventions in any one quarter had no apparent influence on the baby’s tendency to cry later on. In conjunction with the other cross-quarter findings, the implication is that, at least in the early months, it is the promptness and consistency of a mother’s response to infant crying, not the skill with which she finds the most appropriate and effective intervention, that is associated with the relative degree of reduction of infant crying later on. 2 . Behavior Relevant to Close Bodily Contact

Blehar et al. (1978) undertook four cross-quarter correlations between maternal and infant behavior relevant to close bodily contact. The infant variables used were positive and negative responses to being held, and the maternal variables

ATTACHMENT AND MOTHER-INFANT INTERACTION

29

TABLE VII CROSS-QUARTER CORRELATIONS BETWEEN TENDER, CAREFUL

MATERNAL HOLDMGAND INFANT POSITIVE RESPONSETO BEINGHELD' Infant positive response to being held Tender, careful maternal holding

First quarter

Second quarter

Third quarter

Fourth quarter

First quarter Second quarter Third quarter Fourth quarter

-

.Sib

.28 .38 .26

.53b .69b

.67b

-

.41c

-

.25

.25

.Me

.44c

-

"From Blehar er al. (1978). bp

cp

< .01. < .05.

were those that had emerged as most closely related to infant behavior in the within-quarter factor analyses: tender, careful holding, affectionate behavior, playful behavior, and inept holding. Table VII shows the cross-quarter correlations between infant positive response to being held and tender, careful maternal holding behavior. It may be seen that the correlations between maternal behavior in each quarter and subsequent infant behavior, shown above the diagonal, are all positive and significant, and indeed that each is larger than its opposite number below the diagonal. Thus it would appear that tender, careful maternal holding facilitates the development of a positive response to being held on the part of the infant. Any tendency of a positive infant response to lead his mother subsequently to hold him more tenderly and carefully is comparatively weak. The fact that infant response in the fourth quarter is so substantially correlated with tender, careful holding in earlier quarters is particularly noteworthy, since the fourth-quarter factor analysis of infant and maternal behaviors suggested that these two behaviors were not closely associated within the fourth quarter. Table VIII yields an entirely different picture for the relationship between infant positive response to being held and the percentage of pick-up episodes in which the mother displays affectionate behavior. In neither the first nor second quarter is maternal behavior significantly correlated with infant positive response in subsequent quarters. To be sure, infant positive response to being held in the first quarter is not significantly related to later affectionatebehavior on the part of the mother, but infant behavior in the second and third quarters is significantly so related. It appears that, from the second quarter on, the more consistent the baby's positive response to contact the more likely the mother is to display

30

MARY D. SALTER AINSWORTH

TABLE VUI CROSS-QUARTER CORRELATIONS BETWEEN THE PERCENTAGE OF PICK-UP EPISODES I N WHICH MOTHERSHOWS AFFECTIONATE BEHAVIOR AND INFANT POSITIVE RESPONSETO BEINGHELD" Infant positive response to being held Percentage of pick-up episodes in which mother shows affectionate behavior

First quarter

Second quarter

Third quarter

Fourth quarter

First quarter Second quarter Third quarter Fourth quarter

-

.I3

.32 .36 .28

.22 .36

.49b .4Ib

.I9 .33 -

'

-

.51c

.44b

-

"From Blehar ef a/.(1978). bp < .05. 'p < .01.

affectionatebehavior while holding him. In conjunction with the findings of Table VII, a virtuous spiral might be hypothesized, namely that tender, careful holding by the mother early on fosters the tendency of a baby to respond positively to close bodily contact, and that this positive response encourages the mother to begin (or to continue) to show affectionate behavior. Let us merely summarize the findings of a third cross-quarter matrix that deals with intercorrelations between infant positive response to being held and playful maternal behavior. The first-quarter behavior of neither mother nor baby is significantly correlated with the subsequent behavior of the other. Playful maternal behavior in the second and third quarters is, however, significantly correlated with subsequent positive infant response to being held. (It will be recalled that maternal playfulness in the context of contact is both most frequent and seemingly most appropriate in the middle half of the first year.) The fourth cross-quarter matrix, between negative infant response to being held and inept maternal holding behavior, is remarkably like that shown in Table VI for duration of infant crying and maternal unresponsiveness. Inept maternal holding in each quarter is significantly related to a negative infant response to being held in the subsequent quarter. Negative infant behavior in the first quarter is not significantly correlated with maternal ineptness in any subsequent quarter, but such behavior in the second and third quarters i s significantly correlated with maternal ineptness. It appears as though a vicious spiral had become established by the second quarter, in which maternal ineptness of handling makes for a negative infant response, while at the same time the way the infant cries, squirms, and fails to cuddle in makes for maternal ineptness. Nevertheless it

ATTACHMENT AND MOTHER-INFANT INTERACTION

31

appears as though inept maternal behavior in the first quarter is implicated in tripping off the vicious spiral.

H. RELATIONSHIP OF INFANT BEHAVIOR AT HOMETO ATTACHMENT PATTERNS IN THE STRANGE SITUATION It will be recalled that three major patterns of behavior in the strange situation were identified in infants approximately one year of age. Ainsworth, Blehar, Waters, and Wall (1978) have reported how these are related to infant behaviors at home in both the fourth and first quarters, as well as giving a much more detailed description of the strange-situation behaviors that differentiated the three groups than the summary given here in Section 11, D. The comparisons among the three groups were done in two chief ways: by t tests of the differences between the means of the groups for the home variables, and by correlating each of the home variables with two sets of discriminant function scores for strangesituation behavior, the first of which discriminated Group A from Groups B and C, and the second of which discriminated Group C from Groups A and B. The findings for the fourth quarter will be presented first, since they refer to roughly the same phase of development as do the strange-situation findings. 1 , Fourth-Quarter Comparisons

Both groups of anxiously attached babies (Groups A and C) cried significantly more (in terms of duration) than did the securely attached babies of Group B; a finding which was largely responsible for the identification of the groups as anxiously rather than securely attached. Furthermore, the babies of the anxious, resistant group (Group C) were significantly less adept in noncrying modes of communication than were securely attached (Group B) babies. However, both frequency and duration of crying as well as low scores on communication were significantly correlated with Discriminant Function 11, (DF 11) rather than with DF I, and hence seem more characteristic of Group C than of the anxious, avoidant babies of Group A. Both of the anxious groups showed more separation distress (crying when mother leaves the room) than did the securely attached group, another behavior that links both to the anxious end of the anxiety-security dimension identified by Stayton and Ainsworth (1973; see Section 111, D, 3). In regad to following when mother leaves the room there was no difference between the securely attached and anxious, avoidant babies, but the anxious, resistant babies followed significantly less often. Again, both crying and a tendency nor to follow in everyday separation situations were significantly correlated with DF 11, and hence seem more characteristic of the anxious, resistant group (C) than of the anxious, avoidant group (A). The securely attached babies more frequently than the babies of either

32

MARY D. SALTER AINSWORTH

A or C groups greeted their mothers positively when they returned from an absence, and Group C babies more frequently than Group B (securely attached) babies cried when the mother returned. The securely attached babies, more often than the anxious babies of either Group A or C, responded positively to being held, and less often than infants of the anxious, avoidant group (A) responded negatively to close bodily contact. Of these the failure to respond positively seems more important, and judging from its substantial correlation with DF I is especially characteristic of Group A babies. By the fourth quarter most instances of being put down were responded to positively, but anxious, resistant infants did so less frequently than securely attached infants. Babies of both anxious groups, less frequently than secure babies, responded negatively to being put down, but the substantial correlation of this with DF I suggests that it is particularly characteristic of avoidant babies. I am indebted to Mary Main (Blehar et al., 1978) for analysis of our data in regard to certain physical-contact behaviors hypothesized to discriminate mother-avoidant infants (Group A) from the anxious, resistant infants of Group C. The three infant behaviors investigated were: tentative contact behaviors which resemble intention movements, sinking in when picked up, and active contact behaviors. The latter two, hypothesized to be uncharacteristic of A babies, were in fact significantly more frequent among Group B babies, and sinking in also significantly distinguished Group C from Group A. All three behaviors yielded significant correlations with DF I, the discriminant function that distinguished A from non-A infants. Main also hypothesized that angry behavior would discriminate motheravoidant babies from those of the other two groups. The data supported this hypothesis, and in addition C babies were more frequently angry than the securely attached B babies. Indeed of all the infant variables angry behavior received the highest correlation with DF I ( r = .79) and hence is the best single distinguishing feature of the behavior of mother-avoidant babies at home. This is of interest, since in the strange situation it was the anxious, resistant (Group C) babies who behaved most angrily. Finally, compliance with mother’s commands distinguished the securely attached group from each of the anxious groups, although it did not discriminate between Groups A and C. 2 . First-Quarter Comparisons

It must be pointed out that groups A and C were so small (numbering 6 and 4 infants respectively) that differences must be very sharp indeed to be statistically significant. It was assumed that the differences that subsequently distinguish Group A from Group C and each from Group B would not have developed as early as the first quarter. Therefore, for the first-quarter comparisons the Group B babies (who later were characterized as securely attached) were compared with

ATTACHMENT AND MOTHER-INFANT INTERACTION

33

Groups A and C combined (that is, with babies who later were identified as anxiously attached). It was found that Group B infants cried significantly less than A/C babies, in terms of both frequency and duration. They more often responded pqitively to being held by their mothers, and less often responded negatively to being put down. In face-to-face interaction, they less frequently made no response to their mothers’ initiations of interaction and less frequently terminated interaction.

3 . Discussion Let us refer to the two major dimensions, identified by Stayton and Ainsworth (1973), in terms of which individual differences in fourth-quarter home behavior could be described. The security-anxiety dimension does indeed discriminate between babies who in terms of their strange-situation behavior were identified as securely attached from those identified as anxiously attached. The securely attached babies (Group B) cried less than A/C babies (in both first and fourth quarters), showed less distress in little everyday separations, and more frequently greeted their mothers positively upon reunion. These were the behaviors most heavily loaded on Factor I of the Stayton-Ainsworth analysis. The second dimension of the Stayton-Ainsworth analysis (Factor 11) is believed to reflect presence or absence of conflicts relevant to close bodily contact. It is of interest to note that it was behaviors relevant to contact that were most highly correlated with Discriminant Function I, which discriminated A from non-A babies. These included: positive response to being held, sinking in, and active contact behaviors as characteristic of non-A infants, and tentative contact behaviors, characteristic of A babies. The dimensions represented by the two factors may be used to describe the characteristics of the strange-situation groups. Thus securely attached infants (Group B) not only cry little and show little separation distress at home, but they also respond more positively to close bodily contact with their mothers than other babies, more frequently sinking in and displaying active and more rambunctious contact behaviors. In general, they seem to have a more harmonious relationship with their mothers, including ways not specified by the original StaytonAinsworth factor analysis. Specifically, they are more disposed to cooperate with their mother’s commands (and wishes), and are much less often angry, presumably because their mothers frustrate them less often. Although mother-avoidant babies (Group A) are significantly more anxious than securely attached babies (Group B), crying more frequently and showing more separation distress, it is clear that anxious, resistant babies (Group C) are the most overtly anxious among the three groups. This was also the case in the strange situation, in which C babies were the most clearly disturbed, showing some distress even in the preseparation episodes, whereas Group A babies manifested the least overt disturbance. C infants seem to have less conflict about

34

MARY D. SALTER AINSWORTH

close bodily contact with their mothers than A infants; especially, they are more likely to sink in, molding their posture to fit closely with the mother’s body. Nevertheless they show some difficulty relevant to close bodily contact. In comparison with B babies, they respond less positively to being held and to being put down, less often initiate being picked up, and more often respond negatively to being put down. As we will argue later, both anxious groups are in conflict about close bodily contact with their mothers, but the conflicts experienced by the anxious, avoidant babies differ in kind from those experienced by the anxious, resistant babies. Although angry behavior was not included as a variable in the Stayton-Ainsworth factor analysis, it is clearly relevant. Both A and C babies are more frequently angry than B babies, but in the home environment anger is particularly characteristic of Group A. Finally, although because of small sample size A and C babies cannot be significantly discriminated from each other during the first quarter, it is notable that they can be discriminated from the B babies who later are identified as securely attached. They cry more, are less positive in regard to bodily contact, and respond less in face-to-face interaction with their mothers.

OF MATERNAL BEHAVIOR AT HOMETO INFANT I. RELATIONSHIP ATTACHMENT PATTERNS ASSESSED IN THE STRANGE SITUATION

I . First-Quarter Comparisons If one hypothesizes that a mother’s behavior influences the nature of her baby’s attachment to her, one would expect that the mothers of the babies in the three strange-situationgroups would differ in behavior as early as the first quarter. Mothers of babies who were later identified as anxiously attached (Groups A and C) were less responsive to crying than mothers of babies who were later identified as securely attached (Group B), although this was so only in terms of duration of unresponsiveness and not number of crying episodes ignored. Group B mothers spent a significantly greater proportion of their “holding time” in tender, careful holding than did A and C mothers, and spent less time in inept holding. B mothers also were more often affectionate when in physical contact with their babies. Main’s analysis (Blehar et al., 1978) assessed two physical-contact variables which were hypothesized to distinguish between A and C mothers-aversion to physical contact, and providing the baby with unpleasant experiences relevant to contact. Indeed, Group A mothers admitted and/or displayed aversion to close bodily contact with their babies significantly more frequently than mothers of C babies @< .OOOl), and, of course, more frequently than the mothers of B babies. Group A mothers also tended to provide their babies with unpleasant and even painful experiences in the context of close bodily contact significantly more often than non-A mothers.

ATTACHMENT AND MOTHER-INFANT INTERACTION

35

Two variables significantly distinguished B from non-B mothers in respect to first-quarter face-to-faceinteraction-contingent pacing which was characteristic of the B mothers and routine manner which was characteristic of the non-B mothers. Ainsworth and Bell (1969) undertook an examination of mother-infant interaction in the feeding situation during the first quarter. They identified four major aspects of such interaction, and concluded that in each the most important dimension of maternal behavior was the extent to which it was geared to infant behavioral cues and signals, in timing of initiation of feeding, timing of termination of feeding, dealing with the baby’s food preferences, and pacing rate of feeding in accordance with the baby’s rate of intake. Four 9-point rating scales were later constructed on the basis of this analysis. All proved significantly to differentiate the mothers of babies who were later identified as securely attached from the mothers of babies later identified as anxiously attached. Finally, two variables were examined which Main had identified, hypothesizing that they would differentiate the mothers of the anxious, avoidant (Group A) babies from the mothers of the anxious, resistant (Group C) babies-lack of emotional expression and rigidity. She had noticed in a study independent of ours (Main, 1977; Tolan, 1975) that A mothers displayed a remarkable lack of emotional (facial)expression when watching or in interaction with their babies. She interpreted this as due to repressed or suppressed anger, and indeed it is very unlikely that a mother will overtly express anger toward her baby while being observed, particularly in a laboratory situation. Assuming that this interpretation would also hold when observations were undertaken in the home environment, she undertook an analysis of our narrative report data. The ratings, undertaken by an assistant working blind, covered the whole of the first year. Group A mothers were found to be less emotionally expressive than either B or C mothers, the difference between A and B being statistically significant (p < .003)although the difference between A and C fell short of the .05 level. Rigidity and compulsiveness were also rated on the basis of the entire first year, largely because of a hunch of mine. Non-B mothers were found to be significantly more rigid and compulsive than B mothers, and this effect seemed largely attributable to the fact that A mothers were significantly more compulsive than B mothers. This rigid compulsiveness could be interpreted as a way of keeping anger under control.

2 . Fourth-Quarter Comparisons Mothers of securely attached babies (Group B) show significantly less delay in responding to infant crying than do the mothers of either A or C babies. It is the mothers of the C babies, however, who are typically most unresponsive to crying, as shown by significant correlations of both frequency and duration measures of unresponsiveness to Discriminant Function 11, which discriminates C from non-C infants. The greater responsiveness of Group B mothers is shown

36

MARY D. SALTER AINSWORTH

also by the fact that they are more likely to acknowledge their babies when they enter the room after an absence. In regard to close bodily contact, the most conspicuous fourth-quarter difference is that mothers of B babies more often behave affectionately than the mothers of either A or C babies, and this is significantly correlated with both DF I and DF 11. Mothers of A babies tend more often to be abrupt and interfering when picking a baby up than do B mothers. B mothers are less frequently inept in handling their babies than either A or C mothers, and C mothers are particularly likely to be inept. Mothers of C babies devote more of the time they hold their babies to routines (feeding, for example) than do either B or A mothers; a variable which we believe to reflect insensitivity to developmental changes in the baby (see Section 111, A, 2). In regard to the general characteristics assessed by the four rating scales, mothers of securely attached babies (Group B) are sensitive to infant signals, acceptant, cooperative, and accessible, whereas mothers of anxiously attached babies (both Groups A and C) are significantly more insensitive, rejecting, interfering, and ignoring. Ainsworth et al. (1971) reported that the scale that best differentiated mothers of anxious, avoidant babies (Group A) from mothers of the other two groups was acceptance-rejection. According to this scale Group A mothers are rejecting, relatively frequently allowing imtation and resentment to overcome their positive feelings for the baby, and more often resenting the way in which the baby interfered with their other interests and activities. However, the correlations with the discriminant-function scores suggests that all four of these scales serve to distinguish A from non-A mothers, whereas they do not so clearly distinguish C from non-C. J. INTERPRETATIVE SUMMARY OF FINDINGS It is evident from the findings here reported that infants differ from one another in accordance with two major dimensions: security versus anxiety and absence versus presence of conflict in regard to close bodily contact. Associated with the security-anxiety dimension is the extent to which mothers are sensitively responsive to infant signals in a wide variety of different contexts and over the entire span of the infant’s first year. Associated with the physical-contact dimension are a variety of maternal behaviors and attitudes-those obviously related to physical contact itself and others such as rejection, anger, and rigidityxompulsiveness. The babies who can be identified as securely attached to their mothers have obviously experienced harmonious mother-infant interaction throughout the first year. They may be distinguished from babies who are anxiously attached primarily in terms of the security-anxiety dimension, but also by the dimension relevant to close bodily contact. Our hypothesis is that their mothers’ responsiveness to their signals in all contexts, including close bodily contact, has enabled them in the second half of the first year to build up a representational model of the mother

ATTACHMENT AND MOTHER-INFANT INTERACTION

37

as accessible and responsive. Consequently, they rarely show separation anxiety under ordinary circumstances, because they are confident of the mother’s accessibility and responsiveness. Indeed confidence in her responsiveness to signals is likely to have played a major role also in reducing the amount of crying and increasing their ability to utilize noncrying modes of communication (Bell and Ainsworth, 1972). Throughout a variety of contexts of interaction with their mothers babies who eventually become securely attached display behaviors reflecting positive affect. At first these positive behaviors might be directly attributed to the mother’s contingent behavior (and thus to her responsiveness to signals) but later on it may be inferred that part of the representational model of the mother includes expectations that interaction will be pleasant and enjoyable. Despite the pleasant quality of his interaction with his mother, the securely attached infant is freer than the anxiously attached infant to move away from his mother into exploratory play without being unduly concerned about mother’s whereabouts, that is, to use mother as a secure base from which to explore the world. The behavior of the securely attached infant and his responsive mother, in both familiar and unfamiliar surroundings, may be recognized as the expected evolutionary outcome of infant attachment and attachment behavior and of a reciprocal maternal behavior system which are preadapted to each other. As long as the dyad is in familiar surroundings in which neither threat nor inner promptings activate proximity-seeking behavior, each can pursue more or less independent activities, confident of the other’s whereabouts within reasonable limits of time and distance. In an unfamiliar environment and with the arrival of a strange person, both tend to maintain closer proximity than at home. These circumstances in combination with maternal departure tend to activate attachment behavior to a level of intensity that rarely occurs at home, but heightened attachment behavior, responded to appropriately by the mother, tends to restore proximitykontact and soon attachment behavior can subside. If, however, a baby is led by his exploratory activity into a potentially dangerous situation, his mother is likely to intervene with a verbal command, or a physical intervention, or both. In response to a mere vocal signal by his mother, the securely attached baby is likely to arrest his activity, or approach his mother, or perhaps both. Such maternal control of a baby’s activity across a distance is obviously adaptive and so is the baby’s general willingness to cooperate with his mother’s wishes. The babies who may be identified as anxious and resistant are distinguishable from securely attached infants primarily in terms of the security-anxiety dimension, and their mothers clearly differ from the mothers of the latter in terms of their general insensitivity to infant signals and communications. It is suggested that because of this insensitivity the baby cannot feel confident that his mother will come when he wants or needs her and cannot feel sure that she will be responsive even when she is close at hand. His working model of mother is of a relatively inaccessible and unresponsive person, and therein lies his anxiety.

38

MARY D. SALTER AINSWORTH

This anxiety is especially conspicuous when the baby is alarmed or otherwise likely to have his attachment behavior system activated at a high level of intensity. As Bowlby (1973) pointed out, the infant’s fear is compounded by the fact that he cannot trust his mother’s accessibility and responsiveness. Consequently such a baby has difficulty in using his mother as a secure base from which to explore, and tends not to be able to do so under even the mildest of stressful conditions. The anxious, resistant infants differ from the securely attached infants also in regard to behavior relevant to close bodily contact. When attachment behavior is activated at a high level of intensity, close bodily contact is required to terminate it. Therefore, the anxious baby has even greater need for contact than does the securely attached baby under the same kind of environmental conditions. Associated with her general insensitivity to his signals, his mother may not respond to signals for contact even when they are intense, and even when she does pick him up she may also not respond to the cues which might help her to judge when his attachment behavior is terminated and he can be put down without protest. Consequently, when his proximity/contact-promoting behavior is strongly activated, this baby lacks confidence in his mother’s responsiveness. Thus he may feel frustrated in anticipation of unresponsiveness, and thus mingles angry behavior with attachment behavior. This constitutes his anxious resistance, his ambivalence. The babies who may be identified as anxious and avoidant are distinguishable from securely attached infants in terms of the security versus anxiety dimension; they are distinguished both from the securely attached and from the anxious, resistant babies in terms of their approach-avoidance conflict with reference to close bodily contact with their mothers. Their mothers differ from the other mothers in two major ways, both of which contribute to a tendency for the mother to reject the baby: aversion to close bodily contact with the baby, and a rigid, compulsive pattern which in turn leads the mother to feel impatient, resentful, or downright angry when the baby interferes with her plans and activities. Whereas it is perhaps the mother’s general insensitivity to infant signals that is associated with the baby’s building up a representational model of his mother as inaccessible andor unresponsive, and hence contributing to an anxious attachment pattern, it is her rejection, especially her rebuffs in the context of physical contact, that contribute to his approach-avoidanceconflict. As indicated earlier, it is this conflict that we hold responsible for his avoidance of her in situations that activate the attachment system at a high level of intensity.

IV . DISCUSSION One major issue in studies of mother-infant interaction is whether it is the mother or the baby who plays the more important role in determining the course of the interaction. In longitudinal studies, such as the one here reported, since the

ATTACHMENT AND MOTHER-INFANT INTERACTION

39

focus is on changes of behavior over time, specific attention is likely to be directed toward the influence of the interaction upon the course of the infant’s development. Under these circumstances the question is extended to ask whether the contribution made by the mother or by the infant to the interaction between them plays a more important role in shaping his development. Since one of the most striking sets of findings to emerge from the present study suggests that certain deviant patterns of infant behavior are closely associated with deeply ingrained (and deviant) patterns of maternal behavior, we have been led to a serious consideration of the issue of “direction of effects” of mother on infant and/or of infant on the mother, and to the search for pertinent theoretical models. The discussion of findings will focus on this issue. First let us briefly consider the three major views that are relevant to the issue. A.

THREEVIEWS OF DIRECTION OF EFFECTS

I.

The Contributions of Both Mother and Infant Are Important

By definition the term “interaction”imp1ies a contribution from each of the individuals concerned. Consequently, as an article of faith to which many have given at least lip service, it is held that both partners in the interaction contribute to it in more or less equal measure, and that, by extension, both the mother’s behavior and the infant’s potential for development interact to shape the course of that development. 2.

The Contribution of the Mother is More Important

This view had for many years been dominant in the thinking of both developmentalists and clinicians; although, contrary to what is widely supposed, this was not Freud’s view nor is it the view of the majority of psychoanalysts today. It has thus often been held that the mother’s behavior is the fundamentally important factor in influencing the development of the child, at least during his earliest years. In many developmental inquiries, any significant correlation between maternal and infant measures of behavior was interpreted as a demonstration of the effect of the mother on the infant. To many, this has appeared to be an obviously correct assumption because of the relative helplessness of the infant and the seemingly greater power of the adult; although such an interpretation does not take into account the many ways in which an infant and his behavior exert great power over the adult. 3 . The Contribution of the Infant is More Important

During the last decade or so the pendulum has swung to a third view, not featuring the role of the child’s autonomous fantasy as many psychoanalysts do, but emphasizing the role of the infant in influencing the behavior of his mother. Contributing to this view was Yarrow’s (1963) report that the same foster mother

40

MARY D. SALTER AINSWORTH

behaves differently toward different infants, Rheingold’s ( 1969) argument that the infant “socializes” his mother as well as being socialized by her, and R. Q. Bell’s evidence (Bell, 1968; Bell and Harper,1977) of the ways in which infant characteristics and behavior can influence the behavior of the mother. Thomas et al. (1963) have argued for the continuity of the constitutional characteristics of the infant, thus implying that maternal behavior has relatively little influence on them. Although not all those who have stressed the role of the infant mean to imply that his role is more important than his mother’s, some recent research has presented rather a one-sided view of mother-infant interaction. Nevertheless, such research has been a desirable corrective to the notion that a mother can mold the behavior of her baby into any pattern she desires, provided that she goes about it “the right way.” The difficulty with all of these views, at least as here stated, is that they are too global. They do not allow for the likelihood that the direction of effects might differ at different points of development, in different contexts of interaction, in regard to different developmental issues, or for different infant-mother pairs. Nor do they allow for possible differences in direction of effects if one examines sequences of interaction within a limited time period in contrast to an investigation of effects over a substantial developmental span. OF EFFECTSIN B. DIRECTION

A

LIMITED TIMEPERIOD

Let us first consider studies of sequences of interaction within any one limited period of time. Such studies tend to focus on the basic processes of mother-infant interaction (at that time and within a specified context); they can be fruitful in identifying the contribution of each member of the dyad, without necessarily implying any direction of effects. Thus, when Stem (1971) identified the role of infant gaze aversion in regulating early face-to-face interaction, he did not imply that this was more important in determining the course of the interaction than the mothers’ and infants’ roles should be dealt with by asking more specific questions interactional process can be enriched by ascertaining what specific kinds of behavior on the part of one member of the dyad tend to be followed by other specific kinds of behavior on the part of the other, both for an individual dyad or in a normative sense, without raising the issue of their relative importance. Indeed, as long as the question is phrased in terms of overall importance, it is as unanswerable as the question of whether the chicken or the egg comes first. Whether one assigns to either member of the dyad the ‘‘leading’’ or “stimulus” role depends upon the point at which one “slices” the behavioral sequence. Hinde (1975) suggested that the question of the relative “importance” of mothers’ and infants’ roles should be dealt with by asking more specific questions that define the implication of importance. Two of the questions that Blehar et al.

ATTACHMENT AND MOTHER-INFANT INTERACTION

41

(1977) asked about relative roles of mother and infant in early face-to-face

interaction were: Which member of the dyad initiates most episodes of interaction? and Which terminates most? It was clearly the mother who initiated most (9 1% of the episodes); but the findings gave an equivocal answer about termination (mothers terminated 44%, but in 37% the termination was either mutual or it could not be ascertained whether mother or infant was responsible for it). In conjunction with episodes of ventral-ventral physical contact in his longitudinal study of mother-infant interaction of rhesus monkeys, Hinde (1975) reported on one specific question relevant to any one time period, namely, whether it was mother or infant who was primarily responsible for determining the length of contact. The measure generated to answer this question combined initiations and terminations; it was the proportion of episodes in which it was the infant who made contact minus the proportion of episodes in which it was the infant who broke contact. The relevant findings were different for each time period considered; but, in summary, it was the mother who was primarily responsible for the length of contact in the early weeks, whereas it was the infant later on.

c.

DIRECTION OF EFFECTS OVER

SEVERAL PERIODS OF

TIME

It is in the context of changes of behavior that occur over substantial spans of time that the issue of direction of effects is most likely to be raised. Let us consider three ways in which the question may be phrased. 1 . In General, Which Partner is More Important in Changing the

Other’s Behavior and in Influencing the Course of Infant Development? This question refers to an overall judgment as to whether it is the mother or the infant who plays the more important long-term role, throughout the developmental period, across all contexts of interaction, both normatively and in regard to individual differences among dyads. I admit that, for the sake of argument, I am beginning with a question that I consider to be unproductive, unanswerable, and at the very least unanswered in the light of the relatively small volume of research to date. My own bias has been to consider the roles of both mother and infant to be important in an overall sense, despite the fact that the findings of our research suggest that in some ways one member of the dyad seems to take the leading role and in other ways the other. Although I do not intend to argue causal issues from it, I nevertheless believe that evolutionary theory provides a useful perspective to the issue of direction of effects. Here the premise is that in the course of evolution certain speciescharacteristic behaviors of both infant and mother become preadapted to each other-those that contribute to the infant’s protection and hence to survival.

42

MARY D. SALTER AINSWORTH

Therefore, in the absence of gross anomalies, both mother-infant interaction and infant development tend to proceed along species-characteristic lines. One important feature of the environment to which a baby’s behavior is preadapted is a mother figure who is responsive to his behavioral cues, not only his specific signaling behaviors such as crying and smiling but also the signal value of his behavioral repertoire as a whole. Consequently, as infant behavior changes in the course of development, maternal behavior tends to change concomitantly, as Marvin (1977) has pointed out. This does not imply that the mother is predisposed to continue to respond positively to such cues throughout the entire period of infancy and early childhood. Trivers’s (1 974) cost-benefit theory of the relation of a mother’s behavior to her own eventual reproductive success suggests that from a natural selection viewpoint her investment in the infant will taper off. However, this consideration does not essentially change the general notion that mother-infant interaction, in the absence of anomalies, tends to proceed along species-characteristic lines. Although it is of interest to document the parallel courses of behavioral change, and to identify points in development at which the behavior of either member of the dyad may play a catalytic role (see Section IV, C, 2), as long as the changes over time proceed along species-characteristiclines and without marked deviation, it seems unprofitable to attempt an overall assessment of the relative importance of the roles of mother and infant in the changing interaction between them. When the issue is extended to ask which member of the dyad makes the more important contribution to the infant’s development, it may be perceived as similar to the issue of nature versus nurture, and equally unanswerable. The genetic ground plan that guides development requires certain environmental characteristics for it to proceed normally; and clearly one of the most important aspects of an infant’s environment is his principal caregiver or mother figure. Both heredity and environment interact to influence development of the individual, and, within normal limits, it is unprofitable to attempt to assess their relative importance. Relevant to this issue, I am impressed with the geneticists’ notion of “phenotypical buffering,” which implies that there is a vastly greater variation among genotypes than among phenotypes, and that it tends to be the buffering action of the environment that accounts for the smaller phenotypical variation. Our hypothesis is that interaction with the mother may accomplish such buffering. Assuming that a mother has some concept of behavioral norms for infants of different ages, she is likely to attempt, more or less skillfully, to nudge her baby’s behavior toward her concept of the norm. Thus, the mother of an overactive baby may try to moderate his activity by avoiding overstimulation, whereas the mother of an underactive baby may try to rouse him to more active interaction with her and with other aspects of its environment. Consequently, in time, many babies tend to converge toward a more “average” pattern of behavior than might have been expected from their neonatal patterns. When, for

ATTACHMENT AND MOTHER-INFANT INTERACTION

43

whatever reason, such buffering does not take place, one may expect the phenotypical outcome to be perhaps even more extreme than neonatal patterns might have predicted. In either case,-there is obviously an important interaction between constitutional and environmental influences. In summary, it is suggested that it is unproductive to raise the question of whether mother or infant is more important either in determining the course of changes in interaction or in influencing the course of the infant’s development as long as that question is phrased to imply overall importance. There are, however, at least two specific questions which promise to be more productive. 2. Can One Partner Be Identified as a Catalyst f o r a Specific Change?

Even though the contributions of both members of the dyad are essential to the interaction between them, it still could be that one or the other takes the leading role in triggering a specific change in interaction at a specific point in development. For example, Hinde (1975) addressed himself to the question of whether it is the infant rhesus who leads in achieving increasing independence of its mother, or whether it is she who promotes this change by increasing rejection of her baby’s attempts to achieve and to maintain physical contact with her. Using the same measures described earlier (see Section IV, B), taken at various times over the first 30 weeks of life, Hinde concluded that changes in the mother are more important than changes in the infant in regulating the speed at which the infant achieves independence. As Hinde himself has pointed out, the mother’s decreasing tendency to initiate contact and her increasing tendency to terminate it could be influenced by changes in the infant itself, such as change in coat color, increasing competence, increasing interest in exploration and in play with other infants. Nevertheless, his findings suggest that it is the mother’s changed behavior, proceeding from whatever cues her infant may have provided, that plays the leading role in this developmental shift.

3. Which Partner is the More “Responsible” f o r Deviant Development? It is suggested that in some instances of clearly deviant infant development it is possible to identify one member of the mother-infant dyad as being more “responsible” than the other. If the child has gross genetic defects or has suffered damage in the prenatal or perinatal period, he is responsible for his own subsequent deviant development in the sense that the roots of the deviation lie within his own constitutional structure, and that his developmentalcourse will be deviant to some extent even when the environment in which he is reared (including his mother’s behavior) approximates the environment of evolutionary adaptation. Thus, a baby with Down’s syndrome cames within himself a genetic ground plan

44

MARY

D.

SALTER AINSWORTH

for appearance, behavior, and development that deviates from the norm. Thus, also, Prechtl ( 1963) reported that mothers of even minimally brain-damaged infants have difficulty in establishing normal interaction with them. This second example, however, highlights the important point that even in cases of constitutional defect the behavior of the mother figure may to a greater or lesser extent buffer the effects of the defect if she is able to make unusual effort to gear her behavior appropriately to that of the defective infant. Conversely, the mother, dismayed by the extent to which her baby falls short of expectations, may find herself unable to behave in ways that would minimize the baby’s deviant development. On the other hand, there are some cases in which a child’s developmental anomalies seem primarily attributable to his environment of rearing, departing grossly from that to which his behavior is preadapted. A well-known example of such an environment is an institution in which the staffing or infant-care procedures are such that there is no one figure (or even a small set of figures) who is able to be contingently responsive to infant signals. In the present report, however, we are concerned with instances in which there is a principal caregiver (mother figure), but one whose behavior departs grossly from that to which infant behavior is preadapted, and who thus may be said to be more responsible than her child for his deviant development. To be sure the baby may individually adjust his behavior as best he can to a deviant environment. Thus, when an infant with long institutional rearing appears to have lost the capacity for becoming attached, he might be viewed as protecting himself against the pain of the repeated rebuffs he received whenever he did begin to focus on one of his many caregivers as a potential attachment figure. In that sense, even deviant development has sometimes been identified as adaptive. Thus, even in instances in which either the infant or his mother figure may be identified as the more important source of deviant development, there is still the possibility that the behavior of the other may adjust itself in a way to reduce the extent of the deviation. On the other hand, the behavior of the partner may exacerbate the deviation. Thus, it might well be expected that the most severe developmental deviations would occur when there is both a constitutional defect in the infant and caregivers who fail to gear their behavior appropriately to the infant’s signals. OF FINDINGS I N LIGHT OF THE ABOVE D. DISCUSSION CONSIDERATIONS

1 . The Relation of Maternal Responsiveness to Signals to the Development of Secure Infant -Mother Attachment

Those features of maternal behavior found in the present study to be the most significantly associated with infant behavior and development involve, directly or indirectly, the extent to which the mother responds to infant signals and

ATTACHMENT AND MOTHER-INFANT INTERACTION

45

communications, and thus gears her behavior to the characteristics and behavior of her own particular infant. Thus, although the infant through his own idiosyncratic patterns of behavior certainly contributes to the interaction with his mother, the extent to which his mother goes along with, disregards, or opposes the implications of the baby’s behavioral cues makes a great deal of difference to the quality of the interaction. We have suggested that infant behavior is preadapted to a mother figure who is responsive to his signals, and who thus intervenes promptly when he cries, picks him up when his signals suggest that he desires contact, feeds him when his signals imply hunger, and so on. We have also suggested that the infant who, by the end of the first year, can be identified as securely attached, has developed normally, i.e., along species-characteristic lines. It is the mothers of these securely attached infants who have been found to be most sensitively (and appropriately) responsive to infant signals throughout many contexts during the first year. The way in which our measures were chosen tend, however, to cloak two important features of maternal responsiveness to infant signals. They cannot show the extent to which different mothers behaved differently because they were responding to infants with different characteristics. Therefore, we can cite no clear-cut evidence of phenotypical buffering although we are convinced that it occurred. Indirect evidence is offered by the fact that it was not so much the mother’s behavior in absolute terms that differentiated mothers of secure versus anxious infants as it was the extent to which her behavior was geared to infant cues. Second, the fact that we sought measures of maternal behavior appropriate to the whole span of the first year tends to obscure the fact that the mothers in our sample were responsive to developmental cues, altering their behavior to mesh with changing infant cues, although some did so more skillfully than others. Our theoretical and empirical emphasis on the significance of maternal responsiveness to infant behavioral cues does not imply that mothers should be entirely reactive to infant behavior and without plans of their own about influencing it, otherwise phenotypical buffering could not take place. Thus, for example, the sensitively responsive mothers in our sample did not respond to every infant cry, regardless of its nature, duration, and context. Part of being sensitively responsive is responding appropriately, and sometimes it is most appropriate to do nothing, at least for the moment. In regard to the infants in our sample who developed a secure attachment to their mothers, it seems unprofitable to attempt a general assessment of the relative potency of mother and infant in changing the behavior of the other or in influencing the course of infant development. In every particular their contributions to interaction tend to interlock, and to approximate theoretical expectations from the concept of evolutionary preadaptation. It is nevertheless of value to document the parallel course of behavioral change, if only to establish a baseline to facilitate identification of either mothers or infants who appear to be clearly deviant in their behavior.

46

MARY D. SALTER AINSWORTH

2 . Cross-Quarter Correlational Analyses In regard to the question of whether it is the behavior of the mother or that of the baby which seems primarily “responsible” for triggering a specific change, our cross-quartercorrelations of pairs of infant and maternal behavioral measures are relevant. To be sure, some of the correlation matrices suggested a reciprocal directional effect, but a few suggested that the behavior of one partner triggered a change in the behavior of the other partner. One obvious shortcoming of the cross-quarter correlational findings is that it is artificial to isolate pairs of behavioral measures when in reality maternal behavior is patterned from the beginning and infant behavior increasingly becomes so. Thus, we have suggested that the influence of maternal responsiveness to infant crying in reducing the subsequent amount of crying may be attributable to a pervasive pattern of responsiveness to signals of all kinds. Another noteworthy cross-quarter correlational finding was that maternal behaviors were much more stable in the course of the infant’s first year than were his behaviors, and that, in particular, infant behavior in the first three months had no predictive value. Sander (1962) suggested that the most fundamental issue facing the mother-infant dyad during the baby’s first three months of life is the regulation of his basic rhythms. His later research (e.g., Sander, 1969) suggested that the normal baby is remarkably flexible in adjusting most basic rhythms (activity, sleep, hunger, crying) to the consistent behavior of a foster mother, since different babies cared for by the same mother figure emerged with strikingly similar patterns. It could well be that during the first three months or so a stable maternal pattern of behavior does more to trigger changes in the specifics of infant behavior than it can accomplish later on after the infant’s behavior has become more organized. Also relevant to the issue of stability of infant behavior is the concept of his building up an inner representation (Piaget, 1937) or a “working model” (Bowlby, 1969), of his mother, a model that must be based on his previous experience in interaction with his mother. To be sure, a mother also has an inner representation of her baby, but this may well have developed to some extent even before his birth. Although each partner’s models of the other are subject to change through experience, the contributions of neither to the interaction between them can be comprehended simply within the span of the current interaction. Furthermore, the fact that the mother’s model antedates the baby’s capacity for inner representation tends to give her behavior a degree of stability during the early months that his behavior seems to lack.

3 . Findings Relevant to Deviant Development The pattern of behavior characteristic of the 1-year-olds that we have identified as securely attached to their mothers may be viewed as the norm, both in the modal sense and in terms of theoretical expectations from an ethological, evolu-

ATTACHMENT AND MOTHER-INFANT INTERACTION

47

tionary model. The two anxiously attached groups may both be judged to show behavior patterns deviating from the norm. We reject the hypothesis that it was the babies in this sample whose constitutional characteristics were responsible for their development of deviant patterns. They were all reported to have been normal newborns with normal births. Furthermore, the fact that none of our behavioral measures revealed a significant tendency for behavior characteristic of the earliest months to persist into later months supports the conclusion that there was no adequate constitutional basis for their later deviant behavior. On the other hand, it is clear that the deviant outcomes among the anxiously attached babies were associated with long-term patterns of maternal behavior which made for insensitivity to infant behavioral cues. We have reported that the mothers of the anxious, avoidant babies manifested deep aversion to close bodily contact and marked rigidity and compulsiveness, both of which may be inferred to be of long standing. The mothers of the anxious, resistant babies were anxious with strong underlying depressive tendencies, two of the mothers becoming fragmented when faced with two or more simultaneous demands on their attention. It is clear that the rearing environments provided by these mothers constitute gross deviations from that to which infant behavior is preadapted. It is therefore justified to conclude that in such cases it was the mother who was more responsible than the infant for his deviant development. It must be emphasized that in each case the deviant patterns of behavior shown by the mothers of anxiously attached babies appeared to be deeply ingrained and resistant to substantial change in response to those infant cues that have a powerful effect on other mothers. In this context, it is relevant to mention four mothers whose behavior shifted markedly over the first year, two of them involving a couple of months of a depressive, unresponsive period immediately postpartum and two involving a sharp decrease of maternal accessibility and responsiveness during a period of unusual familial stress. The babies in question responded both to maternal unresponsiveness and later to increased responsiveness, and indeed developed normally enough that they were eventually identified as securely attached. Nevertheless, they seemed more in conflict about proximitykontact with their mothers than other Group B babies. The implication is that, somehow, in the mother’s unresponsive period, there was the basis for the baby forming a working model of his mother as not quite trustworthy in regard to accessibility andor responsiveness, and this aspect of the model was carried forward despite change in maternal behavior. E. PRACTICAL IMPLICATIONS

It is obvious that the whole issue of “direction of effects” in mother-infant interaction and its influence on infant development has profound implications for

48

MARY D. SALTER AINSWORTH

infant-care practices. To the extent that it is the infant’s contribution that is stressed, it might be concluded that the infant will develop along lines predestined by his constitutional structure regardless of what his parents do, or even that it does not much matter what kind of care is provided for infants and small children. Our argument is contrary to such conclusions however. Regardless of whether either member of the dyad can be identified as chiefly responsible, both nevertheless contribute to the interaction between them. This principle, in addition to the concept of phenotypical buffering, suggests that the mother’s contribution to interaction with her infant can influence his development to proceed along lines that more closely approximate a norm that does his own constitutional endowment, and even in the case of gross constitutional deviations buffering may have some effect in reducing the magnitude of the ensuing developmental deviation. To the extent that it is the mother’s contribution that emerges as the more important, it could be hoped that information, advice, training, andor intervention might assist mothers to adopt practices likely to facilitate normal infant development. Even though both members of a mother-infant dyad contribute to their interaction and thus to the course of infant development, the mother may be conceived as generally having more “degrees of freedom” than does the baby, in the sense that the baby only gradually becomes capable of intentional behavior and of organizing his behavior in terms of plans. Therefore, the mother, unless very handicapped by deeply ingrained personality patterns, is much better able consciously and deliberately to plan her behavior relevant to infant care than the infant is able to plan his behavior toward her. Therefore, she can presumably profit somewhat from experience, advice, and education to shape her own contribution to the interaction to the advantage of the baby’s development, and perhaps in particular cease to follow pronouncements that would lead her to work against the grain of the interaction to which both her behavior and her baby’s are preadapted. In instances in which the mother’s deviant personality patterns are deeply ingrained, however, she does not have the same degrees of freedom as the average mother. It seems unlikely that anything short of intervention could be effective in altering deep-seated ways of behaving that are not amenable to conscious control, whether the intervention takes the form of individual therapy or the kind of intervention that either Fraiberg (Shapiro et a l., 1976) or Parmelee (Kass et al., 1976) and their teams have offered. Finally, it is perhaps because of the practical implications of research into mother-infant interaction that the issue of direction of effects has loomed large in the recent literature. We have argued that, except in instances of clearly deviant development, it is an unanswerable question as to whose contribution to interaction and to behavioral change is generally the more important. Nevertheless, it is acknowledged that changes in the behavior of one partner may at some particular

ATTACHMENT AND MOTHER-INFANT INTERACTION

49

stage of infant development and in regard to some specific aspect of motherinfant interaction trigger changes in the behavior of the other. Thus, attempts to identify the contributions made by each partner to the interaction between them may well have useful implications for infant-care practices, and, in the case of deviant infant development, to try to disentangle the direction of effects has potentially very practical implications. Acknowledgments The project that yielded the data herein reported was supported by grant 62-244 of the Foundations’ Fund for Research in Psychiatry, USPHS Grant ROI HD 01712, and by grants from the Office of Child Development, the Grant Foundation, and the Spencer Foundation; this support is gratefully acknowledged. I wish also to thank Barbara Wittig, George Allyn, and Robert Marvin who collected most of the data, and my several coauthors, named throughout the chapter, who have contributed to data analysis, conceptualization, and publication of the various works upon which this chapter is based. Finally, 1 wish to thank Robert Hinde, R. Q. Bell, and especially Robert Marvin, who have induced me to clarify my thinking about the issue of direction of effects as it is pertinent to the findings of this project, although they cannot be held responsible for the use that I have made of their catalytic assistance.

References Ainsworth, M . D. S. 1967. “Infancy in Uganda: Infant Care and the Growth of Love.” Johns Hopkins Press, Baltimore, Maryland. Ainsworth, M. D. S. 1969. Object relations, dependency and attachment: A theoretical review of the infant-mother relationship. Child Dev. 40, 969-1025. Ainsworth, M. D. S. 1972. Attachment and dependency: A comparison. In “Attachment and Dependency” (J. L. Gewirtz, ed.), pp. 97-137. Winston, Washington, D.C. Ainsworth, M. D. S. 1973. The development of infant-mother attachment. In “Review of Child Development Research” (B. M. Caldwell and H. N. Ricciuti, eds.), Vol. 3, pp. 1-94. Univ. of Chicago Press, Chicago, Illinois. Ainsworth, M. D. S. 1977a. Attachment theory and its utility in cross-cultural research. In “Culture and Infancy: Variations on the Human Experience” (P. H. Leiderman and S. Tulkin, eds.), pp. 49-67. Academic Press, New York. Ainsworth, M. D. S. 1977b. Infant development and mother-infant interaction among Ganda and American families. In “Culture and Infancy: Variations on the Human Experience” (P. H. Leiderman and S. Tulkin, eds.), pp. 119-149. Academic Press, New York. Ainsworth. M. D. S., and Bell, S. B. 1969. Some contemporary patterns of mother-infant interaction in the feeding situation. In ”Stimulation in Early Infancy” (A. Ambrose, ed.), pp. 133-170. The Academic Press, New York. Ainsworth, M. D. S.. and Bell, S. M. 1977. Infant crying and maternal responsiveness: A rejoinder to Gewirtz and Boyd. Child Dev. 48, 1208-1216. Ainsworth, M. D. S., Bell, S. M., and Stayton, D. J. 1971. Individual differences in strangesituation behavior of one-year-olds. In “The Origins of Human Social Relations” (H. R. Schaffer, ed.), pp. 17-52. Academic Press, New York. Ainsworth, M.D. S . , Bell, S. M., and Stayton, D. J. 1972. Individual differences in the development of some attachment behaviors. Merrifl-Palmer Q . 18, 123-143.

50

MARY D. SALTER AINSWORTH

Ainsworth, M. D. S., Bell, S. M., and Stayton, D. J. 1974. Infant-mother attachment and social development: “Socialisation” as a product of reciprocal responsiveness to signals. In “The Integration of a Child into a Social World” (M. P. M. Richards, ed.), pp. 99-135. Cambridge Univ. Press, London and New York. Ainsworth, M. D. S., Blehar, M. C., Waters, E., and Wall, S. 1978. “Patterns of Attachment.” Erlbaum, Hillsdale, New Jersey. Bell, R. Q. 1968. A reinterpretation of the direction of effects in studies of socialization. Psychol. Rev. 75, 81-95. Bell, R. Q., and Harper, L. V. 1977. “The Effects of Children on Adults.” Erlbaum, Hillsdale, New Jersey. Bell, S.M.. and Ainsworth, M. D. S. 1972. Infant crying and maternal responsiveness. Child Dev. 43, 1171-1190. Blehar, M. C., Lieberman, A. F., and Ainsworth, M. D. S. 1977. Early face-to-face interaction and its relation to later infant-mother attachment. Child Dev. 48, 182-194. Blehar, M. C., Ainsworth, M. D.S., and Main, M. 1978. Mother-infant interaction relevant to close bodily contact: A longitudinal study. In preparation. Bowlby, J. 1958. The nature of a child’s tie to his mother. Inr. J. Psychoanal. 39, 350-373. Bowlby, J. 1969. “Attachment and Loss. Vol. I Attachment.” Basic Books, New York. Bowlby, J. 1973. “Attachment and Loss. Vol. 2 Separation: Anxiety and Anger.” Basic Books, New York. Cronbach, L. J., and Meehl, P. E. 1955. Construct validity in psychological tests. Psychol. Bull. 52, 28 1-302.

Hinde, R. A. 1975. Mothers’ and infants’ roles: Distinguishing the questions to be asked. Ciba Found. Symp. 33, 5-13. Hinde, R. A. 1976. Interactions, relationships and social StNCtUre. Man 11, 1-17. Kass, E. R.,Sigman. M.. Bromwich, R. F.,and P m e l e e . A. H. 1976. Educational intervention with high risk infants. In “Intervention Strategies for High Risk Infants and Young Children” (T. D. Tjossem, ed.), pp. 535-543. Univ. Park Press, Baltimore, Maryland. Kenny, D. A. 1975. Cross-lagged panel correlation: A test for spuriousness. Psychol. Bull. 82, 887-903.

Mahler, M. S., Pine, F.,and Bergman, A. 1975. “The Psychological Birth of the Human Infant.” Basic Books, New York. Main, M. 1977. Analysis of a peculiar form of reunion behavior seen in some daycare children: Its history and sequelae in children who are home-reared. “Social Development in Daycare” (R. Webb, ed.). JohnS Hopkins Press, Baltimore, Maryland. Marvin, R. S. 1977. An ethological-cognitive model for the attenuation of mother-child attachment behavior. In “Advances in the Study of Communication and Affect. Vol. 3. The Development of Social Attachments” (T. M. Alloway, L. Krames, and P. Pliner. eds.), pp. 25-60. Plenum, New York. Miller, G . A., Galanter, E., and Pribram. K.H. 1960. “Plans and the Structure of Behavior.” Holt, New York. Piaget. J. 1936. “The Origins of Intelligence in Children” 2nd ed. International Univ. Press, New York (Engl. transl., 1952.) Piaget, J. 1937. “The Construction of Reality in the Child.” Basic Books, New York. (Engl. transl., 1954.)

Prechtl, H. F. R. 1963. The mothershild interaction in babies with minimal brain damage. In “Determinants of Infant Behavior 11” (B. M. Foss, ed.), pp. 53-58. Wiley. New York. Rheingold, H. L. 1969. The social and socializing infant. I n “Handbook of Socialization Theory and Research” (D. A. , G o s h , ed.), pp. 779-790. Rand McNally, Chicago, Illinois. Sander, L. W. 1%2. Issues in early mother
ATTACHMENT AND MOTHER-INFANT INTERACTION

51

Sander, L. W. 1969. Regulation and organization in the early infant-caretaker system. In "Brain and Early Behavior" (R. Robinson, ed.), pp. 31 1-333. Academic Press, New York. Schaffer, H. R., and Emerson, P. E. 1964. The development of social attachments in infancy. Monogr. Soc. Res. Child Dev. 29, Serial No. 94. Shapiro, V., Fraiberg, S., and Adelson, E. 1976. Infant-parent psychotherapy on behalf of a child in a critical nutritional state. Psychoanal. Study Child. 31, 461 4 9 1 . Stayton, D. J., and Ainsworth, M. D. S. 1973. Individual differences in infant responses to brief, everyday separations as related to other infant and maternal behaviors. Dev. Psychol. 9, 226235. Stayton, D. J., Hogan, R., and Ainsworth, M. D. S. 1971. Infant obedience and maternal behavior: The origins of socialization reconsidered. Child Dev. 42, 1057-1069. Stayton, D. J . , Ainsworth, M. D. S.. and Main, M. 1973. The development of separation behavior in the first year of life: Protest, following, and greeting. Dev. Psychol. 9, 213-225. Stern, D. N . 1971. A micro-analysis of mother-infant interaction: Behavior regulating social contact between a mother and her 3% month-old twins. J . Am. Acad. Child Psychiat. 10, 501517. Thomas, A,. Chess, S.,Birch, H. G.. Hertzig, M. E., and Kern, S. 1963. "Behavioral Individuality in Early Childhood." New York Univ. Press, New York. Tolan, W . J . 1975. Maternal Facial Expression as Related to the Child-Mother Attachment. Senior Thesis, Univ. of California, Berkeley. Tracy, R . L.. Lamb, M. E.. and Ainsworth. M. D. S. 1976. Infant approach behavior as related to attachment. Child Dev. 47, 57 1-578. Trivers, R. L. 1974. Parent-offspring conflict. Am. Zool. 14, 249-264. Yarrow, L. J . 1963. Research in dimensions of early maternal care. Merrill-Palmer Q . 9, 101-I 14.

This Page Intentionally Left Blank

ADVANCES

IN THE STUDY OF BEHAVIOR.

VOL. Y

Feeding: An Ecological Approach F. REEDHAINSWORTH AND LARRY L. WOLF DEPARTMENT OF BIOLOGY SYRACUSE UNIVERSITY SYRACUSE, NEW YORK

........................ ............................

1. Introduction: Feeding as an Economic Problem

11. Some Determinants of Costs and Benefits

A . Energetic Costs Determine Requirements for Energy

........................

53 56 56 58 60

61 B. Natural Interpretation of Hummingbird Food Choice . . . . . . . . . . . . . . . . . C. Other Determinants of Food Choice D. “Search Images” and Food Choice IV. Feeding Patterns . . . . . . . . . A. Meal Initiation ........................................ B. Meal Size . . . . . . . . . . . V. Economics of Patch Exploitation A. A Priori Information.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. A Posteriori Information . . . . . . . . . . . . . . . VI. Synopsis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

FEEDING AS I. INTRODUCTION:

AN

61

65 67 68

70 71 73 73 80 83 88 89

ECONOMIC PROBLEM

Studies of feeding follow two general approaches. Physiological studies seek to explain feeding in terms of internal negative feedback systems that respond to a variety of hypothesized variables (e.g., “glucostatic,” “thermostatic,” “lipostatic,” and “hepatostatic” theories, for recent reviews, see papers in Novin et a l . , 1976). Ecological studies emphasize the external variables that influence feeding. The two approaches ultimately must be integrated. Whether, on what, or how much an organism feeds may depend not only on an internal state of hunger but also on the availability, nature, and distribution of food, and on the degree of predation risk associated with feeding (for general discussions, see Schoener, 1971; Curio, 1976; Wolf and Hainsworth, 1978; McFarland, 1977, 1978). Cupyright u IY7Y by ALddemlr P r e w h r 53

All nghts crf repnxlucliim in dny form reserved ISBN 0 12-I1045(W-5

54

F. REED HAINSWORTH A N D LARRY L. WOLF

We will employ economic theories applied to biological systems to provide a unified view of feeding behavior. These are termed “economic,” “cost:benefit,” or “optimality ” theories (Rapport and Turner, 1977). The basic biological hypothesis asserts that organisms should maximize some function of benefits and costs in order to maximize biological “fitness” (relative ability to survive and reproduce). Ecologists argue that one function for optimal feeding could be to maximize the rate of net energy gain and/or the rate of net gain of important nutrients. This criterion has been applied to diet choice (Pulliarn, 1974, 1975; Estabrook and Dunharn, 1976; Ellis et al., 1976), meal size (DeBenedictis et al., 1978), resource exploitation through movement patterns within and between food patches (Cody, 1974; Kiester and Slatkin, 1974; Ware, 1975; Charnov, 1976a), and the coevolution of predators and prey (Slobodkin, 1974; J. Taylor, 1976; R. J. Taylor, 1976). Relationships between benefits and costs are illustrated very generally in Fig. 1, and some variables that may influence them through feeding are indicated in Table I. Costs and benefits often are considered in energetic (caloric) terms, although nutritional requirements can and should affect feeding (Rozin, 1976; Wolf and Hainsworth, 1978). The emphasis on an energetic basis for feeding lies in the requirements for energy in many cost terms. For example, maintenance, activity, and reproduction require energy expenditures that must be provided for from food. Also, time could be maximized as a benefit and minimized as a cost through efficient feeding (Schoener, 1969b; Wolf et al., 1975; Norberg, 1977). It is a major task of comparative studies of feeding to explain similarities and differences among species. A common basis for a variety of approaches to feeding can be illustrated by emphasizing the distinction between regulation and control (Brobeck, 1965). Several controls could govern feeding, but to be effective they must regulate energy. Different organisms are subject to different

FIG. I . General relationshipbetween costs and benefits and variables influencing feeding. See Table I for some variables that can influence feeding.

FEEDING: AN ECOLOGICAL APPROACH

55

TABLE I VARIABLES INFLUENCING FEEDING costs Maintenance Body size Environmental Temperature Photoperiod Activity

Social Reproduction Predation Time

Benefits

Food quality Rate of intake

Food availability Spatial Temporal Nutrition Social Time

limitations on energy balance as the result of evolution in different environments. We expect controls to differ, but we expect them to result in energy regulation. Since controls are expected to differ due to environmental differences, any hypothesized control mechanism ultimately must explain regulation under natural conditions. We will indicate situations in which apparent controls observed under laboratory situations can lead to inappropriate interpretations of behavior in natural situations. Controls may operate at several levels of organization. Recent interpretations of physiological controls of feeding stress the role of the liver in response to supplies of metabolic fuels (e.g., Friedman and Stricker, 1977). At another level, sensory information from the environment provides input for control of proximate food choice. At a further level, an organism’s ability to adjust behavior to spatial and temporal distribution of food can contribute to control of energy regulation. Unless these various levels are integrated into an explanation of natural behavior, it is difficult to obtain an appropriate perspective for the operation of controls in regulation. Our approach to feeding examines integration of controls in natural situations with emphasis at the level of interaction of the organism with its environment. What is the evidence for an economic interpretation for feeding? In the following sections we will indicate briefly some energetic determinants of general cost and benefit functions. We then will examine evidence for food choice, meal patterns, and resource exploitation as determined by the economics of energetic costs and benefits. Our research on nectar feeding birds will form a focus due to the extent to which costs and benefits can be. specified, but we will attempt to integrate this into a general comparative treatment of feeding.

56

F. REED HAINSWORTH A N D LARRY L. WOLF

11.

A.

SOME DETERMINANTS OF COSTS AND BENEFITS

ENERGETIC COSTS DETERMINE REQUIREMENTS FOR ENERGY

Energy expenditures determine basic daily food requirements for consumer organisms. Requirements for periodically demanding situations such as reproduction or migration are usually thought of as additive to minimum maintenance and activity expenditures (King, 1972; Wolf and Hainsworth, 1978).

I . Maintenance a . Body Mass. Mass is a major determinant of energy expenditures, and it is perhaps the most noticeable difference among species. Within each major group of organisms (including microorganisms to mammals) total energy expenditures (calkme) for organisms at thermoneutral (nonstressful) temperatures are related to the 3/4 power of mass with different expenditure levels for different major taxa (Kleiber, 196 1 ; Schmidt-Nielsen, 1975). Size related expenditures (costs) relative to available energy supplies (benefits) should influence feeding, For example, digestive storage capacity is related linearly to mass (Calder, 1974) so larger organisms could consume more energy at a feeding relative to minimum maintenance expenditures than smaller organisms. This could make feeding frequency depend on body mass. Hummingbirds are interesting since they include the smallest species of birds with high feeding frequencies (several bout s/hour). b. Environmental Temperature. A variety of environmental factors influence rates of energy expenditure (Calder, 1974; King, 1974), and the most thoroughly studied is environmental temperature. Organisms that regulate body temperature increase heat production as environmental temperature decreases. Small homeotherms are relatively more poorly insulated than large homeotherms (Herreid and Kessel, 1967; Kleiber, 1972) so their rate of heat loss (call gmxhour) is higher at a given temperature. Thus, ambient temperature will affect food requirements differentially for large and small species. Even though small organisms have absolutely lower energy requirements (cayhour), a higher rate of loss due to size and insulation factors (callgmxhour) would dictate use of a larger proportion of ingested energy for body temperature regulation. Some organisms lower energy expenditures associated with cold environments by reducing body temperature (torpor). These include “poikilotherms” as well as some birds and mammals that may enter torpor daily or seasonally (Hainsworth and Wolf, 1978). Hummingbirds have this ability and it can save considerable energy (more than 90% at minimum expenditures in torpor, Hainsworth and Wolf, 1970). Organisms that enter torpor may require less food. Howeker, this depends on whether torpor is utilized. A variety of organisms do not utilize torpor to reduce energy expenditures unless there is some environmen-

FEEDING: AN ECOLOGICAL APPROACH

57

tal limitation (such as reduced food availability) that forces a decrease in body temperature (Hainsworth and Wolf, 1978). Since there appears to be an advantage to maintaining a homeothermic temperature, body temperature will be maintained by hummingbirds and a variety of other species whenever possible (Brown and Bartholomew, 1969; French, 1976; Hainsworth and Wolf, 1978). Rather than lowering subsequent food requirements, torpor should be followed by increased demand for energy to replenish reserves and remove the necessity for torpor (Hainsworth and Wolf, 1978). c. Photoperiod. Most organisms have a circadian rhythmicity in feeding. Dark and light periods set the periodicity for many species, and some that feed in both phases of a light cycle show different behavior in each (e.g., rats, LeMagnen, 1975; or hamsters, Silverman and Zucker, 1976; see below). If feeding is restricted to light or dark, photoperiod will influence energy requirements through the time that energy must be expended with no intake. For example, hummingbirds do not feed at night and must store energy for overnight periods. Effects of photoperiod vary with season and latitude and will form part of our discussion of meal patterns (see Section IV). 2. Activity

Most consumer organisms move to obtain food. This increases requirements for energy and is an important part of energetic costs under natural circumstances. Specific expenditures depend on the form of movement, speed, distance, and mass of the organism (Schmidt-Nielsen, 1972; Wolf and Hainsworth, 1978). At the most efficient speeds for a given body mass, organisms that swim have lower expenditureslkm than those that fly and flying organisms have lower costs/km than those that walk or run (Schmidt-Nielsen, 1972). However, these comparisons are based on speeds at which transport costs are minimum; but energy expenditures vary with speed within a locomotion mode (Pennycuick, 1969; Taylor et al., 1970; Tucker, 1971; Wolf and Hainsworth, 1978). Since organisms may not always move at speeds that minimize expenditures, it is important to assess the impact of various activities for energy requirements. Although the energetic costs at a given body mass to cover distance may be lower for flying animals, energetic costs per unit time generally are higher for flight (Tucker, 1971). Hummingbirds that consume nectar from flowers are somewhat special since they hover (flight at zero speed). This is a particularly costly form of flight (Pennycuick, 1969) since an aircraft or bird obtains lift from forward movement. Helicopters and hummingbirds in stationary flight must supply all of the power to lift their masses. Measurements of oxygen consumption for hovering hummingbirds indicate expenditures of about 2 15 cal/gm X hour (Lasiewski, 1963; Wolf and Hainsworth, 1971; Berger and Hart, 1972; Epting and Casey, 1973; Berger, 1974), the highest per gram values measured for vertebrates (Wolf and Hainsworth, 1978).

58

F. REED HAINSWORTH AND LARRY L. WOLF

Body mass influences energy expenditures for activity (Hainsworth and Wolf, 1972a; Greenewalt, 1975) while low environmental temperature has less impact since heat production during activity usually is high (Berger and Hart, 1972). One way to examine the importance of activity for food requirements for species of different sizes is to calculate the ratio of energy expended for activity to energy expended for sitting (maintenance) for organisms of different masses. Figure 2 compares the relative increase in energy expended for hovering above that for sitting for hummingbirds and suggests that small species may experience relatively less of an increase in expenditure for activity (Hainsworth and Wolf, 1972a). We also expect differences in expenditures for activity relative to maintenance among species of different masses with other forms of locomotion, although the specific relationship may not be the same as for hummingbirds. The relative expenditures should have an important influence on feeding behavior within and between species (Norberg, 1977; Schoener, 1969a). B. BENEFITSFROM FOOD To interpret feeding economically, it is necessary to specify the energy or nutritional benefit of food. This is seldom achieved. For example, several recent laboratory studies of feeding of mammals (e.g., opposums, Maller et al., 1965; guinea pigs, Hirsch, 1973; cats, Kanarek, 1975; hamsters, Silverman and Zucker, 1976) have suggested that differences in their feeding compared to the white rat laboratory model may be due to evolutionary differences in behavior produced by differences in diet. This is a reasonable hypothesis but it is based

FIG.2. Energetic costs per unit time for hovering relative to energetic costs per unit time for resting metabolic rate for hummingbirds of different sizes. Calculations based on an environmental temperature of 20°C.

FEEDING: AN ECOLOGICAL APPROACH

59

entirely on animals fed artificial diets, and there is little information on natural diets. Most information on natural diets comes from analysis of stomach contents or interpretations of general morphological adaptations (e.g., granivores vs. herbivores vs. carnivores). This does not permit assessing the economic balance between costs and benefits in feeding which requires knowing the quality of the natural diet as well as costs. Laboratory investigations should be interpreted relative to the importance of costs and benefits for feeding under natural conditions. The degree to which this is achieved will form a basis for much of our discussion. The problem of specifying important natural characteristics of the food of hummingbirds is simplified because of mutalism between the birds and their food. Hummingbirds obtain food from two sources: plant nectar and insects. They generally spend little time catching insects (Stiles, 1971; Wolf and Hainsworth, 1971; Wolf et af., 1976), and this is thought to be less important in providing energy although it usually is considered to be nutritionally important. Most energy comes from nectar produced by plants. The resource is visible, stationary, and easy to characterize in energetic terms (Hainsworth, 1973; Wolf et af., 1972, 1975, 1976; Baker, 1975). This is a coevolved relationship between consumer and food where each benefits. To obtain nectar, some part of the hummingbird usually contacts the anthers or stigmas of the plants and pollen is transferred from one plant to another (Grant and Grant, 1968). Pollination is the ruison d'erre for nectar production by many plants since their lack of mobility requires an agent for cross-pollination(Grant and Grant, 1968; Levin and Anderson, 1970; Faegri and van der Pijl, 1971; Snow and Snow, 1972). The extent of cross-pollination depends on the characteristics plants have evolved to attract pollinators to ensure pollen movement (Levin and Kerster, 1974). Pollen can be moved more efficiently if a pollinator visits a limited number of plant species for food (Levin and Anderson, 1970; Snow and Snow, 1972; Straw, 1972). If a hummingbird visited many species, then pollen would more likely mix and pollen dispersal could be less effective (Waser, 1977). With this mutualistic relationship, we can predict that plants (equivalent to prey) should have evolved food characteristics to attract and maintain visitation from particular pollinator species (equivalent to predators). These characteristics should contribute to maximizing the fitness of pollinators (Heinrich and Raven, 1972) within the constraints that lead to maximizing pollen flow between plants. However, for many consumer organisms food characteristics will be influenced by nonmutualistic factors. A predator generally reduces fitness of prey. This had led to the evolution of a variety of antipredator defenses (Curio, 1976). For example, chemical (Feeny, 1970; Levin, 1976) or physical (Gilbert, 1971; Smith, 1975) defenses can deter predators by increasing costs for consumers through either short-term palatability effects or long-term learned aversive postingestional effects (Brower and Brower, 1964; Rozin, 1976; see below). This can be accompanied by counter-evolutionby predators of detoxification mechanisms

60

F. REED HAINSWORTH AND LARRY L. WOLF

for specific chemical defenses (Rosenthal e f al., 1976). The complexity of these types of interactions makes specification of costs and benefits much more difficult compared with the coevolved system of nectar feeders and their food sources.

OF FOODCHOICE 111. THEECONOMICS

A number of laboratory studies suggest that food selection depends on shortterm taste or palatability effects (e.g., Young, 1967; Epstein, 1967; Dethier, 1976). A general conclusion is that some organisms “prefer” foods that have a sensory quality related to energy value. Some studies have examined the generality of the receptor system in response to food quality. Organisms may select nonnutritive foods that may be palatable (e.g., rats select saccharin, Collier and Novell, 1967; or blowflies select sugars that cannot be used metabolically, Dethier, 1976). The stimulus chemicals can be carbohydrates (Richter and Campbell, 1940; Dethier, 1976) or other substances that may provide information relative to specific prey detection (e.g., certain amino acids, Reiner and Reiner, 1975, Can and Chaney, 1976; Hartman and Hartman, 1977). However, we know little about the extent to which demonstrated food preferences are related to rates of net energy (or nutrient) gain under natural situations. Other laboratory studies indicate that food intake can be adjusted relative to either sensory characteristics of food andor postingestional effects. Rats (Epstein, 1967) and blowflies (Dethier, 1976) generally show “preference-aversion” functions for food concentration. Intake increases with concentration to a maximum and then decreases. The decrease is called an “aversion,” but it is associated with increased energy value so rate of net caloric intake may remain constant (Richter and Campbell, 1940) although sensory characteristics of food may modify this somewhat (Dethier, 1976). It often is difficult to interpret this behavior in a natural context (as well as in many laboratory situations) since costs may not be measured and little may be known about the range of quality of prey under natural circumstances. Additional laboratory experiments suggest that rate of intake or factors other than caloric value may be major determinants of food choice for some organisms. Some granivores select seeds in the laboratory based on ease of handling rather than caloric value may be major determinants of food choice for some organisms. Rosenzweig and Sterner, 1970; Kear, 1962). Also, cats (Kanarek, 1975), guinea pigs (Hirsch, 1973), and oppossums (Maller ef al., 1965) do not respond to caloric dilution of food by increasing consumption in the laboratory. Some experimental data support food choice based on net effects of costs and benefits. Smith and Follmer (1972) examined preferences of gray squirrels (Sciurus carolinensis) and fox squirrels (S.niger) for acorns, hickory nuts, and

FEEDING: AN

ECOLOGICAL APPROACH

61

walnuts that occur in their natural diet. From laboratory experiments, they found that net energy gains (assimilation) from nut endosperm were correlated with lipid content and were highest for hickory and walnut compared with acorns of several species of oaks. However, rate of caloric intake was considerably less for the higher quality nuts due to the high handling time to open them. When they were required to open the nuts, the squirrels preferred acorns which provided a higher rate of net (nut) energy gain. Other experiments related to natural situations suggest that rate of net benefit from food can determine food choice (Menge, 1972; Werner and Hall, 1974; Eggers, 1975; Himmelman and Carefoot, 1975; Paine, 1976). These underscore the conclusion that assessing factors important in food choice depends on determining variables that have an impact on the economics of feeding under natural circumstances (e.g., Estabrook and Dunham, 1976). We have examined food choice in the laboratory for hummingbirds with respect to several variables that can influence rates of net benefit from food in natural circumstances. We now will consider choice with respect to rate of consumption, caloric value, other food constituents, and availability, and we will attempt to relate laboratory observations on hummingbirds to natural situations. A.

LABORATORY EXPERIMENTS ON FOODCHOICE BY HUMMINGBIRDS

A basic laboratory observation that requires explanation in a natural context is that hummingbirds will select foods that are less efficient with respect to rate of net energy gain. Birds offered a choice between feeders containing detectable differences in sugar concentration persisted in consuming the more concentrated food until it was essentially impossible to obtain as a result of a corolla that reduced rate of consumption and, consequently, rate of net energy gain (Hainsworth and Wolf, 1976). Thus, the behavior of the birds was similar to organisms that appear to select food in the laboratory almost exclusively by concentration (Epstein, 1967; Dethier, 1976). The selection of a less efficient food appears paradoxical with respect to an economic interpretation of feeding. However, this assumes that hummingbirds (or other organisms) in natural situations have choices similar to those used in the laboratory. The results seem less paradoxical when interpreted in light of the characteristics of food normally available to the birds.

B.

NATURALINTERPRETATIONOF HUMMINGBIRD FOODCHOICE

In the coevolutionary relationship with hummingbirds, plants could have evolved characteristics that influence rate of net caloric intake through either the rate of consumption of nectar andor its caloric value. The latter is determined by

62

F. REED HAINSWORTH AND LARRY L. WOLF

sugar concentration, and hummingbirds assimilate essentially 100% of ingested sugars over the range of concentrations normally found in plant nectar (0.25-2.0 M sucrose, Hainsworth, 1974). 1 . Natural Determinants of Volume Intake Rate

The major determinants of volume intake rates are the corolla lengths and nectar volumes of flowers relative to the feeding apparatus of the hummingbirds. Hummingbirds insert their bills into flowers to consume nectar secreted and stored at the base of the corollas (Wolf et a l . , 1976). Nectar is consumed as they lick their tongues 3 4 times per second. The tongue is forked and contains two open grooves that carry nectar (Hainsworth, 1973). The hyoid apparatus permits extension of the tongue; but species with relatively short tongues compared to corolla lengths have difficulty consuming the nectar (Fig. 3). Nectar volume influences rate of volume intake (Fig. 3) through the amount obtained per lick. At low nectar volumes, successive tongue licks return proportionally smaller volumes for species with relatively large tongues. Also, the length of the tongue that contacts the nectar appears to be more important in maximizing rate of intake from flowers with relatively large volumes (Hainsworth, 1973). In the laboratory hummingbirds prefer to visit feeders that provide higher volume rates of intake if concentration is the same (Hainsworth and Wolf, 1976).

I._.

0

5

d E fulpms

Y)

1

5

2

0

2

5

3

0

U

4

0

4

5

COROLLA LENGTH(mm1

FIG.3. Rate of intake as a function of corolla length from artificial flowers with different volumes of sugar water. Values are means ? 2 S.E.Data for 3 individuals of Eugenes fulgens and for one female Archilochus alexandri.

FEEDING: AN ECOLOGICAL APPROACH

63

If plants evolved to attract pollinators by influencing volume rate of intake, then variable rates of nectar production would be sufficient at many corolla lengths to affect intake rates (Fig. 3). Hummingbirds with relatively small tongues could achieve rates of intake near the maximum possible from flowers with small nectar volumes since relatively small volumes could load their tongues. Larger hummingbirds with larger tongues would be expected to visit flowers that contained larger nectar volumes where corolla lengths would influence volume rates of intake (Fig. 3). Small species of hummingbirds may be excluded from visiting these flowers by the long corollas. This suggests that food selection by a hummingbird species may be limited under natural circumstances by maximum achievable volume rates of intake. In support of this, there is evidence that plants with small flowers produce relatively small quantities of nectar; and naturalists have noted that there is a good relationship between the bill length (related to tongue length) of hummingbirds and the corolla lengths of flowers they normally visit for food (Grant and Grant, 1968; Snow and Snow, 1972; Wolf et a l . , 1976). This is similar to the relationship between “tongue” length and flower morphology for bees and the plants they pollinate (Brian, 1957; Heinrich, 1975).

2. Nectar Concentrations in Natural Foods To assess nectar concentration as a natural economic determinant of food choice requires assessing the ability of hummingbirds to discriminate foods of different concentrations within the range of values normally found in plant nectars. Most plant nectars are composed of sucrose, glucose, andor fructose, and energy value can be measured easily by refractive index (Hocking, 1968; Hainsworth and Wolf, 1972b; Baker, 1975; Stiles, 1975). Sugar concentrations of nectar have been measured for a variety of plant species in several habitats (Hainsworth and Wolf, 1972b; Stiles, 1975; Baker, 1975). Within any locality, nectar concentrations are variable among plant species (Table 11). However, laboratory experiments indicate that the ability of hummingbirds to detect a difference depends on the absolute concentration as well as the difference (Table 111). Most, but not necessarily all, plants in an area produce nectar with differences in concentration that could not be detected (Tables I1 and III), suggesting that many plant species have not evolved differences in nectar concentrations to attract particular hummingbird species. This can be understood by visualizing what might happen if these plants competed for pollinators with adjustments in nectar concentration. If one evolved a detectably higher concentration, others could evolve even higher concentrations; but as the absolute concentration increased, it would take a larger difference to be detected (Table 111). Eventually excessive energetic cost could begin to reduce the fitness of the plant. What about plants that produce detectably higher sugar concentrations (e.g., Tropaeolum and Salvia in Table II)? These concentrations may result from

64

F. REED HAINSWORTH AND LARRY L. WOLF

TABLE L1 NECTAR CONCENTRATIONS FOR PLANTS POLLINATED BY HUMMINGBIRDS IN A HIGHLANDHABITAT IN COSTA RIGA'

Species

Mean and range of equivalent sucrose concentration

Thecophyllum orosiense Bomarea costaricensis Tropaeolum morirzianum Fuchsia microphylla Fuchsia splendens Cavendishia smirhii Macleania glabra Salvia iodochroa Casrilleja irasuensis Centropogon talamancensis C . valerii C . brumalis Cirsium subcoriaceum

0.50 (0.44-0.53) 0.61 (0.54-0.65) 0.90 (0.86-1 .OO) 0.56 (0.52-0.66) 0.40 (0.29-0.53) 0.44 (0.384.51) 0.48 (0.384.54) 0.90 (0.72-1.06) 0.47 (0.384.60) 0.44 (0.30-0.52) 0.47 (0.42-0.59) 0.38 (0.37-0.42) 0.59 (0.514.66)

“From Wolf er al. (1976).

competition with plants pollinated primarily by insects (Hainsworth and Wolf, 1976). Many insect-pollinated plants produce more concentrated nectar than larger flowers visited by some hummingbirds (Baker, 1975). Nectar volumes of most of these plants are low so they would be relatively inefficient for most large hummingbirds (with large tongues). However, smaller hummingbirds have lower costs for flight and they can more efficiently consume small volumes. This means that plants that have evolved to be pollinated primarily by small hummingbirds should have nectar that is not detectably less concentrated than nectar in the insect-pollinatedplants these birds might visit. Otherwise, the preferences TABLE I11 MINIMUMREQUIREDDIFFERENCE IN CONCENTRATION TO BE SUGAR CONCENTRATIONS‘ DISCRIMINATED AT DIFFERENT

Sugar concentration (molar sucrose) 0.35 0.50 0.80 I .20

“From Hainsworth and Wolf (1976).

Minimum required difference (molar sucrose) 0.05 0.10

0.20

> 0.20

FEEDING: AN ECOLOGICAL APPROACH

65

of the birds for concentrated nectar would result in their visiting the primarily insect-pollinated plants. In this context, a major difference in available nectar volumes could influence selection by small hummingbirds through variations in volume intake rates. 3. Laboratory versus Natural Preference Behavior

Under natural conditions the major determinants of net energetic benefits from food choice are based on volume rate of consumption. In the laboratory the hummingbirds behave according to caloric value. Caloric value also is important in some natural situations. We have observed one species (Panterpe insignis) that visited and defended flowers of a plant (Tropaeolurn moritzianum) that produced high nectar concentration but was less efficiently exploited (benefits were less relative to costs for consuming nectar) than other species the hummingbird could have visited (Wolf el al., 1976). An explanation in mechanistic terms for the laboratory and limited field observations suggesting inefficient food choice may relate to the preference portion of a “preference-aversion” function. If the weight of a meal influenced rates of net energy gain, selecting a higher concentration would reduce total weight of a calorically constant meal and would yield a higher rate of net energy gain (see Section IV, B). Additionally, if natural selection resulted in preference for the most concentrated nectar but never for a less concentrated nectar then high concentrations could.represent “supernormal” stimuli for hummingbirds (stimuli that are always significantly responded to, see Staddon, 1975). However, under most natural situations, volume rate of consumption appears to be the important variable so “inappropriate” food selection would be rare. Discrepancy between laboratory and natural situations could provide a rationale for interpretations of feeding behavior in other species. For example, laboratory observations that some seed-eating birds and mammals select food based on volume rate of intake to the detriment of rate of net energy gain (Rosenzweig and Sterner, 1970; Willson and Harmeson, 1973) could have a natural, economic basis if seeds normally available to these granivores differed little in energy value. Rate of intake would then provide the best cue to rate of net energy gain.

c.

OTHER

DETERMINANTS OF FOODCHOICE

I . Nutritional Factors

Energetic costs and benefits form only one basis for an economic explanation for food selection. As we indicated earlier, nutritional deficiencies or poisons also are likely to influence food choice. Nutritional aspects have been extensively studied, and the experiments of Rozin (1976) and Garcia et al. (1966) on learned

66

F. REED HAINSWORTH A N D LARRY L. WOLF

aversions with respect to nutritional deficiencies and poisons emphasize their importance. A well-documented, natural case is the effect on avian predators of the model-mimic relationship for Monarch and Viceroy butterflies (Brower and Brower, 1964). Cardiac glycosides sequestered by Monarch butterflies cause vomiting in Blue Jays. The experience modifies food choice and has an effect on costs and benefits for feeding (Freeland and Janzen, 1974). Feeding of hummingbirds could be influenced by nutritional factors since nectar contains small quantities of amino acids (Baker and Baker, 1975; Cruden and Hermann-Parker, 1977). Although hummingbirds probably normally obtain most noncarbohydrate nutrients by catching insects, it is possible that amino acids in nectar could supplement their nutritional requirements. However, choice experiments suggest that hummingbirds do not prefer food containing amino acids (Hainsworth and Wolf, 1976). In many cases, if the concentration of amino acids was increased above values normally found in nectar, the birds rejected them. Amino acids may be present in nectar as an “accident” related to sugar production (Baker and Baker, 1975; Hainsworth and Wolf, 1976). Preference experiments involving all combinations of the sugars sucrose, glucose, and fructose at equal caloric value suggest that variations in sugar composition also may be relatively unimportant as determinants of food choice for hummingbirds (Stiles, 1976; Hainsworth and Wolf, 1976). 2. Food Abundance We have discussed food choice independently of differences in abundance of different foods. A variety of economic theories of diet composition suggest a crucial importance for absolute abundance of different prey types (Emlen, 1966, 1968; Schoener, 1969b, 1971; Pulliam, 1974; Estabrook and Dunham, 1976). They all suggest that high quality items should be selected as encountered. Lower quality items should be added to the diet as absolute abundance of preferred prey declines. Relative abundance should play a minor role (Krebs er af., 1977; but see Murdoch and- Oaten, 1975). In practice, many laboratory studies provide food in excess of requirements making it hard to document these proposed abundance effects. An effect of abundance on food selection has been examined in the context of specialization by predators on prey types as a function of the encounter rate with profitable prey. Krebs et af. (1977) studied this in Great Tits (Parus major) by measuring the percent selection of whole versus half meal worms from a conveyor belt moving through a cage. As the number of more profitable prey that could be taken increased, selection of those prey increased, but not in a step-wise or threshold manner as predicted by theory. Krebs et al. (1977) attributed the persistence of some less profitable prey in the diet to “sampling behavior” or some mechanism related to assessing changes in prey quality.

FEEDING: AN ECOLOGICAL APPROACH

67

Captive sunfish (Lepomis mucrochirus) added smaller size classes of Duphniu to their diet as the absolute abundance of the largest prey size declined (Werner and Hall, 1974). This was interpreted as support for an optimal diet model based on maximizing energy intake per unit handling time. However, O’Brien et al. (1976) reinterpreted these data in light of their hypothesis that the fish selected the prey items that appeared largest at the time of a capture decision. In their model, a small prey item could appear largest (and perhaps yield higher net energy by requiring relatively less energy to capture) by being much closer to the predator. According to the O’Brien er ul. model, as abundance of the smaller prey increased at a constant absolute abundance of large prey, the smaller prey should appear more often in the diet. The Werner and Hall model predicts that the choice is determined only by the absolute abundance of the large prey and should be independent of the abundance of small prey. Controlled laboratory experiments should be able to discriminate these hypotheses by more careful definition of realized costs and benefits associated with prey size discrimination. Goss-Custard (1977) noted that redshanks feeding on worms in the field selected prey based on the absolute density of large worms and not on the density of small worms. Small worms were added to the diet only as the density of large worms declined and not in a proportional manner. This tends to support the predictions of the optimal diet models that are unconstrained by mechanisms of selection. Gill and Wolf (1975a) reported that several species of sunbirds tended to select among alternative types of mistletoe flowers in a way that maximized total reward per unit foraging time. In this case, total foraging time was strongly influenced by the very patchy distribution of the clusters of flowers. Differences between bird species in the proportion of the higher quality flower type selected depended on differences in efficiencies of exploiting the two flower types. A basic assumption of many economic theories dealing with abundance effects on prey selection is that prey are randomly distributed. This may apply to some natural situations, but many others can involve patchy prey distribution. Also, depending on resource renewal, predator selectivity can generate a patchy distribution from an initially random prey distribution. Factors governing patch exploitation generally are considered separately, and we will treat the subject in a separate section (Section V). IMAGES”A N D FOODCHOICE D. “SEARCH Food selection by hummingbirds at the level of item choice is characterized by conspicuous flower color and morphology (Grant and Grant, 1968). However, for many nonmutualistic predator-prey relationships, prey have evolved mechanisms to avoid predator detection. With changes in prey abundance and quality, efficient feeding may depend on a predator’s ability to detect changing

68

F. REED HAINSWORTH A N D LARRY L. WOLF

characteristics of prey. In this context, a considerable literature exists on the concept of “specific search image” formation (for detailed discussions, see Dawkins, 1971; see also review in Krebs, 1973). Tinbergen (1960) attempted to explain changes in the proportions of those prey items selected with changes in their density by hypothesizing that avian predators could form specific search images for certain cryptic prey. As Krebs (1973) points out, this hypothesis describes what is observed rather than explaining why it occurs. We would expect a predator to employ any mechanism available to increase the profitability of its feeding. An important question is whether and how the mechanisms underlying feeding result in economical food selection (Royama, 1970). Dawkins (1971) and Krebs (1973) list various types of learning which should be excluded before accepting the search image formation hypothesis. These generally involve learning associated with place, path of search, handling time, or avoidance of alternative prey. Even though these types of mechanisms for changing feeding behavior may not strictly involve a “search image” for prey characteristics, they could contribute to efficient feeding (see Section V).What is required is information on the consequences to a predator for the different mechanisms. Experiments that examine mechanisms underlying economic feeding where differences in profitability can be demonstrated will contribute substantially to an assessment of the importance of different mechanisms for food selection.

IV. FEEDING PATTERNS Once food is selected, the quantity of energy consumed relative to expenditures determines the timing of feeding episodes. The general relationship between food and its use by an organism is illustrated in Fig. 4. Feeding behavior is interposed between aspects of the resource (quality, quantity, etc.) and internal factors. For most organisms, food initially is held in a specialized internal organ (e.g., a stomach or crop). From this, energy is provided for two general processes: immediate short-term maintenance and storage for nonfeeding periods or for periods when energy demands exceed short-term intake. Energy storage usually is considered to be primarily in the form of calorically dense fat that permits carrying energy at minimum cost (King, 1974). Energy for immediate maintenance while feeding probably does not come from storage since some energy is lost converting carbohydrate to fat and back (Milligan, 1971). More direct utilization of food energy would provide for immediate expenditures without this cost. Recent physiological studies of energy regulation examined possible controls of onset and termination of individual feeding episodes. The rationale is that a

FEEDING: AN ECOLOGICAL APPROACH

69

SHORT TERM MAINTENANCE

,

FOOO HOLDING

\

\

\

\ \

/

I

'

FEEDING

(MI fnqurncy ond rim]

I

FOOD [quality, quantity,otc.)

FIG.4.Model of energy use at the level of interaction between an organism and its food supply.

daily pattern of caloric regulation may be reflected in individual components (meals). A daily control mechanism could be thought of as the sum of mechanisms operating over shorter time intervals. This hypothesis has its critics (e.g., Panksepp, 1973; Panksepp and Krost, 1979, but supporting evidence for some organisms comes from analysis of food intake from individual meals relative to intervals prior to and following meals. For rats (Snowdon and Wampler, 1974; LeMagnen, 1976), mice (Petersen, 1976), chickens (Duncan etal., 1970), Zebra Finches (Slater, 1974), and hummingbirds (Wolf and Hainsworth, 1977), for example, length of time to the next feeding is correlated with the prior but not the following time feeding (or meal size). The correlation with postmeal intervals suggests regulation of feeding initiation relative to rate of use of energy consumed in a meal. For hummingbirds, we have shown that caloric intake in the laboratory relative to caloric expenditures determines time to the next feeding. Observations under natural conditions indicate that these meal relationships are not laboratory artifacts (Wolf and Hainsworth, 1977). Control of meal initiation and termination may be related to some metabolic consequence of the functioning of food holding organs. These probably empty in an exponential manner (i.e., proportional to contents) as generally shown in Fig. 5 (Gelperin, 1966; Hunt and Knox, 1968). The supply of energy from the organ should respond to use of energy for both maintenance and storage. Effects of the storage component are seldom specified. However, rats ingest excess energy relative to intermeal expenditures at night, and the excess is stored in fat and utilized during the day when fewer calories are ingested per meal relative to intermeal expenditures (LeMagnen and Devos, 1970; LeMagnen et al., 1973). Kendeigh er al. (1969) found that energy storage by House Sparrows (Passer domesricus) and White-throated Sparrow (Zonotrichia albicollis) varied with overnight energy expenditures. Also, hummingbirds store energy relative to

70

F. REED HAINSWORTH AND LARRY L. WOLF

P

INTfIYfAL

4

4

-

lNlfRVALS

4

TIME

-0

b

FIG.5 . A general emptying function for a food holding organ. Arrows denote meal initiation (i) or termination (T). (A) and (B) refer to different rates of emptying that may influence meal initiation. (C) and (D) refer to different meal sizes that may influence meal initiation.

overnight costs (Hainsworth, 1978). The rate of net energy gain for hummingbirds is relatively constant within a day (see Fig. 8) and with ad libitum access to a high quality food source gains generally are sufficient for overnight expenditures (Wolf and Hainsworth, 1977). A.

MEALINITIATION

Feeding initiation (frequency) and termination (meal size) should influence the economics of feeding. In terms of physiological mechanisms, feeding initiation could be triggered by some internal signal related to energy balance (Toates and Booth, 1974; Friedman and Sticker, 1976). In Fig. 5, this is depicted as some threshold related to contents in the food storage organ, although the storage organ need not supply the control signal. In hummingbirds and chickens, feeding initiation may be correlated with energy depletion from the crop (Duncan er a l . , 1970; Wolf and Hainsworth, 1977), but the actual controlling signal is unknown. For some mammals, factors related to energy utilization have been suggested as control signals and these form the basis of “glucostatic,” “thermostatic,” “lipostatic,” and “hepatostatic” control theories applied to individual feeding episodes (DeCastro and Balagura, 1975a; Sanderson and Vanderweele, 1975; LeMagnen, 1976; Stevenson and Fierstein, 1976). For other organisms the threshold need not be sensitive to food energy per se. For example, “contents”

FEEDING: A N ECOLOGICAL APPROACH

71

in Fig. 5 do not appear to be in energy units for guinea pigs (Hirsch, 1973), cats (Kanarek, 1975), and oppossums (Maller et al., 1965) since dilution of their food results in no short-term compensation in intake. The energy depletion relation explains differences among intermeal intervals with differences in food quality. Food quality could influence intermeal intervals by generating emptying curves with lower slopes as quality increased (e.g., A + B in Fig. 5) or through a change in meal size (e.g., C * D in Fig. 5). In blowflies, crop emptying is controlled by blood osmotic pressure which is influenced by rate of use of energy for both maintenance and storage (Dethier, 1976). Also, stomach emptying in mammals is related to meal concentration through duodenal osmoreceptors and feedback mechanisms responsive to fatty acid concentration (Hunt and Knox, 1968; Anderson, 1973). Situations may occur where imprecise internal signals for initiating feeding could result in low or negative net energy gains from one meal to another. For example, the asymptotic form of the general emptying function in Fig. 5 could result in imprecise signals for feeding depending on intake. One factor that could influence rate of emptying is the quantity of food consumed (Gelperin, 1966; Hunt and Knox, 1968), and there is evidence that smaller than average meal sizes in hummingbirds can result in low or negative net energy gains (Wolf and Hainsworth, 1977). However, this is likely to be rare since other cost:benefit factors influence the size of meals for hummingbirds. For other organisms, such as hamsters (Silverman and Zucker, 1976), energy requirements for daily maintenance and storage do not appear to influence short-term feeding. Hamsters deprived of food require longer than daily intervals to replenish energy reserves. This observation may be related to environmental factors (such as food availability from hoarding) that could generate efficient net energy gains without short-term (daily) feedback associations (Silverman and Zucker, 1976). For hummingbirds, a major determinant of feeding frequency appears to be the rate of use of energy for maintenance between meals. Hainsworth (1978) revised a predictive economic model of hummingbird feeding (DeBenedictis et al., 1978) to incorporate overnight storage effects on energetics and predicted that overnight costs would have little effect on feeding frequency while maintenance costs during the day would have a major impact. The model was based on the assumption that hummingbirds fed to maximize the rate of net energy gain. Experimental tests supported the predictions since decreased temperatures during the day increased feeding frequency while decreased temperatures overnight did not (Hainsworth, 1978).

B. MEALSIZE For many organisms, a meal would continue after initiation until some control mechanism(s) signal(s) cessation. In practice it often is difficult to define a meal

72

F. REED HAINSWORTH AND LARRY L. WOLF

since feeding could be interrupted for reasons other than a control signal. Slater (1974) dealt with this problem by using discontinuities in frequency distributions of intermeal intervals to define feeding bout length for Zebra Finches (Poephila guttata). Hummingbirds and some Zebra finches in ad libitum feeding situations have approximately normal frequency distributions of bout lengths (Slater, 1974; Wolf and Hainsworth, 1977). The meal size for hummingbirds is generally less than half the quantity they could store in their crops (Hainsworth and Wolf, 1972b). The characteristic size of meals for hummingbirds is independent of rate of intake (except at very low rates of intake) of either fluid or calories and is a linear function of body mass (Wolf and Hainsworth, 1977; DeBenedictis et al., 1978). Although we have no information concerning signals that terminate feeding in hummingbirds, we have attempted to explain meal size by constructing a benefitcost model from the energy budgets of hummingbirds from one meal to the next (DeBenedictis et a l . , 1978) for an ad libitum laboratory feeding situation (detailed in Wolf and Hainsworth, 1977). We assumed the mass of a meal influenced energetic costs for flight. We also constructed models where change in mass as a result of feeding influenced sitting costs (from a possible postural effect). We hypothesized that birds may adjust meal size to maximize rate of net energy gain. We also examined other possible criteria such as maximization of net energy gain per feeding bout, maximization of efficiency per bout (gains/ cost), and minimization of feeding time (DeBenedictis ef a l . , 1978). From independent measurements of food intake of hummingbirds (from Wolf and Hainsworth, 1977), we compared predicted volumes under various criteria with observed average volumes consumed per meal. Models which minimized feeding time or maximized net energy gains per bout predicted meals in excess of observations. Models which maximized efficiency or maximized rate of net energy gain predicted meal sizes very similar to those observed (DeBenedictis ef a l . , 1978). Although we cannot discriminate these two criteria, rate of net energy gain may be more easily measurable in physiological terms and may be sensitive to a daily storage component. The physiological signals that govern meal size in hummingbirds by terminating feeding should operate to maximize rate of net energy gain. Hainsworth (1978) revised the economic model of hummingbird feeding and incorporated overnight storage of energy in the DeBenedictis et al. ( 1978) model to extend it to a daily time scale. The revision predicted that overnight energy expenditures would influence meal size for the subsequent day, and experimental tests supported the predictions, although changes in meal size also produced some changes in feeding frequency (Hainsworth, 1978). Thus, at least part of the adjustment for hummingbirds with respect to daily storage requirements appears to be through meal size; while adjustments with respect to daytime maintenance requirements appear to be primarily through feeding frequency.

FEEDING: AN

c.

ECOLOGICAL APPROACH

73

OTHER INFLUENCES ON MEALPATTERNS

Why should organisms have storage organ capacities that exceed the most economical meal sizes? For hummingbirds, our analysis of meal patterns has been restricted to the laboratory where some important natural constraints may not apply. By varying parameters in the predictive models of meal patterns, we have identified some potentially important factors. In the models, meal size is a direct square root function of flight time to and from a perch (DeBenedictis et af., 1978), so for long flight times to a food source we predict larger meal sizes. Also, a shorter day length should increase meal size through the overnight storage requirement (Hainsworth, 1978). Experimental tests of these predictions may suggest additional influences on meal patterns. For other species the contribution of meal patterns to the economics of feeding under natural circumstances often is not clear, but we have listed a number of effects and responses for several species in Table IV. The predominance of an effect on meal size in species such as the laboratory rat may indicate less constraint on a characteristic meal size than for hummingbirds (Table IV) perhaps as a result of different costs associated with meal sizes.

v.

ECONOMICS OF PATCH EXPLOITATION

Energy requirements in nectar specialists are satisfied in the real world primarily by visiting flowers. Because of differences in nectar production rates among plants, the birds are continually presented with the potential choices among food items discussed in the preceding sections. Additionally, foraging in bouts (i.e., meals where only a fraction of the total flowers are visited) generates spatial variation of nectar content of the flowers. Thus, the birds are faced with a patchy food environment. Furthermore, the spatial patchiness and the mean and variance of patch quality can change continually. Any explanation of the regulation of energy balance must consider controls of feeding behavior which may depend on food patch characteristics. Initially we can assume the distance between patches (measured as time and/or energy) is approximately equal, or at least independent of reward within a patch and that rate of net reward is highest in the richest part of the environment (MacArthur and Pianka, 1966; Wolf et af., 1975), although which portion is richest may vary (Charnov, 1976b; Gill and Wolf, 1977). The model of patch utilization should be similar to the food choice model in optimal diet theory in which breadth of diet is predicted to change with changing food density (see Section IIIC; Pulliam, 1974; Werner and Hall, 1974; Estabrook and Dunham, 1976). With costs equal, the values of the reward would determine net benefits. In general, the value of a patch is an increasing function of average nectar content of

TABLE IV RESFONSES TO VARIOUS INFLUENCES ON MAINTENANCE OR STORAGE SOMEMEALPATTERN

Animal

Laboratory rat

Influence on maintenance or siorage Decreased food quality Increased food quality Food deprivation (24 hours) Low temperature

Reentry to warm temperature Alloxan diabetes Ventro-medial hypothalamic lesions Increased food quality in diurnal period Decreased accessibility of food (rate of intake) Ovariectomy Vagotomy plus lateral hypothalamic lesions

Meal pattern response" Increased meal size Decreased meal size Increased meal size Decreased nocturnal meal frequency Long-term increased meal size (-4 days) Increased nocturnal meal frequency Decreased meal size Increased meal size Increased diurnal meal size relative to expenditures Increased food intake in diurnal period Increased meal size Decreased meal frequency Increased meal size Decreased meal frequency Absence of postmeal correlation

Reference Levitsky and Collier (I%@

h u n g and Horwitz ( I 976)

Thpmas er al. (1976) LeMagnen et uf. (1973) Panksepp and Krost (1975) Levitsky ( 1 974)

Kenney and Mook (1974) Snowdon and Wampler (1974)

Rabbit Guinea pig

Cat

Mouse

Hummingbird

Pigeon

Cross blood perfusion from obese donor Cross blood perfusion from lean donor Anosmia Care of young through nursing Infusion of noradrenaline into forebrain at meal initiation Streptozotocin diabetes Growth Vagotomy Growth Food deprivation Apparent decrease in food quality Increased activity for food Reduced food quality Increased activity for food Pro-oestrous

Metoestrous Increased food quality Decreased food quality Decreased rate of intake Food deprivation

Decreased meal size

King (1976)

Increased meal Increased meal Increased meal Increased meal

LaRue and LeMagnen ( 1972) Fleming (1976) Ritter and Epstein (1975)

size size (from nibbling) size and frequency size

Increased meal size Increased meal size Increased meal frequency Increased meal size First meal size increased No change Increased meal size No change Increased meal size Increased meal size for palatable food Decreased meal size for relatively unpalatable food Increased meal frequency Decreased meal frequency Increased meal frequency No change Increased meal size

DeCastro and Balagura (1975a)

DeCastro and Balagura (1975b) Sanderson and Vandenveele (1975) Hirsch ( I 973)

Kanarek ( 1975) Petersen ( 1976)

Wolf and Hainsworth (1977)

Zeigleretal. (1971)

“A response depends on the definition of a meal. These may vary considerably, but we have listed responses as reported in the references. The list was completed in September, 1977.

76

F. REED HAINSWORTH AND LARRY L. WOLF

flowers in a patch. We can illustrate this with laboratory data (Fig. 6). The shape of the curve is a negatively accelerating exponential. As the initial volume per flower increases, added volume provides decreasing additional benefit to a point at which there is effectively no further increased benefit associated with higher volumes. We also must consider how the net benefit curve is translated into biological attributes that influence organism “fitness.” In Fig. 7 we show how changing net benefits per time may influence total foraging time. If we assume an organism can maximize fitness by minimizing foraging time (time minimizer, see Schoener, 1971), then it would be advantageous for the organism to select the highest available rewards, at least to some asymptote. Minimizing foraging time can be considered to increase fitness in a variety of ways, including: (a) providing additional time for other activities such as courtship or predator avoidance, (b) reducing the time foraging, which could reduce exposure to predators, intense radiation, etc., and (c) providing needed flexibility in times of shifting reward levels. For most territorial nectar feeders, total foraging time is sufficiently small (7-50% of daylight hours) as a proportion of the total available time (Wolf and Hainsworth,. 1971; Stiles, 1971; Wolf, 1975; Gill and Wolf, 1975b; Carpenter and MacMillen, 1976; Hainsworth, 1977) that we can assume they usually are acquiring sufficient resources. In our laboratory experiments, hummingbirds

pI IFLOWER

FIG.6. Relation between net benefit per unit time and the volume of sugar water (0.5M sucrose) contained in artificial flowers. Net benefit is calculated from the intake in calories minus the caloric cost from the time spent extracting the sugar water. The two curves are for flowers with different corolla lengths with the longer corolla producing a reduction in rate of intake.

FEEDING: AN ECOLOGICAL APPROACH

77

FIG. 7. Theoretical relationship between the ratio of benefits to costs of foraging and the proportion of time spent foraging based on the assumption that a sunbird will attain a neutral energy budget over a 24-hour period. The curves specify the required foraging efficiency (benefitkost) for particular foraging times. The cost portion is all costs per unit time associated with foraging. The benefit term is the total intake per unit time from the sugar in the flower nectar, assuming 100% assimilation.

apparently do not absolutely maximize their rate of net energy gain but achieve a level that is coincident with requirements over perhaps a 24-hour basis, modified seasonally to incorporate storage for uses such as for molt, breeding, and perhaps migration (see Section IV; see also Katz, 1974). If foraging times increased beyond 30-50% of daylight hours, the birds in natural situations would be operating under conditions in which smali shifts in net benefits would have dramatic effects on foraging time (Wolf et al., 1975). When foraging time is very high, we assume the birds are doing about as well as they can. However, if foraging time is low, and the birds could achieve even higher rates of net energy gain, it would have virtually no impact on their feeding time (Wolf et al., 1975). We might expect nectar feeding birds, at least in the nonbreeding season, to attempt to minimize foraging time by maximizing rate of net energy gain to achieve maximum fitness. This could be achieved by selecting flowers with greatest nectar volumes, although additional benefits tend to decrease with increasing average availability. With variation in available nectar per flower we would expect the birds to feed nonrandomly by feeding preferentially from flowers with the most nectar. The range of nectar volumes that should be selected will depend on total energy availability relative to individual demands. Low availability would necessitate that a larger range of volumes be selected than if availability was high. At high availability, random foraging could produce similar time budgets to nonrandom foraging. We will deal primarily with the way in which foraging organisms respond to patches of different qualities; but before proceeding we need to consider possible

78

F. REED HAINSWORTH A N D LARRY L. WOLF

definitions of a patch. The smallest potential patch for feeding nectarivores is within a flower. Nectar in a flower may initially occur as small droplets at several nectaries. However, as volume increases, the droplets coalesce. Use of volume within a single flower as measure of patch quality by a foraging bird could then involve either accepting or rejecting a flower depending on the size of the individual droplets. Several flowers may be clustered together on a single inflorescence so birds could use information from a few flowers as an index to the quality of the others (Gill and Wolf, 1977; F‘yke, 1978b). Additionally, depending on the dispersion pattern of inflorescences or plants, the birds may recognize other patches of variable size within a larger array. While some “patches” may be obvious to an observer as clumps of inflorescences, it is not certain that the birds use the same information. It is likely that they continually redefine patch boundaries as they forage, and that definition of the size of a patch may vary within and between foraging bouts. An organism potentially has available two general nonexclusive types of information about patch quality: (a) a priori information where it “knows” the relative value of a patch prior to a visit and (b) a posteriori information where the patch must be visited before information is obtained on patch quality. Obviously, most a priori information is available only as a result of previous visits, so the distinction between a priori and a posteriori is primarily behavioral. Both types of information are potentially available, and there are some data to suggest that sunbirds and other nectar feeders use both (Gill and Wolf, 1977). However, the benefit from the two types differs since using a posteriori information requires more time and energy commitment for the same total intake per feeding bout. With relatively poor patches, the time and energy could be better spent with an a priori assessment of patch quality. Both types require some decision making, but a priori assessments more directly involve memory in a classic learning sense than a posteriori. Generally, memory is retention of environmental information. For a priori foraging decisions, an organism must obtain information about patch quality characteristics before moving to the patch. In cases in which resources are depleted by feeding, this may require “remembering” where previous feeding occurred or perhaps when a particular foraging site was last visited. Ability to make appropriate decisions based on this information will depend on the renewal rate of the resource in relation to the information storage capacity of the individual. As time for renewal increases, making the value lower for a specific time span (at least to the asymptote; see Fig. 6), this information value decreases. If information storage partly depends on its value measured as rate of net benefits, we would expect organisms to use memory most often in situations with high renewal rates, such as nectar production in flowers, and less often in situations of long-term renewal, such as seeds that are produced once a year.

FEEDING: AN ECOLOGICAL APPROACH

79

Memory in a posreriori decisions depends on what information is integrated. As we shall see, it is likely that many foraging individuals integrate at least information about immediately preceding direction and distance moved and probably also about average quality of recently visited patches. Without trail marking systems, such as occur in ants, some bees, and slugs, it seems mandatory that these organisms have a memory of locations just visited. On the other hand, to integrate information about average environmental quality may require only an energy storage compartment that can be monitored through time. High quality environments would fill the compartment faster than low quality environments. Preliminary data for hummingbirds suggest that they not only store energy at an approximately constant rate during the day (Fig. 8)

TIME OF DAY FIG. 8. Pattern of energy accumulation by two hummingbirds maintained on a 14L:lOD photoperiod with 0.5M sucrose. Ambient temperature averaged 23°C for an Archilochus ulexundri (Black-chinned Hummingbird) and a Lampornis clernenciae (Blue-throated Hummingbird).

80

F. REED HAINSWORTH AND LARRY L. WOLF

(Wolf and Hainsworth, 1977) but also that they may modify the rate of storage according to the initial size of the store already in the compartment at the beginning of foraging activity for the day. Kendeigh er al. (1969) noted similar effects for two granivorous species of birds. Thus, a bird with a depleted energy store early in the day would accumulate energy faster. We should also note that an organism’s view of what is a full store undoubtedly changes in relation to seasonal changes in energy requirements (e.g., for breeding, molt, etc.; King, 1 974). A. A Priori INFORMATION

Ideally, decisions on patch quality before feeding could be achieved if a patch signaled quality. This is only likely to occur where there is an advantage to the food being eaten, as in animal-pollination and dispersal systems. For nectarfeeding organisms, patch quality might be signaled by number of flowers, their color (Grant and Grant, 1968), or differences in flower quality that might be assessed without probing all flowers. For example, Gill and Wolf ( 1 975a) postulated that patch value of mistletoe (Phragmanthera s p . ) flowers on Acacia trees in East Africa to foraging sunbirds depended on relative proportions of mature, closed flowers (high quality) and open flowers (low quality). The flower types differed in color and morphology so a bird had cues to assess patch quality but probably not from a very great distance. Some territorial sunbirds feeding at Leonoris flowers biased their visits so the number of visits per patch were more equal across all patches observed than expected from a random foraging model (Table V) (Gill and Wolf, 1977). In each case of a nonrandom (non-Poisson) frequency distribution of visits per patch, the bias was always such that the variance to mean ratio was less than one. TABLE V RANDOMA N D NONRANDOM PATTERNS OF VISITATION TO INFLORESCENCES BY RESIDENT (NONTERIUTORIAL BUT WITH RESTRICTED FORAGING RANGE)A N D TERRITORIAL SUNBIRDS FEEDING ON NECTARPRODUCED BY LeOnOfiS nC’pfif d i u IN EASTAFRICA“ INCIDENCE OF

Resident Territorial

Random

Nonrandom

6

I II

10

“Random is defined as a frequency distribution of visits per inflorescence that is not significantly different from a Poisson distribution while nonrandom is a significant departure from Poisson. Data from Gill and Wolf (1977).

FEEDING: AN ECOLOGICAL APPROACH

81

This suggests that the birds were biasing visits to patches visited least recently such that a greater than expected proportion of the patches were visited once before second and subsequent visits. This decreased the variance of time between visits and increased the average amount of nectar per flower in each patch visited over what was expected if the bird foraged randomly. In several bird-flower systems,birds tend to bias foraging visits to plants (or stalks) that have more open, nectar producing flowers that are morphologically distinct from both younger and older flowers (Wolf, unpublished observations). In this situation more frequent visits to the stalks with more flowers mean that the average available volumes per flower on a visit may be less than if the birds randomly visited available patches. At this juncture we can hypothesize that the behavior results from the importance of total reward per stalk rather than average reward per flower, perhaps because of costs of moving between stalks. This hypothesis predicts that as the density of stalks increases the importance of between stalk costs decreases and the importance of flowers per stalk should also decrease. We are concerned here only with which inflorescences are visited, not which are emptied once a visit is made. In an Aloe-sunbird foraging system with a relatively low density of flowers, the birds regularly biased visits to the plants or clumps with the most flowers (Wolf, unpubl.). In a Leonoris-sunbird foraging system in which stalk and patch densities were very high, the birds did not preferentially visit inflorescences with higher average numbers of flowers (for details, see Gill and Wolf, 1977). The general hypothesis relating visits per stalk and flower density is presented graphically in Fig. 9. Note that, although the actual shape of the curve could be somewhat different, we have suggested a smooth transition with a monotonically

I FLOWER DENSITY

-

FIG.9. Hypothetical relationship between the variance to mean ratio of the number of visits to a particular inflorescence and the average inflorescence density. A ratio of 1 .O indicates a random distribution of visits per inflorescence; a ratio significantly greater than 1 .O indicates a bias toward particular inflorescences, perhaps those with most flowers; a ratio significantly less than I .O indicates that each inflorescence receives approximately the same number of visits.

82

F. REED HAINSWORTH AND LARRY L. WOLF

decreasing function. This may appear, at first glance, to contradict predictions of optimal diet theory (Pulliam, 1974; Estabrook and Dunham, 1976), which suggest that selectivity of the best alternatives increases as abundance increases but probably as a step function rather than a gradual transition (but see Krebs et al., 1977; Gill and Wolf, 1977). However, in most optimal diet models the decision is made upon arriving at a food item (or a patch in this context) and assumes that a forager has no information available that allows an a priori decision. Certainly, a priori information permits more benefits and costs to be integrated into the decision equation. Particularly, there is the possibility of using information on relative costs between patches to decide which patches to visit. Later, we will deal with the question of which patch to stay in and for how long once a patch is visited. Another potential source of a priori information is the presence of other organisms as signals of environmental quality (Kiester and Slatkin, 1974). Krebs (1974) noted that the probability of individual Great Blue Herons (Ardea herodias) landing at a feeding location was related positively to the presence of models of herons. He interpreted this as possible use of the presence of feeding birds to indicate high quality feeding areas to searching birds. It is also possible that feeding individuals might displace other individuals at a patch where rate of net energy intake is higher. In this case the dominance hierarchy would be an important correlate of use of this information since ability to displace or co-occur with a feeding organism at a better location should depend on relative dominance positions (Marler, 1956; Caraco, 1977). Most specialized nectar feeding birds forage individually. This may be due primarily to the conspicuousness of potential feeding areas. However, the critical variable is patch quality not patch location. In this situation the value of a priori information rests on its usefulness for predicting environmental quality without making a visit. Using a priori information is restricted to individuals that can insure that their view of patch quality corresponds closely to reality. Presumably this is possible only where an individual is the sole forager at a particular location. A common form of restricting use by other individuals is territoriality or dominance if spatial locations change (we view these responses as related forms of aggressive behavior along a continuum). Another possible mechanism, with limited supporting evidence, is called traplining (Janzen, 197 1; Baker, 1975; Feinsinger, 1976). This involves visiting a series of dispersed feeding sites in sequence. The sites are not sufficiently close to warrant or permit defense but use by other birds is less than by the trapliner. Differential use can be achieved by: (1) dominance interactions when a trapliner is at the site with the regular forager having a dominance advantage and (2) differences in reward probability for a trapliner versus other visitors. It is possible that a few initial rewards for the

FEEDING: AN ECOLOGICAL APPROACH

83

trapliner are sufficient to stimulate further visits, while birds that receive limited rewards are less likely to revisit. Use of a priori information should be coupled to increased rate of net energy intake per location if the behavior is to be beneficial; otherwise the information would not be used. We would expect the usefulness of a priori information to decline as average nectar volume per patch increased or the variance between patches decreased while the mean remained constant. As nectar volumes per patch increase, the rate of increase of the reward of searching for the highest volumes decreases (Fig. 6). If the variance of nectar volumes per patch is low, the reward differential among patches decreases and the relative benefit from choosing the highest volume also declines. However, the importance of changing variance will depend also on the mean since some portions of the net reward curve show major changes with minor shifts in average patch quality. If the curves in Fig. 6 are general, then the role of variance ought to increase as the mean patch quality decreases. In at least one sunbird-plant (Leonoris)foraging system, the variance of nectar availability per flower decreases with decreasing nectar volumes (Gill and Wolf, 1977).

B. A Posteriori INFORMATION A posteriori information can be used regardless of territorial status or dominance position. It requires only an assessment of patch quality once the organism is there, and it should be a valuable addition to a priori information. This information ultimately would have to be integrated into a larger environmental context. Search for foraging locations may not be required for nectar feeding birds feeding at point sources (flowers) that may signal quality but they still must estimate the relative reward structure of a patch once there. The general conceptual framework for our discussion of the relation between patch quality and use of patches is the idea of marginal value (Charnov, 1976b). Charnov argued that a feeding individual should leave a patch when the rate of food intake (capture rate) reached a level that approximated the average quality of the remainder of the patches. One index of quality (not necessarily used by organisms) that has been examined is “giving up time” (GUT), or the time that an individual will spend without reward before leaving a patch (see Krebs et al., 1974). This is a quality index that is useful when the prey are cryptic and a Friori estimates of prey availability are difficult. We would expect that a predator should increase GUT as average environmental quality declined. In his initial formulation of the marginal value theorem in a foraging context, Chamov assumed that time between patches was constant. In this case the organism simply had to compare within patch quality to the average quality. However, a predator should assess not only relative patch quality, but it also

84

F. REED HAINSWORTH AND LARRY L. WOLF

should weigh costs, such as between patch costs, with projected benefits. The projected benefits probably are not the average environmental quality, but are the predator’s view of anticipated rewards in the next patch. This view is gained from prior foraging experience in the environment and is integrated, perhaps by assessing energy balance, through some finite time period. Two other aspects of the marginal value theorem should be mentioned. First, as noted by Charnov, it is a deterministic view. It seems likely that as the variance of patch quality increased the probability would decrease that a predator’s view of average patch quality following a finite sampling period would coincide with the actual average. Thus, prior information about habitat quality may or may not correspond closely with reality. Second, average habitat quali y can continually change as a result of the foraging activities of predators (Charnov et ul., 1976; Zach and Falls, 1976a,b,c; Gill and Wolf, 1977). This may be particularly true for circumscribed areas such as territories. The effect of change in habitat quality would be to force a continual reassessment of reward structure of the environment with appropriate behavioral change. For example, a male Malachite Sunbird (Necturiniu furnosu) defending a breeding temtory shifted from rigid defense to partial defense of the periphery as its foraging time budget increased and average available nectar volumes decreased (Wolf, 1975). Since nectarivores can be faced with changing nectar availability per patch over relatively short periods (Gill and Wolf, 1975a,b, 1977), the decision making process probably incorporates information that is much more stochastic in nature than the Charnov model assumes. For nectarivores, we assume that the principal index of patch quality is also some index to the rate of net energy intake which, in turn, could be influenced by nectar concentrations, available volumes and corolla lengths (see Section 111). For simplicity, at the moment we will assume that the birds have one or more indices of patch quality that depend on intake rate; the index could be intake rate itself, but need not be. Upon visiting a flower, a bird could assess flower quality (available nectar per flower) and use the u posteriori information to determine how long to remain at a flower as it depletes the nectar (Charnov et.ul., 1976). If the birds use this information, the volumes remaining after a visit should be a function of energy available in the average flower. In a natural system, with sunbirds feeding at Leonotis flowers, Gill and Wolf (1979) found that each species tended to reduce nectar volumes to a constant percentage of availability independent of the initial volume. The proportion removed varied among species in relation to ability to reach the nectar as a result of differing morphological “fits” of corolla and bill. These results suggest that the birds could treat a single flower as a patch and respond to different patch qualities via behavior that may reflect their assessment of the average in relation to present patch quality.

f

FEEDING: AN ECOLOGICAL APPROACH

85

For inflorescences with more than one flower, birds may use information from initial flowers as an index to quality of remaining flowers. In a sunbird-leonotis system, we have evidence that this plays an important role in the foraging behavior of nontemtorial birds (Gill and Wolf, 1977). Territorial individuals also may use this a posteriori information, but probably less frequently since they also can use a priori information. The birds did not always visit all flowers on a inflorescence before leaving. Under conditions of relatively high average availability per flower, about 25% of the inflorescences visited were left before all flowers were probed. The value of leaving is in potential benefits associated with subsequent visits to higher quality inflorescences. In a situation with 25% rejections the average increase in nectar available per patch that was completely visited amounted to nearly a doubling of, what was available in the average rejected flowers. The effect for a foraging sunbird in the situation studied was to increase intake per flower by approximately 15% over what would have occurred if all flowers were probed on each inflorescence visited (Gill and Wolf, 1977). Some characteristics of the first few flowers (perhaps probing an empty flower) was used as an index of the quality of the remainder of the patch. The patch was accepted or rejected in relation to what was initially visited and alternatives available at other patches. It is unlikely that the birds responded only to individual patch conditions since the proportion of rejected patches varied with average environmental quality, which itself changed as a function of the foraging intensity of the birds (Gill and Wolf, 1977). The probability of rejection declined as average environmental quality declined, as predicted by the Charnov model. Even though the characteristicsof the first few flowers visited in a patch changed (e.g., the probability of visiting an empty flower increased), the birds were less likely to reject a patch as average nectar volumes declined. Since rate of intake per patch is directly related to the number of empty flowers per patch, the results appear consistent with the marginal value theorem. Gill and Wolf showed that the shift in rejection rate with the change in nectar volumes per flower occurred over as little as 4 hours during a day. However, it is still not known over what smaller time intervals the birds integrate information about changing environmental quality. We have discussed foraging at patches with recognizable boundaries (i.e., an inflorescence was classed as a patch) and how patches are used within a foraging bout. In each case the patch is either accepted or rejected and foraging continues. However, it is possible that a predator either cannot recognize patch boundaries or that a patch is not depleted to a rejection threshold by the end of a foraging bout. Both have the effect of making patch boundaries arbitrary and dynamic. In these cases the rules change somewhat. If boundaries are not fixed, predators may modify behavior in a way that shifts the probabilities of remaining in what appears to be rewarding area and leaving areas that seem to have low reward

86

F. REED HAINSWORTH AND LARRY L. WOLF

levels. Since the boundaries are not known, we would expect behavioral responses to shift gradually as the birds move into and out of rewarding areas. One simple way to leave nonrewarding areas is to increase the distance moved in a straight line. This will maximize the probability of movement away from an area. On the other hand, a predator could remain in a rewarding area by shortening the distance and increasing the angle of move relative to the previous move. Smith (1974a,b) has shown behavior of this sort for thrushes hunting for prey on mowed lawns. However, in Smith’s study, primarily turn angles were affected by prior reward experience (for similar data on bumble bees, see Pyke, 1978a; for ovenbirds, see Zachs and Falls, 1976a,b,c). In general, a reward increased the likelihood of walking a circular path rather than alternating directions of movement. This “area-restricted search” has been shown to occur in birds and mammals and a variety of other organisms (Krebs, 1973). Data on area restricted search are not available for hummingbirds in the field, but we have preliminary data in the laboratory that suggest that birds respond to local “flower” characteristics. We arranged syringe needle flowers with plastic corollas in a circular pattern (20 to 40 total flowers). It took a bird several foraging bouts to visit all the flowers, and we did not replenish the sugar water in flowers following a visit until a number of flowers equal to the total had been visited. Thus, after the first visit, a bird could visit both empty and full flowers. A foraging bird could maintain, or change, its behavior in relation to whether the flower just visited was full or empty. As Table VI indicates there was a low probability that the differences in responses to full and empty flowers were by chance. The birds continued their foraging pattern after a full flower and changed after an empty flower. We also asked if the behavior shift was influenced significantly by flowers visited prior to the ultimate flower. We found no evidence that a bird changed behavior in relation to the food content of earlier flowers visited. Preliminary data on foraging movements are available from sunbirds foraging in a dense patch of Leonotis in eastern Africa (Gill and Wolf, 1977). We examined a variety of behaviors that might be influenced by local reward levels. We assessed local reward levels by noting whether the bird visited all flowers on the inflorescence (high quality) or left after probing only a few flowers (low quality; see p. 85). The frequency distribution of angles that the birds turned when leaving an inflorescence relative to arrival direction was uniform and not unimodally distributed around a forward direction as has been reported for many other species (e.g., Siniff and Jessen, 1969; Pyke, 1978a). There also was no evidence that the angle changed significantly following rejection of an inflorescence. The birds turned regularly when foraging, and the average direction was not obviously influenced by reward level, at least in terms of the inflorescence just visited. For one species ( N . reichenowi) there also was no evidence from combined data for many individuals that average distance moved vaned following visits to

FEEDING: AN ECOLOGICAL APPROACH

87

TABLE VI THEEFFECTON FORAGING BEHAVIOROF MALEEugenes fulgens AT A CIRCULAR ARRAYOF ARTIFICIAL FLOWERS OF VISITING EITHER A FULL(F) OR EMPTY(E) FLOWER.".^ Behavior after visit Flower visited

S

C

F E

3 10 39

20 29

"The behavior subsequent to the flower visit is considered to be either the same as before the visit (S), or to change ( C ) following the visit. (S) means the bird continued in the same direction around the inflorescence. (C) means the bird either changed direction and/or skipped flowers. Data from Wolferal. (unpublished observations). bx2 = 69.9; df = I ; p < 0.001.

accepted or rejected inflorescences. However, for another species (N.furnosu) distance was longer following a visit to a rejected patch compared with an accepted patch. Considering only these two types of behavior, the birds apparently made few adjustments in response to local reward levels although they showed a response to local patch quality through acceptance or rejection. These sunbirds also showed a definite tendency to forage within a narrow vertical range as they moved from inflorescence to inflorescence. This tendency was not altered by variations in the bird's view of environmental quality, at least as measured by acceptance and rejection of inflorescences. Again a possible shift in behavior that would alter the ongoing foraging route in relation to reward levels was not incorporated into the foraging tactics of these birds. Several explanations are possible for apparent differences between sunbird foraging movements and those of other organisms that apparently continually change movement patterns in relation to local food availability (Krebs, 1973; Smith, 1974a,b). First, we might expect no shift in behavior for the sunbirds if they were feeding in a uniformly high quality environment where they would be expected to turn continually. We also would expect flight distances to be short in a high quality environment. In addition, from the marginal value theorem, we would expect the time over which a single high reward produced area-restricted search (giving up time for search behavior) would vary with the level of average

88

F. REED HAINSWORTH AND LARRY L. WOLF

reward density. Thus, even in Smith’s (1974a,b) studies, the thrushes continued foraging efforts that appeared to indicate a high quality site for some time with no reward; the length of time should be related to reward level. Additionally, aggressive interactions may constrain foraging birds. For example, temtorial birds would tend to stay within a territory while nontemtorial birds would tend to avoid areas where they were likely to be chased. This could lead to varying degrees of area restriction in search paths. A second foraging technique that appears to be area-restricted searching, but is accomplished differently, is continued return to the same feeding area over some number of foraging bouts (Royama, 1970; Smith and Sweatman, 1974). In this case we assume that the area will support continued foraging effort and the birds will quickly learn to return to these high reward areas. Behavior of this type has been shown to occur in birds in both laboratory and field situations (Partridge, 1976; Zach and Falls, 1976a,b). Hummingbirds also show this type of area restricted search in relation to the presence of feeders. They regularly return to feeders and may concentrate their foraging at these continually rewarding sites. Miller and Miller (197 1) reported that hummingbirds returned to a feeder location when the feeder was not present in early spring after having been absent for at least 6 months.

VI. SYNOHIS Physiological and ecological approaches to comparative studies of feeding behavior have a common basis in energy regulation. Theories are examined that suggest organisms should maximize benefits from feeding relative to costs measured perhaps as the rate of net energy gain subject to biologically important constraints. Experimental information is examined relative to these theories for aspects of feeding including item choice, meal patterns (meal size and frequency), food abundance, and resource exploitation patterns. Emphasis is placed on the interpretation of possible controls at the interface between an organism and its environment; and the operation of controls for feeding are viewed to be interpretable only with respect to natural conditions. Research on hummingbird and sunbird feeding forms a focus for discussion because of the extent to which benefits and costs can be specified and placed in a natural context; but viewing feeding behavior as an optimization problem has considerable potential to predict behavior for other species. Although benefit and cost models are very rewarding hypotheses for examining feeding behavior, the number of direct quantitative tests is limited. This is especially true of field tests; the number of laboratory tests is increasing fairly rapidly although caution is always needed in translating laboratory results to natural situations. There are some qualitative tests of the models; but, as the

FEEDING: AN ECOLOGICAL APPROACH

89

similarity between the predictions of the Werner and Hall and the O’Brien et al. models indicate (see Section III,C,2), the tests must be carefully designed and quantitatively assessed. These two models differ primarily in emphasis on underlying mechanisms of item choice, and this points out the important possibility that feeding behavior may not be regularly optimized at a single maximum. There may be several maxima which may or may not reach equivalent levels of the function being maximized. An important question then would be how organisms arrive at a particular maximum, especially the importance of stochastic events. It is possible, for example, that chance encounters with a series of one prey type may increase efficiency of prey capture for that type even though a similar series of chance encounters with other prey might eventually lead to another peak in capture efficiency. Presumably the ability of an organism to move between maxima will depend on the characteristics of the intervening minima as well as the absolute levels of the maxima. Within these constraints we are also faced with two additional questions: How does an organism trade off different maximization criteria through time? and What is the time interval over which information is integrated to arrive at a view of environmental quality? The first concerns reaching maxima subject to conflicting demands. A simple example would be food item choice where the conflicts are between energy maximization and nutrient requirements. What is the optimal pattern of food choice where these demands may be met with different prey items? The second problem is partly coupled to this in the sense that the relative strengths of demands for two conflicting choices can change in relation to ongoing behavior (Sibly and McFarland, 1976). The choice that an organism makes will depend on its “view” of the results of past feeding. In optimal foraging theory this can mean that the short-term view of environmental quality can be quite different from the long-term availability of different prey types. Understanding the time span over which past experience influences present and future behavior will be extremely important in testing optimal feeding models as well as in understanding how organisms organize their view of a changing environment. Acknowledgments Supported by grants from the National Science Foundation. The assistance of Terre Mercier is greatly appreciated. We thank Drs. E. Stricker, G . Pyke, and J . Krebs for comments on an early draft of the manuscript.

References Andersson, S . 1973. Secretion of gastrointestinal hormones. Ann. Rev. Physiol. 35, 431452. Baker, H . G . 1975. Sugar concentrations in nectars from hummingbird flowers. Biorropicu 7, 137-141.

90

F. REED HAINSWORTH AND LARRY L. WOLF

Baker, H. G., and Baker, I. 1975. Studies of nectar-constitutionand pollinator-plantcoevolution. In “Coevolution of Animals and Plants” (L. E. Gilbert and P. H. Raven, eds.). pp. 100-140. Univ. of Texas Press, Austin. Berger, M. 1974. Energiewechsel von Kolibris beim Schwirrflug unter Hohenbedingungen. J. Orniihol. 115, 273-288. Berger, M., and Hart, J. S. 1972. Die Atmung beim Kolibri Amaziliafimbripta wahrend des Schwirrfluges bei verschiedenen Umgebungstemperaturen. J. Comp. Physiol. 81, 363-380. Brian, A. P. 1957. Differences in the flowers visited by four species of bumble-bees and their causes. J . Anim. Ecol. 26, 71-98. Brobeck, J . R. 1965. Exchange, control, and regulation. In “Physiological Controls and Regulations” (W. S. Yamamoto and J. R. Brobeck, eds.), pp. 1-13. Saunders, Philadelphia, Pennsylvania. Brower, L. P., and Brower, J. V. Z. 1964. Birds, butterflies, and plant poisons: A study in ecological chemistry. Zoologica (N.Y.) 49, 137-159. Brown, 1. H., and Bartholomew, G . A. 1969. Periodicity and energetics of torpor in the kangaroo mouse, Microdipodops pallidus. Ecology 50, 705-709. Calder, W. A. 1974. Consequences of body size for avian energetics. I n “Avian Energetics” (R.A. Paynter, Jr., ed.), Publ. Nuttall Omithol. Club, No. 15, pp. 86-144. Cambridge, Massachusetts. Caraco, T. B. 1977. Ecological Regulation of Social System Stochastic Dynamics. Ph.D. Thesis, Syracuse Univ., Syracuse, New York. Carpenter, F. L., and MacMillen, R. E. 1976. Energetic cost of feeding temtories in an Hawaiian honeycreeper. Oecologia 26, 2 13-223. Can, W. E. S., and Chaney, T. B. 1976. Chemical stimulation of feeding behavior in the pinfish, Lagodon rhomboides: Characterization and identification of stimulating substances extracted from shrimp. Comp. Biochem. Physiol. B 54, 437441. Chamov, E. L. 1976a. Optimal foraging: Attack strategy of a mantid. Am. Nai. 110, 141-151. Chamov, E. L. 1976b. Optimal foraging: The marginal value theorem. Theor. Popul. Biol. 9, 129-1 36. Chamov, E. L., Orians, G. H., and Hyatt, K. 1976. Ecological implications of resource depression. Am. Nat. 110, 247-259. Cody, M. L. 1974. Optimization in ecology. Science 183, 1156-1 164. Collier, G., and Novell, K. 1967. Saccharin as a sugar surrogate. J . Comp. Physiol. Psychol. 64, 404-408.

Cruden, R. W., andHermann-Parker, S. M. 1977. Defense of feeding sites by orioles and hepatic tanagers in Mexico. Auk 94, 594-596. Curio, E. 1976. “The Ethology of Predation” (D. S. Famer, ed.), Zoophysiology and Ecology, Vol. 7. Springer-Verlag. Berlin and New York. Dawkins, M. 1971. Perceptual changes in chicks: Another look at the “search image’’ concept. Anim. Behav. 19, 566-574. DeBenedictis, P., Gill, F. B., Hainsworth. F. R.,Pyke, G. H.. and Wolf, L. L. 1978. Optimal meal size in hummingbirds. Am. Nut. 112, 301-316. DeCastro, J. M., and Balagura, S. 1975a. Meal patterning in the streptozotocin-diabeticrat. Physiol. Behav. IS, 259-263. DeCastro, J. M., and Balagura, S. 1975b. Relationship between endogenous, natural feeding patterns and body composition in the rat. Physiol. Behav. 15, 635-639. Dethier, V. G. 1976. “The Hungry Fly.” Harvard Univ. Press, Cambridge, Massachusetts. Duncan, 1. 1. H., Home, A. R., Hughes, 8. O., and Wood-Gush, D. G . M. 1970. The pattern of food intake in female brown leghorn fowls as recorded in a skinner box. Anim. Behav. 18, 245-255.

FEEDING: AN ECOLOGICAL APPROACH

91

Eggers. D. 1975. A Synthesis of the Feeding Behavior and Growth of Juvenile Sockeye Salmon. Ph.D. Thesis, Univ. of Washington, Seattle. Ellis, J . E., Wiens, J . A,, Rodell, C. F., and Anway, I. C . 1976. A conceptual model of diet selection as an ecosystem process. J. Theor. Biol. 60, 93-108. Emlen. J. M . 1966. The role of time and energy in food preference. Am. Nm. 100, 61 1-617. Emlen, J . M . 1968. Optimal choice in animals. Am. Nut. 102, 385-390. Epstein, A. N. 1967. Oropharyngeal factors in feeding and drinking. In “Handbook of Physiology, Sect. 6: Alimentary Canal” (C. F. Code, ed.), pp. 197-218. Am. Physiol. Soc., Washington, D.C. Epting. R, J., and Casey, T. M. 1973. Power output and wing disc loading in hovering hummingbirds. Am. Nut. 107, 761 -765. Estabrook, G. F.. and Dunham, A. E. 1976. Optimal diet as a function of absolute abundance, relative abundance, and relative value of available prey. Am. Nut. 110, 401413. Faegri, F., and van der Pijl. L. 1971. ”The Principles of Pollination Ecology,” Pergamon. Oxford. Feeny, P. P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51, 656681. Feinsinger, P. 1976. Organization of a tropical guild of nectarivorous birds. Ecol. Monogr. 46, 257-291. Fleming, A. S . 1976. Ovarian influences on food intake and body weight regulation in lactating rats. Physiol. Behuv. 17, 969-978. Freeland. W. J., and Janzen, D. H. 1974. Strategies in herbivory by mammals: The role of plant secondary compounds. Am. Nar. 108, 269-289. French, A. R. 1976. Selection of high temperaturesfor hibernation by the pocket mouse Perognurhus longimembris: Ecological advantages and energetic consequences. Ecology 57, 185-191. Friedman, M.I., and Stricker, E. M. 1976. The physiological psychology of hunger: A physiological perspective. Psychol. Rev. 83, 409-431. Garcia, J.. Ervin, F. R..and Koelling, R. A. 1966. Learning with prolonged delay of reinforcement. Psychon. Sci. 5 , 121-122. Gelperin, A. 1966. Control of crop emptying in the blowfly. J. Insect Physiol. 12, 331-345. Gilbert, L. E. 1971. Butterfly-plantcoevolution: Has Passifloru udenopodu won the selectional race with heliconine butterflies? Science 172, 585-586. Gill, F. B.. and Wolf, L. L. 1975a. Foraging strategies and energetics of East African sunbirds at mistletoe flowers. Am. Nar. 109, 491-510. Gill, F. B., and Wolf, L. L. 1975b. Economics of territoriality in the golden-winged sunbird. Ecology 56, 333-345. Gill, F. B., and Wolf. L. L. 1977. Nonrandom foraging by sunbirds in a patchy environment. Ecology 58, 1284-1296. Gill, F. B., and Wolf, L. L. 1979. In press. Goss-Custard, J . D. 1977. Optimal foraging and the size selection of worms by redshank, Tringu torunus, in the field. Anim. Behav. 25, 10-29. Grant, K. A., and Grant, V. 1968. “Hummingbirds and Their Flowers.” Columbia Univ. Press, New York. Greenewalt, C. C. 1975. The flight of birds. Truns. Am. Philos. SOC.65(4), 1-67. Hainsworth, F. R. 1973. On the tongue of a hummingbird: Its role in the rate and energetics of feeding. Comp. Biochem. Physiol. A 46, 65-78. Hainsworth. F. R. 1974. Food quality and foraging efficiency: The efficiency of sugar assimilation by hummingbirds. J. Comp. Physiol. 88, 425-431. Hainsworth. F. R. 1977. Foraging efficiency and parental care in Colibri coruscuns. Condor 79, 69-75.

92

F. REED HAINSWORTH AND LARRY L. WOLF

Hainsworth. F. R. 1978. Feeding: Models of costs and benefits in energy regulation. Am. Zool. (in press). Hainsworth, F. R., and Wolf, L. L. 1970. Regulation of oxygen consumption and body temperature during torpor in a hummingbird, Eulmpis jugularis. Science 168, 368-369. Hainsworth, F. R.,and Wolf, L. L. 1972a. Power for hovering flight in relation to body size in hummingbirds. Am. Nut. 106, 5894%. Hainsworth, F. R., and Wolf, L. L. 1972b. Crop volume, nectar concentration, and hummingbird energetics. Comp. Biochem. Physiol. A 42, 359-366. Hainsworth, F. R., and Wolf, L. L. 1976. Nectar characteristics and food selection by hummingbirds. Oecologia 25, 101-1 13. Hainsworth, F. R., and Wolf, L. L. 1978. Economics of temperature regulation and torpor in non-mammalian organisms. In “Natural Torpidity and Thennogenesis” (L. Wang and J. Hudson, eds.). Academic Press, New York. In press. Hainsworth, F. R., Collins, B. G., and Wolf, L. L. 1977. The function of torpor in hummingbirds. Physiol. 2001.50, 215-222. Hartman, H. B., and Hartman, M. S. 1977. The stimulation of filter feeding in the porcelain crab Perrolisrhes cincripes Randall by amino acids and sugars. Comp. Biochem. Physiol. E 56, 19-22.

Heinrich, B. 1975. The role of energetics in bumblebee-flower interrelationships. In “Coevolution of Animals and Plants” (L. E. Gilbert and P. H. Raven, eds.), pp. 141-158. Univ. of Texas Press, Austin. Heinrich, B.,and Raven, P. H. 1972. Energetics and pollination ecology. Science 176, 597-602. Herreid, C. F.,and Kessel, B. 1967. Thermal conductance in birds and mammals. Comp. Biochem. Physiol. 21, 405414. Himmelman. J. H.. and Carefoot, T. H. 1975. Seasonal changes in calorific value of three Pacific coast seaweeds, and their significance to some marine invertebrate herbivores. J . Exp. Mar. Biol. Ecol. 18, 139-151. Hirsch, E. 1973. Some determinants of intake and patterns of feeding in the guinea pig. Physiol. Behav. 11, 687-704. Hocking, B. 1968. Insect-flower associations in the high Arctic with special reference to nectar. Oikos 19, 359-388. Hunt, J. N., and Knox, M. T. 1968. Regulation of gastric emptying. In “Handbook of Physiology, Sect. 6: Alimentary Canal, Vol. IV, Motility” (C. F. Code. ed.), pp. 1917-1935. Am. Physiol. Soc.,Washington, D.C. Janzen, D. H. 1971. Euglossine bees as long distance pollinators of tropical plants. Science 171, 203 -205.

Kanarek, R. B. 1975. Availability and caloric density of the diet as determinants of meal patterns in cats. Physiol. Eehuv. IS, 61 1-618. Katz, P. L. 1974. A long-term approach to foraging optimization. Am. Nar. 108, 758-782 Kear, J. 1962. Food selection in finches with special reference to inter-specific differences. Proc. Zool. SOC.London 138, 163-204. Kendeigh, S. C., Kontogiannis, J. E.. Malzac, A,, and Roth, R. R. 1969. Environmental regulation of food intake by birds. Comp. Biochem. Physiol. 31, 941-957. Kenney, N. J., and Mook, D.G. 1974. Effects of ovariectomy on meal pattern in the albino rat. J . Comp. Physiol. Psychol. 87, 302-309. Kiester, A. R., and Slatkin, M . 1974. A strategy of movement and resource utilization. Theor. Popul. Biol. 6, 1-20. King, J. R. 1972. Adaptive periodic fat storage by birds. Proc. Inr. Ornirhol. Congr., 15th, 1970 pp. 200-217.

FEEDING: AN ECOLOGICAL APPROACH

93

King, J. R. 1974. Seasonal allocation of time and energy resources in birds. I n “Avian Energetics” (R. A. Paynter, Jr.. ed.), Publ. Nuttall. Ornithol. Club, No. 15, pp. 4-79. Cambridge, Massachusetts. King, K. R. 1976. Lipostatic control of body weight: Evidence of humoral mediation. fhysiol. Psychol. 4, 405-408. Kleiber, M. 1961. “The Fire of Life.” Wiley, New York. Kleiber, M. 1972. Body size, conductance for animal heat flow and Newton’s law of cooling. J . Theor. Biol. 37, 139-150. Krebs, J . R. 1973. Behavioral aspects of predation. I n “Perspectives in Ethology” (P. P. G. Bateson and P. H. Klopfer, eds.), pp. 73-1 I I . Plenum, New York. Krebs, J. R. 1974. Colonial nesting and social feeding as strategies for exploiting food resources in the Great Blue Heron (Ardea herodias). Behaviour 51, 99-134. Krebs, J. R., Ryan, 1. C., and Charnov, E. L. 1974. Hunting by expectation or optimal foraging? A study of patch use by chickadees. h i m . Behav. 22, 953-964. Krebs, J. R.. Ericksen, J. T., Weber, M. I., and Charnov, E. L. 1977. Optimal prey selection in the great tit (farus major). Anim. Behav. 25, 30-38. LaRue, C. G., and LeMagnen, J. 1972. The olfactory control of meal pattern in rats. Physiol. Behav. 9, 817-821. Lasiewski, R. C . 1963. Oxygen consumption of torpid, resting, active, and flying hummingbirds. Physiol. 2001.36, 122-140. LeMagnen, J. 1975. Current concepts in energy balance. I n “Neural Integration of Physiological Mechanisms and Behaviour” (G. J. Mogenson and F. R. Calaresu, eds.), pp. 95-108. Univ. of Toronto Press, Toronto. LeMagnen, J. 1976. Interactions of glucostatic and lipostatic mechanisms in the regulatory control of feeding. I n “Hunger: Basic Mechanisms and Clinical Implications” (D. Novin, W. Wynvicka, and G. Bray, eds.), pp. 89-102. Raven, New York. LeMagnen, J., and Devos, M. 1970. Metabolic correlates of the meal onset in the free food intake of rats. Physiol. Behav. 5 , 805-814. LeMagnen, J., Devos, M., Gaudilliere, J., Louis-Sylvestre, J., and Tallon, S. 1973. Role of a lipostatic mechanism in regulation by feeding of energy balance in rats. J. Comp. fhysiol. Psychol. 84, 1-23. Leung, P. M. B., and Horwitz, B. A. 1976. Free-feeding patterns of rats in response to changes in environmental temperature. Am. J . Physiol. 231, 1220-1224. Levin. D. A. 1976. The chemical defenses of plants to pathogens and herbivores. Annu. Rev. Ecol. Syst. 7, 121-159. Levin, D. A,, and Anderson, W. W. 1970. Competition for pollinators between simultaneously flowering species. Am. Nu?. 104, 55-67. Levin, D. A,, and Kerster. H.W. 1974. Gene flow in seed plants. I n “Evolutionary Biology” (T. Dobzhansky, M. K . Hecht. and W . C. Steere, eds.), pp. 139-220. Plenum, New York. Levitsky, D. A. 1974. Feeding conditions and intermeal relationships. fhysiol. Behav. 12, 779-787. Levitsky. D. A,. and Collier, G. 1968. Effects of diet and deprivation on meal eating behavior in rats. Physiol. Behav. 3, 137-140. MacArthur, R. H., and Pianka, E. R. 1966. On the optimal use of a patchy environment. Am. Nar.

loo, 603409. McFarland. D. J. 1977. Decision making in animals. Narure (London) 269, 15-21. McFarland, D. J . 1978. Hunger in interaction with other aspects of motivation. In “Hunger Models: Computable Theory of Feeding Control” (D. A. Booth, ed.). Academic Press, New York. In press. Maller. 0.. Clark, J. M., and Kare, M. R. 1965. Short-term caloric regulation in the adult opossum (Didelphis virginiana). f r o c . SOC.Exp. Biol. Med. 118, 275-277.

94

F. REED HAINSWORTH AND LARRY L. WOLF

Marler, P. 1956. Studies of fighting in chaffinches. 3. Proximity as a cause of aggression. Br. J . Anim. Behav. 4, 23-30. Menge, B. A. 1972. Foraging strategy of a starfish in relation to actual prey availability and environmental predictability. Ecol. Monogr. 42, 25-50. Miller, R. S., and Miller. R. E. 1971. The memory of hummingbirds. Blue Jay 29, 29-30. Milligan, L. P. 1971. Energetic efficiency and metabolic transformations. Fed. Proc., Fed. Am. Soc. Exp. Biol. 30, 1454-1458. Murdoch, W . W., and Oaten, A. 1975. Predationand population stability. Adv. Ecol. Res. 9, 1-131. Norberg, R. A. 1977. An ecological theory on foraging time and energetics and choice of optimal food searching method. J . h i m . Ecol. 46, 51 1-529. Novin, D., Wyrwicka, W.. and Bray, G. A. 1976. “Hunger: Basic Mechanisms and Clinical Implications.” Raven, New York. O’Brien, W. J., Slade, N. A., and Vinyard, G. L. 1976. Apparent size as the determinant of prey selection by bluegill sunfish (Lepomis macrochirus). Ecology 57, 1304-1310. Paine, R. T . 1976. Size-limited predation: an observational and experimental approach with the Myrilus-Pisaster interaction. Ecology 57, 858-873. Panksepp, J . 1973. Reanalysis of feeding patterns in the rat. J . Comp. Physiol. Psychol. 82, 78-94. Panksepp, J., and Krost, K . 1975. Modification of diurnal feeding patterns by palatability. Physiol. Behav. 15, 673-677. Partridge, L. 1976. Individual differences in feeding efficiencies and feeding preferences of captive great tits. Anim. Behav. 24, 230-240. Pennycuick, C. J. 1969. Mechanics of bird migration. Ibis 111, 525-556. Petersen, S. 1976. The temporal pattern of feeding over the oestrous cycle of the mouse. Anim. Behav. 24, 939-955. F‘ulliam, H. R. 1974. On the theory of optimal diets. Am. Nut. 108, 58-74. Pulliam, H. R. 1975. Diet optimization with nutrient constraints. Am. Nar. 109, 765-768. Qke, G . H. 1978a. Optimal foraging: Movement patterns of bumblebees between inflorescences. Theor. Popl. Biol. 13, 72-98. e k e , G. H. 1978b. Optimal foraging in hummingbirds: Testing the marginal value theorem. Amer. Zool. (in press). Rapport. D. J., and Turner, J. E. 1977. Economic models in ecology. Science 195, 367-373. Reiner, R. D . , and Reiner, A. A . 1975. Chemical control of feeding in four species of tropical ophiuroids of the genus Ophioderma. Comp. Biochem. Physiol. B 51, 915-927. Richter, C. P., and Campbell. K. H. 1940. Taste thresholds and taste perferences of rats for five common sugars. J . Nutr. 20, 3 1-46, Ritter, R. C . , and Epstein. A. N. 1975. Control of meal size by central noradrenergic action. Proc. Narl. Acad. Sci. U.S.A. 72, 3740-3743. Rosenthal, G. A., Dahlman. D. L., and Janzen, D. H. 1976. A novel means for dealing with L-Canavanine, a toxic metabolite. Science 192, 256-258. Rosenzweig. M. L.. and Sterner. P. W. 1970. Population ecology of desert rodent communities: Body size and seed-husking as bases for heteromyid coexistence. Ecology 51, 217-224. Royama, T . 1970. Factors governing the hunting behaviour and selection of food by the great tit (Parus major L.).J . Anim. Ecol. 39, 619468. Rozin, P. 1976. The selection of foods by rats, humans, and other animals. Adv. Srudy Behav. 6 , 2 1-76, Sanderson, J . D., and Vanderweele, D. A. 1975. Analysis of feeding patterns in normal and vagotomized rabbits. Physiol. Behav. 15, 357-364. Schmidt-Nielsen, K. 1972. Locomotion: Energy cost of swimming, flying, and running. Science 177, 222-228. Schmidt-Nielsen. K . 1975. “Animal Physiology.” Cambridge Univ. Press, London and New York.

FEEDING: AN ECOLOGICAL APPROACH

95

Schoener, T. W. 1969a. Models of optimal size for solitary predators. Am. Nat. 103, 277-313. Schoener, T. W. 1969b. Optimal size and specialization in constant and fluctuating environments: An energy-time approach. Brookhaven Symp. Biol. 22, 103-1 14. Schoener, T. W. 1971. Theory of feeding strategies. Annu. Rev. Ecol. Sysr. 2, 369404. Sibly, R., and McFarland, D. 1976. On the fitness of behavior sequences. Am. Nar. 110, 601-617. Silverman, H.J., and Zucker, 1. 1976. Absence of post-fast food compensation in the golden hamster (Mesocricerus auraas). Physiol. Behav. 17, 27 1-285. Siniff, D. B., and Jessen, C. R. 1969. A simulation model of animal movement patterns. Adv. Ecol. Res. 6 , 185-219. Slobodkin, L. B. 1974. Prudent predation does not require group selection. Am. Nar. 108, 665-678. Slater, P. J. B. 1974. The temporal pattern of feeding in the zebra finch. Anim. Behav. 22, 506-515. Smith, C. C. 1975. The coevolution of plants and seed predators. In “Coevolution of Animals and Plants” (L. E. Gilbert and P. H.Raven, eds.), pp. 53-77. Univ. ot Texas Press, Austin. Smith, C. C.. and Follmer, D. 1972. Food preferences of squirrels. Ecology 53, 82-91. Smith, J. N . M. 1974a. The food searching behavior of two European thrushes. I. Description and analysis of search paths. Behaviour 48, 276-302. Smith, J. N. M. 1974b. The food searching behaviour of two European thrushes. 11. The adaptiveness of the search patterns. Behaviour 49, 1-61, Smith, J. N. M., and Sweatman, H. P. A. 1974. Food-searching behavior of titmice in patchy environments. Ecology 55, 1216-1232. Snow, B. K., and Snow, D. W. 1972. Feeding niches of hummingbirds in a Trinidad valley. J. Anim. Ecol. 41, 471485. Snowdon, C. T., and Wampler, R. S. 1974. Effects of lateral hypothalamic lesions and vagotomy on meal patterns in rats. J. Comp. Physiol. Psychol. 87, 399409. Staddon, J. E. R. 1975. A note on the evolutionary significanceof “supernormal” stimuli. Am. Nar. 109, 541-545. Stevenson, N. R., and Fierstein, J. S. 1976. Circadian rhythms of intestinal sucrase and glucose transport: Cued by time of feeding. Am. J. Physiol. 230, 731-735. Stiles, F. G. 1971. Time, energy, and temtoriality of the Anna hummingbird. Science 173, 818-821. Stiles, F. G. 1975. Ecology, flowering phenology, and hummingbird pollination of some Costa Rican Heliconia species. Ecology 56, 285-301. Stiles, F. G. 1976. Taste preferences, color preferences, and flower choice in hummingbirds. Condor 78, 10-26. Straw, R. M. 1972. A Markov model for pollinator constancy and competition. Am. Nar. 106, 597-620. Taylor, C. R.,Schmidt-Nielsen, K.,and Raab, J. L. 1970. Scaling of energetic cost of running to body size in mammals. Am. J. Physiol. 219, I 104-1 107. Taylor. J. 1976. The advantage of spacing-out. J. Theor. Biol. 59, 485490. Taylor, R. J. 1976. Value of clumping to prey and the evolutionary response of ambush predators. Am. Nor. 110, 13-29. Thomas, D. W., Scharrer, E., and Mayer, J. 1976. Effects of alloxan induced diabetes on the feeding patterns of rats. Physiol. Behav. 17, 345-349. Tinbergen, L. 1960. The natural control of insects in pine woods. I. Factors influencing the intensity of predation by songbirds. Arch. Neerl. Zool. 13, 265-343. Toates, F. M.,and Booth, D. A. 1974. Control of food intake by energy supply. Narure (London) 251, 710-711. Tucker, V. A. 1971. Flight energetics in birds. Am. Zool. 11, 115-124. Ware, D. M. 1975. Growth, metabolism, and optimal swimming speed of a pelagic fish. J. Fish. Res. Board Can. 32, 3 3 4 1 .

96

F. REED HAINSWORTH AND LARRY L. WOLF

Waser, N. 1977. Competition for pollination and the evolution of sequential flowering. Bull. Ecol. SOC.Am. 58, 9. Werner, E. E., and Hall. D. J. 1974. Optimal foraging and size selection of prey by the bluegill sunfish (Lepomis machrochirus). Ecology 55, 1042-1052. Willson, M. F.. and Harmeson, 1. C. 1973. Seed preferences and digestive efficiency of cardinals and song sparrows. Condor 75, 225-234. Wolf, L. L. 1975. Energy intake and expenditures in a nectar-feeding sunbird. Ecology 56, 92-104. Wolf, L. L., and Hainsworth. F. R. 1971. Time and energy budgets of territorial hummingbirds. Ecology 52, 980-988. Wolf, L. L., and Hainsworth, F. R. 1977. Temporal patterning of feeding by hummingbirds. h i m . ' Behaw. 25, 976-989. Wolf, L. L., and Hainsworth, F. R. 1978. Energy: Expenditures and intakes. In "Chemical Zoology" (A. Brush, ed.), Vol. X, pp. 307-358. Academic Press, New York. Wolf, L. L., Hainsworth, F. R.,and Stiles, F. G. 1972. Energetics of foraging: Rate and efficiency of nectar extraction by hummingbirds. Science 176, 1351-1352. Wolf, L. L., Hainsworth, F. R.,and Gill, F. B. 1975. Foraging efficiencies and time budgets of nectar feeding birds. Ecology 56, 117-128. Wolf, L. L., Stiles, F. G., and Hainsworth, F. R. 1976. Ecological organization of a tropical, highland hummingbird community. J . Anim. Ecol. 45, 349-379. Young, P.T. 1%7. Palatability: The hedonic response to foodstuffs. In "Handbook of physiology, Sect. 6: Alimentary Canal" (C. F. Code, ed.), pp. 353-366. Am. Physiol. Soc.. Washington, D.C. Zach. R.,and Falls, J . B. 1976a. Ovenbird (Aves: Parulidae) hunting behavior in a patchy environment: An experimental study. Can. J. Zool. 54, 1863-1879. Zach, R.,and Falls. I . B. 1976b. Foraging behavior, learning, and exploration by captive ovenbirds (Aves: Parulidae). Can. J. 2001.54, 1880-1893. Zach, R.,and Falls, J. B. 1976c. Do ovenbirds(Aves: Parulidae) hunt by expectation? Can. J . Zool. 54, 1894-1903. Zeigler, H. P.,Green, H. L., and Lehrer, R. 1971. Patterns of feeding behavior in the pigeon. J . Comp. Physiol. Psychol. 76, 468477.

ADVANCES I N THE STUDY OF BtHAVIOR. VOL. Y

Progress and Prospects in Ring Dove Research: A Personal View MEI-FANGCHENG INSTITUTE OF ANIMAL BEHAVIOR RUTCERS-THE STATE UNIVERSITY NEWARK, NEW JERSEY

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Major Features of Reproductive Behavior in the Ring D o v e . . . . . . . . . . . . . . 111. Hormones and Behavior: Lehrman’s Hypotheses . . . . . . . . . . . . . . . . . . . . . . . ............... A . Courtship and Nest Building

B. Female Reproductive Behavio ..................... C. Copulatory Behavior . . . . . . . . . ..................... D. Incubation and Squab Care . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. Questions of Reproductive Synchrony . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV . New Directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Brain Research with Respect to Steroid Action and Reproductive Function B. Photoperiodic Stimulation and Reproductive Behavior . . . . . . . . . . . . . . . V. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . ...........................................

I.

97 98 98 100 103 I06 109 1 I6 I18 1 I8 120 123 124

INTRODUCTION

Almost 15 years have elapsed since the late Professor Daniel S. Lehrman’s widely quoted chapter on Ring Doves appeared in Professor Frank A. Beach’s first edition of Sex and Behavior in 1965. In that paper Lehrman brilliantly illustrated how environmental cues and hormonal factors interact to induce a succession of synchronized stages in the reproductive cycle of the ring dove. Those of us who had the good fortune to hear Lehrman’s eloquent lectures about the courtship of ring doves remember vividly the classical grace of the experiments and the beautiful bow-coo display of the male dove so colorfully mimicked by him. With the untimely death of Lehrman in 1972, many friends might have thought that this line of research would dwindle. Today ring dove research by his students and colleagues is continuing in a number of laboratories here and abroad. Ring dove research continues to have one of its major centers (Hanebrink et a f . , 1977) in the Institute of Animal Behavior, established by Lehrman in 1957, where it is still one of the main lines of the graduate program in 91

Copyright

0 1Y7Y

by Academic Pre%

InC

All rights of rcprwlucrion in any form reserved. ISBN 0- 12-004SW-S

98

MEI-FANG CHENG

Psychobiology. The present paper is intended to review the more recent work on the reproductive behavior and physiology of the ring dove in the context of Lehrman’s research and theoretical formulations, to revise those concepts that need to be revised, and to restate those which have held up. I will then describe the extension of Lehrman’s theoretical framework and some new directions in which ring dove studies are moving.

11.

MAJORFEATURES OF REPRODUCTIVE BEHAVIOR IN THE RINGDOVE

The ring dove (Srrepropelia risoria) is a long domesticated form of the African Collard Dove, S. roseogrisa (Goodwin, 1967), especially suitable for laboratory study. It breeds well for most of the year in an indoor colony where day length (14 hr light and 10 hr dark) and environmental temperature (72 2 3°F) are controlled. In our colony, squabs at the age of 21 days are separated from their parents and placed in stock cages in groups of 6-10 birds. At 4-5 months of age, the sex of each bird is determined by exploratory laparotomy (Lehrman, 1955). When the birds are sexually mature (5-9 months old), they are placed in pairs and permitted to carry out a complete reproductive cycle. All the experimental birds unless otherwise mentioned had completed the cycle once or twice. When such a male and a female ring dove in breeding condition are placed together in a standard breeding cage (70 x 45 X 3.5 cm) with nest materials and a glass nest bowl, the male bows and coos, and the female responds with excitement (courtship). They enter into a sequence of predictable behavioral changes, highlighted by increasing activity in the nest just before laying and a sharp decline of overall activity upon arrival of a clutch of 2 eggs. Thereafter, the pair take turns in incubating the eggs until hatching. Parental care of the young then follows: it consists of covering the squabs in the nest until 8-10 days of age and feeding them by regurgitation of crop milk until about 18-21 days. Sporadic courtship behavior can be seen during later parental care, although full courtship does not usually occur until the young reach the age of fledgling (about 21 days) and are removed from the parents (Fig. 8). There are reports that the ring dove has established local wild colonies in Los Angeles, Miami, and Tampa, Florida (Robbins et al., 1966). Behavioral observations of these doves in the field revealed certain characteristics not often seen in the indoor colony (Cox and Silver, 1977), but none that has an important bearing on the results discussed here.

111.

HORMONES A N D BEHAVIOR: LEHRMAN’S HYPOTHESES

The most striking feature of the behavioral changes involved in ring dove reproduction is the synchronization between male and female behavior. Shifts

99

RING DOVE RESEARCH

from one behavior to the next in the reproductive sequence do not represent a simple unfolding of a preprogrammed chain of behaviors. Visual, auditory, and tactile stimuli continuously steer them, so that the behavior of one partner is appropriate to that of the other. For example, when a male and a female that have had reproductive experience but have not mated before are placed together (daily for 2 hours), the male, after a few rounds of bow-cooing and chasing, will select a site (usually the glass nest bowl) for his nest-coo behavior. The male will continue nest-coos for 3 4 days until his female partner begins to nest-coo. At that point the male's nest-coo begins to become less frequent (Fig. IA). Now, if you pair the same male with a female that is not easily aroused, the male will bow-coo, chase, and nest-coo as expected, but this time he will continue to nest-coo daily at an undiminished frequency for as long as a month if the female fails to nest-coo. As soon as she begins, however, the male's nest-coo tapers off for the first time (Fig. IB). In both cases, the male is physiologically ready to court (nest-coo), but the duration of the behavior depends upon the behavioral response from the female. It is the male who stirs the female, but the female signals when the male should stop cooing and move on to the next behavior, which is gathering and carrying nesting material to the female, who does most of the nest building. This sort of observation formed the backbone of Lehrman's research and theories. His studies led him to the following formulations: (a) Male courtship is induced by androgen (Erickson and Lehrman, 1964; Erickson, 1970) and stimulates the female via gonadotrophins, to secrete estrogen (Lehrman et al., 1961a,b). (b) Estrogen stimulates the female to build a nest (Lehrman, 1958b).

I

loo0

"I *TyL 0

I23451 DAY

MY

FIG. 1. Pattern of courtship behavior of a male during prelaying phase (A) with a respon. sive female, (B) with a nonresponsive female. (From Cheng, unpublished observations.)

I00

MEI-FANG CHENG

(c) Participation in nest building stimulates the secretion of progesterone in both male and female (Lehrman, 1958a), which induces doves to sit (Lehrman, 1958b). (d) Sensory input from the eggs during incubation (a) stimulates the secretion of prolactin which maintains further incubation (Lehrman and Brody, 1964) and produces “crop milk” (Patel, 1933) for feeding the young and (b) suppresses gonadotrophin secretion. In essence, Lehrman proposed that hormones induce behavior which (1) stimulates further secretion or secretion of a new hormone (effect on individual’s own system) and (2) stimulates hormone secretion in the partner (interindividual effect). These two systems operate simultaneously or in succession to produce synchrony between male and female reproductive behavior and physiology. With a few exceptions, most early research on the role of hormones in reproductive behavior used large-dose injections of exogenous hormone in intact doves, and changes in the activity of the endocrine system were inferred from behavioral data. I will now examine how Lehrman’s proposed outline of behavioral-hormonal interactions has held up under experimental tests using the more sophisticated techniques now available such as (a) measurement of blood concentrations of hormones by the method of radioimmunoassay and (b) evaluation of the causal effects of hormones on behavior by the classical approach of surgical ovariectomy and hormone replacement.

A.

COURTSHIP A N D NEST BUILDING

1.

Estrogen

Essential to the first step of Lehrman’s hypothesis is the idea that male courtship stimulates the female to secrete estrogen. This was tested by measuring the blood content of female doves before and after various lengths of exposure to male courtship. Female doves that were placed in isolation cages where they could not see each other but could hear colony sounds had low blood levels of estrogen (i= 27 pg/ml), but only one or two days after they were paired with males estrogen levels began to rise. They continued to rise as the number of days of association with males increased, reached a peak (i= 85 pg/ml), then declined around the stage of nest building. During the period of incubation blood levels of estrogen remained at a base-line comparable to that of isolated females (Korenbrat et al., 1974). Thus, radioimmunoassay data of pooled samples substantiate the first step of the hypothesis. The role of estrogen during its rising phase and the decline of estrogen during nest building appear somewhat at odds with the notion that estrogen induces nest building. This will be discussed in the context of the role of ovarian hormones in female reproductive behavior.

RING DOVE RESEARCH

101

2 . Gonadotrophins

G. W. Harris’ (1955) elegant work on the neural control of the pituitary-vary axis provided Lehrman with the framework for his hypothesis that courtship stimulates estrogen secretion. The hypothesis implies that gonadotrophins secreted by the anterior pituitary [luteinizing hormone (LH) and follicular stimulating hormone (FSH)], which stimulate and regulate ovarian hormone activity, increase as a result of male courtship. A reliable radioimmunoassay method for avian LH is now available (Follett et al., 1972). The plasma LH of females in social isolation was maintained at a low level = 2.11 ng/ml), rose to a peak = 5.43 ng/ml) after only 2 or 3 days of exposure to male courtship, declined following egg-laying (1= 3.77 ng/ml), and further declined after hatching = 2.23 ng/ml.) Females which had large follicles and which therefore might be expected to have relatively high LH levels (becauseof positive feedback of estrogen) also showed low levels of LH prior to pairing (Cheng and Follett, 1976). These data fit well with Lehrman’s notions that courtship stimulates ovarian hormones via gonadotrophins and that gonadotrophins are low during incubation and brooding; the data are also consonant with the general observation that female ring doves rarely ovulate in isolation even if they have somehow developed large follicles. Plasma FSH levels were not measured in this study since no assay was available at the time. More recent work has shown that changes in FSH level, in general, appear to be very much like those in LH (Follett, personal communication). I would assume therefore that FSH levels in female doves also rise after exposure to male courtship. To determine the exact temporal relationship between estrogen secretion on the one hand, and the release of FSH and LH on the other, would require assaying these hormones from the same blood samples during the breeding cycle.

6

6

(x

3 . Testosterone By manipulating male courtship and looking at its effect on the laying response, Lehrman demonstrated the effect of courtship on the female endocrine system. However, his hypothesis also implies that the female’s response affects the male endocrine system. This was borne out in a study in which an almost immediate rise of testosterone in the blood plasma were found in males exposed to a stimulus female but not to another male (Feder et al., 1977). 4. Role of Bow-Coo and Nest-Coo

The bow-coo display had a prominent place in all the early work on ring doves when the main direction of research was the effect of male courtship on female ovarian development. Erickson showed that both ovarian development and the number of ovulations by females were related to the amount of courtship activity shown by the males with which they were paired (Erickson and Lehrman, 1964; Erickson, 1970). Similarly, Barfield (1971a) found greater ovarian development

102

MEI-FANG CHENG

in females that had been exposed to two males consecutively for a total of one hour than females that had been with one male for one hour. Although in both cases females were exposed daily to one hour of courtship, the females courted by two males presumably received more stimulation. Precisely what is the stimulatory effect of the bow-coo and nest-coo displays? In the courtship repertoire of the ring doves, bow-coos are the main behavioral pattern that is not only androgen dependent (Erickson, 1970; Hutchison, 1970a; Cheng and Lehrman, 1975) but also specific to males (Cheng and Lehrman, 1975). Nest-coos (and wingflip) are performed by both sexes and can be elicited by both androgen and estrogen in males (Hutchison, 1970b; Cheng and Lehrman, 1975) and females (Cheng and Lehrman, 1975). Bow-coos and nest-coos also differ in their acoustic features (Davies, 1974; Mairy, 1977), in posture (Miller and Miller, 1958), and, interestingly, in the kind of response they elicit from females. During the earliest stages of courtship, bow-coos by males characteristically elicit self-preening by females. At this stage bow-coos also may provoke fleeing, especially when coupled with a charging component; the females then continue to display self-preening at a distance from the male. Nest-coos by the male, on the other hand, initially elicit approach by the female, and at a later stage also stimulate the female to nest-coo along with the male. Bow-coos therefore seem to repel females, nest-coos to attract them. In this sense bow-coos exert a negative effect-or do they? Attempts to compare the relative effects of bow-coos or nest-coos on ovarian development have met with a technical difficulty; it is almost impossible to elicit only bow-coos from males. Androgen treatment high enough to restore bow-coos in castrated males also restore nest-coos (Hutchison, 1970a; Cheng and Lehrman, 1975). However, Hutchison and Lovari (1976) recently found that courtship behavior that included both bow-coos and nest-coos had a greater stirnulatory value than courtship that consisted of nest-coos only. Apparently bow-coos exert some positive stimulatory effect on females, even though their immediate effect is to repel them. Erickson (1970) however reported a positive correlation between female ovarian activity and the frequency of nest-coo by the male during the first half-hour after pairing. Can we resolve these seemingly conflicting effects of bow-coos? There are no conspicuous physical characteristics that differentiate males from females in this species. In view of the fact that the bow-coo is specific to males, it can be argued that the bow-coo could communicate sex identity. The significance of bow-coos may be inferred from female-female pairings separated by a glass partition (and from a few cases of male-female pairings as well) where bow-coos are absent in the courtship interaction; it takes significantly longer for ovulation to occur in female-female pairs than in female-male pairs (Cheng, unpublished observation). This notion about the bow-coo also fits the observation that the frequency of the bow-coo typically decreases as the number of courtship days increases

RING DOVE RESEARCH

I03

(Cheng, 1974; Erickson, 1973; Lovari and Hutchson, 1975) but is restored to high levels on the first day of pairing after an interruption of five consecutive daily pairings for 2 days (Cheng, unpublished observations). Erickson and Moms (1972) also found that males perform many fewer bow-coos and more nest-coos to a former mate than to a new mate. In summary, the courtship value of bow-coos lies principally in their ability to shorten the process of sex identification rather than in their direct stimulatory effect on ovarian development. One point must be stressed here: While many aspects of reproductive behavior are hormone dependent, it does not follow that these behavioral events are determined solely by hormonal conditions. Hormonal conditions provide the individual with a potential for the elicitation of a given behavioral pattern (Beach, 1974), but its induction depends upon the presence of adequate appropriate stimuli and the individual’s past experience. This is illustrated by nest-building behavior. While nest building is hormonally influenced (Cheng and Silver, 1975), White (1975a,b,c) has shown that the level of nest-building activity also depends on the condition of the nest. Thus, nest activity is high if the nest is emptied regularly by the experimenter, and low when they have completed a full nest, or a handmade full nest is provided throughout nest building and into the incubation period. This result corroborates the finding in canaries by Hinde (1958). Although this theme has been emphasized both by Hinde (1965) and Lehrman (1965). it is often lost sight of in discussion of the influence of hormones on behavior. REPRODUCTIVE BEHAVIOR AND PHYSIOLOGY B. FEMALE

I . The Prelaying Phase Based on 2-hour daily behavioral observations of doves throughout the breeding cycle, I divided the prelaying phase of the female breeding cycle into 9 stages ranging from nonresponsive to male courtship to active nest building the day before laying (Cheng, 1973a). Each stage was characterized by the display of certain specific behavior patterns, occumng for the first time since pairing in that stage; each stage had definite relationship to the time of egg laying (i.e., number of days prior to the laying of the first egg (Fig. 2). Then, by using egg laying as a reference point ( I ) orderly changes in the behavioral patterns, (2) ovarian development (in terms of follicular size), and (3) estimated blood levels of ovarian hormones, could be expressed side by side on one scale (Cheng, 1974). In the beginning of the courtship phase, while the male courts characteristically with rounds of hop-charging, bow-cooing, and nest-cooing, the response of the female is characteristically that of Stage I or 11. As the days of pairing increase, the female’s responses progress stage by stage along the scale until laying. The female may start with Stage I11 (or IV) if ovarian follicles of 6-8 mm

104

MEI-FANG CHENG Stages of Responswveness

,. ..

In

~snsleRing h a

-

,_.

FIG. 2. Definition of stages of responsiveness in female ring doves. (The horizontal line shows the days (D)on which the respective behavior pattern is present. The vertical stripes indicate the day on which it first appears in greater than 50% of the birds. (Symbols: I = nonresponsive, I1 = low responsive, 111 = approaching, IV = next-coos, V = proceptive sexual crouching, VI = crouched nest-coos, VII = nest-site defense, VIII = nest-coo decline, IX = active nest building, X = egg laying.) (From Cheng, 1973a.)

are already formed when the male is first introduced, but, regardless of the stage at which the female starts, the subsequent behavioral changes occur in the same sequence. The fact that behavioral and physiological changes occur in predictable sequence and in relation to each other suggests some causal relationship. Lehrman’s hypotheses suggest two possible directions of causation: (1) endocrine changes lead to behavioral changes or (2) behavioral changes lead to the individual’s own endocrine changes. I will deal now with the first possibility. 2 . Effects of Ovariectomy In many species of birds, including doves, only the left ovary is normally functional. Reproductively experienced, normal females which show wingflipping or nest-cooing behavior in response to male courtship cease to do so after sinistral ovariectomy. Despite the male’s persistent courtship, such a female

RING DOVE RESEARCH

105

avoids the male and stays on top of the food can, coming down for food or to peck around and occasionally ventures to inspect the male by pecking at his tail but never participates in courtship behavior. As soon as the male directs his courtship behavior toward her, she shies away or flies back to the top of the food can. About 6 to 10 weeks after surgery, however, such females begin to show wingflipping in response to male courtship and eventually develop the female behavior pattern in full. In such cases laparotomy revealed regeneration of ovarian follicles on the right side of the abdomen: apparently these were secreting the hormones responsible for the recovery. Upon removal of the regenerated right ovary, such a female again became nonresponsive (Cheng, 1973a). The ovary clearly regulates the behavioral changes of the female in the prelaying stage. Since follicular growth follows a predictable course, from the viewpoints of both morphology and secretory activity, the next task was to determine whether there is a causal relationship between follicular growth and the orderly changes in behavior seen during the prelaying phase. The basic experimental design involved careful observations of behavior before (3-5 days) and after bilateral ovariectomy (3-5 days) and before and after hormone replacement injections (14 days). Observations of behavior were made daily for a period of 2 hr immediately following the introduction of an actively courting male; a glass bowl and nesting material were always present on the side of the compartment which housed the female. Daily observations during periods of steroid treatment enabled me to follow the course of behavioral recovery. Steroid treatments included estrogen (estradiol benzoate, EB) in the dose range of 5-100 pg for 10 days or progesterone (100 pg/day for 7 days), or estrogen for 7 days plus progesterone on the last 2 days of estrogen treatment. Two features stand out in these studies: ( I ) Estrogen treatment alone restores all characteristic female behavior patterns (such as wingflipping and nest-coo) except nest building and incubation. (2) The former behavior patterns appear during recovery in the same sequence in which they normally appear in the intact female (i.e., they follow the sequence of 9 stages shown in Fig. 2) (Cheng, 1973b; Cheng and Silver, 1975). The behavior patterns characteristic of the earlier stages recover first, followed by those of later stages. Progesterone does not reliably restore any specific behavior pattern; however, combined with estrogen, progesterone enhances nest-cooing behavior and restores all nest-oriented behavior, including nest building, the tucking-in component of nest b-lilding performed normally by females, and incubation behavior (Cheng and Silver, 1975). These findings, together with radioimmunoassay data on blood levels of estrogen and progesterone, allow us to reconstruct the relationship between ovarian hormones and female behavior as follows. Upon exposure to a male, circulating estrogen in the female rises. This induces the female to display first wing-flipping, and then nest-cooing, as the circulating

106

MEI-FANG CHENG

estrogen reaches its peak. Sometime later, progesterone starts to rise and estrogen starts to decline; the combined action of both steroids enhances activity in the nest which includes nest-cooing, nest building, and incubation. Thus Lehrman’s original finding with intact females that estrogen is the hormonal basis for nest building must be revised, what he saw was the combined actions of endogenous progesterone and exogenous estrogen.

C. COPULATORY BEHAVIOR As shown in Figure 2, copulation takes place throughout the courtship phase. Sexual crouching during the earlier stages of courtship is characteristically initiated by the male’s display of preening near to the female, to which the female responds by preening. In turn, the male continues preening while circling the female. At certain points in this mutual display of “displacement preening” (Miller and Miller, 1958) the female approaches the male with the begging posture which leads to billing and courtship feeding. This ritual sequence usually is repeated one to three times before the female finally assumes the crouching posture. However, the female’s active display of sexual behavior begins only in Stage V when she crouches almost immediately after she is introduced to a male even before the male “invites,” this crouch often meets with an aggressive display by the male rather than mounting and copulation. In my previous publications, this type of crouching was designated as an “aggressive sexual crouch” since it often is preceeded by active approaches toward the male (almost charging the male) and often is accompanied by cackling sounds typical of an aroused bird. The term admittedly is awkward, hitherto I adopt the term “proceptive sexual crouch,” borrowing from Beach’s distinction between proceptivity and receptivity (Beach, 1976). The proceptive sexual crouch also is often accompanied by vigorous shoulder vibration. It is sustained longer and is more persistent than the crouching seen earlier.

Hormonal and Nonhormonal Control of the Sexual Crouch The study of the effects of estrogen treatment on ovariectomized doves described earlier included a paradoxical finding: At a dose of 100pg/day for 7 to 10 days, estrogen (EB) effectively blocked the expression of female courtship behavior; although at a lower level (50 pg/day), estrogen reliably induced these behavior patterns (Cheng, 1973b). Since an increase in oviduct weight did occur, reflecting the systemic effects of 100pg EB, the failure in behavioral expression must be due to a central effect. One possibility was that 100 pg/day estrogen exerts a negative effect on the hypothalamo-hypophyseal axis. The failure of estrogen to induce female courtship may be due to the low level of gonadotrophin-releasing factors (from hypothalamus) or gonadotrophins (from pituitary). To explore this possibility, the following experimental treatments were studied with respect to their effect on

RING DOVE RESEARCH

107

the expression of female behavior patterns in ovariectomized doves (Cheng, 1977a): ( I ) high dose estrogen (EB) plus synthetic luteinizing releasing factor (LRF), (2) high dose EB plus LH, (3) high dose EB plus thyrotropin releasing factor (TRF), and (4)high dose EB plus progesterone. Analysis of behavioral data revealed that high doses of estrogen would restore estrogen-dependent female behavior in the bilaterally ovariectomized dove only if supplemented by LRF. This result suggests that the gonadotrophin-releasing factor is normally involved in the induction of female behavior. This notion is supported by another set of results: A subthreshold dose of EB (EB,,,,, a dose level which is not high enough to induce behavior) plus LRF, or EBSubplus progesterone can restore female behavior, whereas EBSubplus TRF, EB,,b plus LH, LH alone, TRH alone, or LRF alone cannot. Interestingly, while both progesterone and LRF are effective in their synergistic actions with a subthreshold dose of estrogen to induce behavior, they differ in the type of female behavior restored. EBSubplus progesterone facilitates nest-coo behavior, while EBSubplus LRF facilitates the proceptive sexual crouch. Consistent with this finding is the ability of an antiovulatory LRF analog (WY-18,185) to block specifically the proceptive sexual crouch in intact females. This specific behavioral effect of combined LRF and EB fits well with the natural occurrence of the proceptive sexual crouch and temporally associated hormonal changes during the normal breeding cycle (see Fig. 3). In the scale of nine stages of behavioral responsiveness, the proceptive sexual crouch characteristically appears just when blood estrogen levels begin to fall and LRF contents rise as projected from the known preovulatory surge of LH. The proceptive sexual crouch therefore is closely related to ovulatory events, much like “heat” is related to preovulatory LH in the estrous cycle of several mammalian species. The relationship between the proceptive sexual crouch and hormonal events is also reflected in an earlier finding: Bilateral ovariectomy abolishes the proceptive sexual crouch but not the sexual crouch initiated by a male; the latter is characterized by sequential mutual display of precopulatory behavior which is seen most frequently in the early phases of courtship (Cheng, 1973a). The significance of the proceptive sexual crouch, closely preceding ovulation, is evident in the following study. Male and female birds were exposed to each other 24 hr a day for 1 to 7 days with a glass partition between them; on the day of the copulation test, the glass partition was removed and the pairs were allowed to copulate once or twice, where upon the glass partition was reinstalled. The percentage yield of fertile eggs was significantly greater when copulation took place around or after Stage V , even if only a single copulation was allowed. Multiple copulations during earlier stages yielded low percentages of fertile eggs (Cheng and Porter, 1976). If one or two copulations are sufficient to produce fertile eggs, why do ring doves copulate 7 to 14 times before Stage V? Why should the males invest their sperm in the “futile” copulations, or do they? These are intriguing questions for

108

MEI-FANG CHENG

~~

~

0

DAYS FROM IST LAYING -7

-6

-5

-4

-3

-2

STAGES OF 1-111

0

I

5

OVlPOSlTlON

ISOLATION

BEHAVIORAL RESPONSIVENESS

-I

IV

v

VI

VI

Vlll

10

I5

HATCHING

20

25

30

WJAB SWAB LEAVE LEAVE NEST WRNTS

IX

PSC

FIG.3. Changes in hormone levels and female responsiveness during the courtship phase of the breeding cycle of ring doves (Streptopelia risoria). The LH curve is based on the findings of Cheng and Follett (1976); the progesterone (P) curve is based on the findings of Silver et a/. (1974); and the estrogen (b)curve is based on the findings of Korenbrot et al. (1974). The stages of behavioral responsiveness are based on the findings of Cheng (1973a). PSC, proceptive sexual crouch. (From Cheng, 1977a; reproduced as appeared in the Journal of Endocrinology.) which there are yet no definite answers. Possible functions of multiple copulations include the following: (a) They may be part of a process of bond formation or mate testing, (2) they may accelerate the process of reaching ovulation, and (3) they may facilitate the production of viable sperm. In our preliminary histological study (Cheng and Butler, unpublished observations), males in isolation and males that have been exposed to females for 24 hr characteristically have sperm attached, and little or no free sperm in the lumen of seminiferous tubules. On the other hand, the testes of males which had paired with females for 5 to 7 days contain free sperm densely packed in the lumen. Erickson and Zenone (1976) reported that males showed more courtship and less aggressive behavior toward unstimulated females and more aggressive and less courtship behavior toward females that have been exposed to other males. They suggested that the difference in response may enable the males to avoid cuckoldry. With respect to the actual interaction between the male and female, clearly the quality of male courtship depends very much on the behavioral pat-

RING DOVE RESEARCH

109

terns exhibited by their mates. What are the behavioral differences exhibited by these two groups of females? They reported that preexposed females readily showed nest-coo display when introduced to the test males while the unstimulated females did not. Unfortunately, data on sexual crouch patterns were not given. In my observation, sexual crouch patterns is a crucial feature differentiating between unstimulated and preexposed females. The proceptive sexual crouch characterizes the stimulated female very well. I find that a male almost never mounts and copulates in response to the persistent, self-initiated proceptive sexual crouch, unless he “knows” the female. Thus, when I expose a pair to each other through a glass partition for several days, and then allow them free access to each other, the female will cackle and aggressively approach the male, then crouch and the male will then stop bow-cooing and mount her.

D. INCUBATION AND SQUABCARE The most striking behavioral change in ring doves during the reproductive cycle is the transition from the highly visible activity of the prelaying phase to minimal activity during incubation and brooding. What makes the bird change from a nonsitting bird to a sitting bird? Lehrman approached this problem first by analyzing the contributions of behavioral (courtship, nest-building) (Lehrman, 1958a) and situational (nest bow, nest materials) (Lehrman et al., 1961a) factors. He then asked what physiological condition underlies the initiation of incubation? He answered that progesterone is probably the hormonal initiator of incubation. In support of this hypothesis he demonstrated that pairs of male and female birds, which were not ready to sit, exhibited incubation behavior with injections of progesterone for 7 days during isolation before the test, which consisted of introducing a handmade nest containing two eggs and the mate (Lehrman, 1958b). Other hormones, such as prolactin, were effective only in maintaining but not in inducing incubation behavior (Lehrman and Brody, (1961). The basic finding has subsequently been corroborated for males: Stem castrated the male and gave replacement injections of androgen or estrogen, with or without progesterone (Stern and Lehrman, 1969; Stern, 1974); and Komisaruk (1 967) induced male sitting behavior by implanting progesterone directly into the brain. On the basis of these studies the original conclusion was refined with the proposal that the combined action of androgen and progesterone initiates male incubation. Based on pooled samples (i.e., data representing various stages of the breeding cycle were drawn from different groups of birds; stages were determined by number of days of pairing), Silver et al. (1974) reported the following patterns of progesterone secretion: (1) In the female, progesterone showed a sharp rise @ = 3.01 ng/ml) around the time of egg laying, a decline thereafter, and remained at a lower level throughout the period of incubation and brooding (2 = 1.12 ng/ml).

110

MEI-FANG CHENG

(2) In the male, progesterone levels did not show a clear pattern of change; the average during the cycle (f = 1.27 ng/ml) was higher but not significantly different from that of females following egg laying. How does this set of data fit into Lehrman’s hypothesis that progesterone is the hormonal initiater of incubation behavior? At first sight, the assay data appear to corroborate the progesterone hypothesis for the female, since in the female progesterone rises around the time of laying. However, this sharp rise in progesterone can be easily accounted for by its role in ovulation (Rothchild and Fraps, 1949; Wilson and Sharp, 1976). Moreover, a progesterone surge has been shown to be closely related to ovulation in hens (Furr et al., 1973; Etches and Cunningham, 1976). The hypothises that the progesterone surge in ring doves has something to do with induction of incubation in the female derives support from the ovariectomy-hormone replacement study discussed previously. This work clearly implicated progesterone, acting with estrogen, in the induction of incubation in female doves. The role of progesterone in the male requires more careful assessment. As stated previously, recent studies suggest that a combined action of androgen and progesterone induces incubation in males. The radioinimunoassay data demonstrate measurable progesterone secretion in the circulation of males during incubation. Therefore, the assay data are in harmony with the hypothesis. They could also be used to negate the hypothesis if one interprets it as implying that there must be an actual rise in blood levels of progesterone for the initiation of incubation in the male. This has been the opinion of Silver, who also reasoned that if progesterone is necessary for male incubation, then birds deprived of circulating progesterone should not show incubation behavior. By injecting males with dexamethasone (DEX), an ACTH blocker, to deplete presumably the circulating progesterone, Silver and Buntin (1973) showed that male doves would sit on eggs for 7 days of the 14-day incubation period despite the drug treatment and concluded that progesterone is not obligatory in the induction of male incubation. However, in this study, and in subsequent studies using castrated males (Silver and Feder, 1973), the progesterone-blocking agent was administered daily for 7 days after the pairs had already established their incubation behavior: With the exception of one group (intact males), DEX was administered starting the evening of the first egg laying (the second egg about 34 hr later). This is unfortunate because (1) these studies were intended to investigate thc induction of incubation behavior and (2) ring doves show all components of sitting behavior and can be induced to sit on eggs before their eggs are laid. These results can be interpreted as follows: For reproductively experienced pairs, the male may continue to participate in incubation even after progesterone secretion has been blocked, when all situational stimuli are normal (e.g., free access to the female during courtship, nesting, and laying stages in a standard breeding condition prior to the

RING DOVE RESEARCH

111

drug treatment). Read in this manner, their results are compatible with Lehrman’s progesterone hypothesis. For reproductively experienced doves, castration does not always block the induction of incubation behavior, especially when they were paired with mates with which they had previously been paired (Cheng, unpublished observations). Thus, hormonal (androgedestrogen and progesterone) factors and situational (mate, nest) factors complement each other in the induction of incubation behavior. Incubation behavior can be induced when either or both of these factors is present, but not when both are absent (Cheng, 1975). In the normal breeding cycle, both factors are present. How does progesterone induce birds to sit on eggs? Does progesterone “turn on” sitting behavior in a similar manner to the drinking response of rats after a hypertonic saline injection? Careful behavioral observations (Cheng, 1975) of doves treated with progesterone suggests that progesterone facilitates the behavioral patterns characteristic of the presitting stage, namely, nest building and nest cooing (wing-flipping and cooing in a partly crouched posture in the nest bowl) (Stem, 1974; Cheng, 1975; Michel, 1977). As it approaches laying, the bird in the nest becomes much quieter. The behavior of the bird in the nest at this stage is almost identical to that of a bird sitting on eggs. It is a small wonder that the bird at this stage will incubate eggs. A similar ability to incubate eggs before laying has also been reported in gulls (Beer, 1963). In summary, recent research results support Lehrman’s hypothesis regarding the role of progesterone in the induction of incubation, with the following modification: Progesterone synergizes with gonadal hormone to facilitate an incubation response by way of inducing nest-related activities. I would like to add the following tentative account of progesterone action in male and female ring doves. The synergistic action of progesterone and gonadal hormones might take place when the progesterone-sensitive neurons are activated, apparently as a result of a lowered threshold. The precise mechanism for the latter is not presently known. However, the differential ratios of progesterone to other hormones such as estrogen in the female (Korenbrat et al., 1974) and testosterone in the male (Feder et ul., 1977), which rise then fall during the prelaying phase, may be the underlying mechanism. In the case of the female, the preovulatory progesterone surge coincides in time with the proposed change in threshold. It is interesting to note in this context that concentration of progestin nuclei receptors in the brain are increased by estrogen priming in the female rat (Blaustein and Wade, 1978). It is conceivable that testosterone priming also has the effect of increasing progestin receptors, either directly or mediated by aromatization in the male system. Finally, behavioral (Blaustein and Wade, 1978) and physiological (Leavitt et al., 1974) effects of progestin depend on the amount of progestin receptors available.

112

MEI-FANG CHENG

I . Suppression of Courtship Once a clutch of two eggs has been laid, the pair enters a relatively quiet period of incubation and parental care. Males sit from the late morning until later afternoon; females take over from late afternoon until the next morning (Fig. 4; Gerlach er al., 1975). In a careful study of 34 pairs of breeding ring doves, Heinrich used computer-monitored recordings of the 24-hr pattern of nest sitting and nest relief by male and female. Nests were well covered at all times throughout the period of incubation, with the exception of a brief irregularity during the initial stage (Heinrich, 1975). Thus, from the first day of incubation (the day after the first egg is laid) until the squabs hatch (15 days later) and reach the age of fledging (21 days later), there are about 35 days during which the pair rarely engage in full courtship that could interfere with incubation or parental behavior.

I 0 C

.L

0 0

.-0C 0

"c 21

Y

u

!!

LL

FIG. 4 . Incubation and relieving schedule of 46 experienced pairs of ring doves (pooled data from the 3rd to 16th day after the first egg is laid). Probability (in percent) that the male and/or female is incubating is presented, including YS% confidence limits of the medians. (From Gerlach ef (11.. 1975.)

RING DOVE RESEARCH

113

What are the mechanisms for such adaptive behavior? Lehrman suggested that the sensory stimuli derived from sitting on eggs and squabs stimulate secretion of prolactin, which maintains further incubation and suppresses gonadotrophin secretion and thereby suppresses courtship. 2 . Sensory Cues

We do not yet have direct evidence whether sensory cues from eggs and squabs can or cannot stimulate the secretion of prolactin, since there is no reliable prolactin assay for doves. Buntin (unpublished observations) found that parents with squabs have a significantly lower content of prolactin in the pituitary than those with squabs removed, hence verifying Hansen's (1966, 197 1, 1973) earlier finding on the stimulatory effect of squabs on the crop gland. He also showed that continued sitting on eggs beyond normal hatching did not cause an increase in crop sac growth-nly squabs could cause such an effect (Buntin, 1977a). Moreover, food-deprived squabs stimulate greater crop-sac growth, which is known to be prolactin dependent (Buntin et al., 1977). Thus, the available evidence supports Lehrman's notion that sensory input from the squab plays a role in prolactin secretion. Parent-squab interactions involve visual, tactile, and auditory cues. Buntin went on further to analyze the type of sensory cues that mediate crop-sac growth and the maintenance of incubation. It was found that ( I ) while maintenance of both incubation and crop-sac growth are prolactin dependent, more tactile stimulation is required to maintain incubation than activity of the crop gland, and (2) while tactile stimuli are most effective in stimulating crop-sac growth and incubation in both males and females, visual stimuli are more effective in the female than in the male. It appears, therefore, that there is a more refined sensory control of prolactin secretion in females. Buntin (1977b) has recently developed a receptor-binding assay for prolactin which will permit more definitive studies of this hormone and the factors that stimulate its secretion. 3 . Prolactin Secretion and Breeding Cycle

Parallel with parental activity is the apparent absence of full-scale courtship activity. In Lehrman's hypothesis, this is mediated by a negative influence of incubation on gonadotrophic activity. Is there evidence for this'? As will be seen, the mechanisms are more complicated than Lehrman originally envision2d. In a radioimmunoassay study of plasma LH levels throughout the breeding cycle, Follett and I were disturbed by the irregularity of LH results after oviposition. But to our surprise the behavioral data showed that, following oviposition, all the birds laying fertile eggs had a low LH level, while all the birds laying infertile eggs had a high LH level until, as would be expected, they laid a new clutch of eggs 2 weeks later (recycling before the completion of an ongoing cycle). Moreover, we did not find any interruptions of incubation behavior which

114

MEI-FANG CHENG

might have triggered the onset of recycling in these birds. These findings raised several intriguing questions: Did the recycling birds ever copulate? Could it be that LH release is mediated by neural feedback? And to what extent could cues from the eggs have contributed to the triggering of a new cycle? In order to answer these questions experimentally, normal females were paired with castrated males which received either (1) androgen treatment, so that they were capable of copulation but not of insemination, or (2) oil treatment, so that they were capable of neither copulation nor insemination (Cheng, 1977b). Additional females were paired with normal males which would copulate and inseminate the females. The results were surprising: Copulation alone did not appear to exert a significant effect on the incidence of recycling. Rather, recycling and hence the LH content of the postoviposition period was contingent on the fertility of the eggs. Information on the fertility of eggs can come from internal sources (insemination andor fertilization) and external sources. Infertile eggs may dry out in the course of time; texture changes of the eggshell, the temperature of the eggs, and acoustic emissions by normally developing embryos may give clues to the parents about the fertility of the eggs. The birds appear to make their “decision” about whether or not to stop the ongoing cycle and to recycle from both sources of information. When the information they receive about fertility of the eggs from both sources is consistent, the birds either complete the ongoing cycle or all recycle, depending on whether the eggs are fertile or infertile. In contrast, when they receive conflicting information, the responses of the birds are divided. Thus, when birds laying infertile eggs were given substitute fertile eggs on the day of laying, and vice versa, about half of them recycle with more variability in latency to recycle than birds laying and sitting on infertile eggs. The other half did not recycle until after the expected span of 42-46 days (which constitutes a normal complete cycle). The basic finding that fertile eggs delay recycling has been corroborated in another lab (T. Allen, submitted for publication). It has been shown that there is a surge in prolactin secretion around the time of ovulation in band-tailed pigeons (March and McKeown, 1973) and around the time of laying in fowl (Scanes et al., 1977). It is possible therefore, that prolactin secretion exerts an antigonadal effect, as shown by Bates et al. (1937) during the early stages of incubation, before the tactile stimuli derived from sitting on the eggs became intensive enough to trigger prolactin-dependent crop-sac growth. It would follow from this that birds which recycle have low levels of prolactin. It also seems that would-be-recycling birds should stop recycling if the prolactin level is artificially elevated by injection around the time of ovulation. This has been confirmed in a study in which about half of female ring doves laying infertile eggs (after mating with castrated, androgen-treated males) did not recycle when they received daily treatment with prolactin (100 pg/day for 7 days); the same pairs recycled in 2 weeks as expected when they received oil treatment instead (Cheng, 1977b). While prolactin treatment is not 100% effective, clearly

RING DOVE RESEARCH

115

changes in prolactin levels are one of the endocrine events associated with suppressing gonadotrophic activity and with recycling. Incubation data on the recycling birds again showed no reliable correlation between patterns of sitting and recycling (Fig. 5 ) . Observations of this type suggest either that under certain circumstances incubation can be maintained in the absence of prolactin, or that high levels of LH and prolactin can coexist. Still another possibility is that the preovulatory progesterone surge serves as a “timer” for the duration of maximum incubation. Thus, regardless of the fertility of eggs and the condition of prolactin secretion, birds may sit continuously for 21 days but not beyond (Cheng and Barbiere, unpublished observations). Since prolactin appears to regulate how soon the ovary starts to accelerate growth, it may serve in doves the function that progesterone serves in the ovarian cycle of most mammalian species (Brown-Grant, 1977). Crop-sac growth, like the development of the corpus luteum in mammals, signifies a temporary arrest of follicular development. Unlike the corpus luteum, the crop-sac itself does not secrete hormones. In summary, the hormonal events following ovulation, and their functions in the regulation of reproductive behavior, can now be reconstructed as follows: (1) Fertilization of the eggs, andor insemination alone, facilitate an initial increase in prolactin secretion around the time of ovulation. (2) Elevated levels of prolactin effectively (a) suppress gonadotrophin release, and thereby delay the onset of recycling, and (b) facilitate incubation behavior before its diurnal rhythm is firmly established.

DAYS AFTER INITIAL LAYINO

FIG.5. Incubation patterns of birds recycled. (From Cheng, 1977b.) Normal females were paired with castrated and androgen-treated males.

116

MEI-FANG CHENG

(3) Throughout incubation and the period of parental care the elevated levels of prolactin and their effects are sustained by tactile and thermal and, to a lesser degree, visual stimuli from sitting on eggs and then on squabs. Sustained high levels of prolactin in turn stimulate crop-sac growth in preparation for feeding the young. (4) After hatching, stimuli from squabs during feeding maintain prolactin levels. As soon as the young are old enough to feed themselves, prolactin secretion levels off in response to a lack of sustaining stimuli from the squabs feeding. This process of termination, at least in part, is aided by active refusal to feed on the part of the parents, beginning shortly after the squabs are old enough to leave the nest but are still dependent on the parents' feeding (Wortis, 1969). It should be quickly pointed out that Item (1) needs to be verified by assay data. This and related studies are currently in progress.

E. QUESTIONS OF REPRODUCTIVE SYNCHRONY Lehrman repeatedly emphasized the importance of sequential interactions between males and females for breeding success. Development of the later stages of the reproductive cycle is contingent on the successful interactions of earlier stages. For a pair to move from one stage to the next stage, the behavior of the male and female must be in synchrony. Is this synchrony achieved by hormonal control? Do male and female communicate their messages in a minute-to-minute manner? Answers to such questions may be found in a study by Friedman ( I977), who devised an ingenious experimental apparatus (Fig. 6) in which sounds from a central cage were transmitted to several peripheral cages that housed female SOUND PORT MIRROR REFLECTION SCREEN HORIZONTAL POLARIZER VERTICAL POLARIZER CAGE W A L L 6 0 W LAMP DOVE'S VIEW

-

~

____

*

...........

*

* *

FIG. 6. The arrangement of experimental cages used by Friedman for studying the influence of differing combinations of male courtship on ovarian growth. (From Friedman, 1977.)

RING DOVE RESEARCH

117

doves. By arrangement, the female doves could receive different combinations and configurations of stimuli provided by a courting male in cage E. Thus, a female in cage D could see and hear a male in cage E who was courting her. A female in cage F could see and hear the same male’s courtship behavior, but from a different angle because the male was facing the female in cage D. Females in cages B and H could see themselves in a mirror and hear the male in cage E (who could not be seen). In cage H the sounds of the courting male appeared to come from the mirror image; in cage B the sound came from the side of the mirror image. One purpose of this experimental arrangement was to determine whether spatial congruence of visual and auditory input is crucial for their stimulatory effect on ovarian development. Females of similar follicular size, determined by laparotomy at the beginning of the experiment, showed different follicular growth at the end of 7 days of exposure in the different cages. Surprisingly, spatial congruence of visual and auditory cues (cages H, etc.) is important, but is not sufficient to stimulate follicular growth. The females (in cage D) which saw and heard the males courting them showed the greatest ovarian development. Females (in cage F) which saw and heard the same male, although he was not oriented to them while courting, showed only mild ovarian development (Friedman, 1977). These results demonstrate that synchrony is achieved in part by close “reading” of the partner’s message. When a male’s display does not reflect a “correct reading” of the female’s message, further communication and transition to a more advanced stage of the reproductive cycle becomes difficult. When asynchrony arises, it is more often the male than the female which realigns its behavior with that of the partner. For example, males paired with females of advanced ovarian stages move quickly from bow-cooing and chasing, characteristic of early courtship, to nest-cooing and the nest-oriented behaviors of advanced stages (Cheng, 1974). Similarly, it takes less time for males to show nest-carrying behavior when paired with females which have received estrogen and progesterone treatment, and which therefore show nest attachment, than when paired with control females (Martinez-Vargas and Erickson, 1973). There is also evidence for a similar process in females. Females with large follicle diameter (13 mm, nearing ovulation) when paired with new males take as many days to ovulate as females with moderate follicular size (FS = 7 mm) (Cheng, 1974). A careful behavioral study is now under way in our lab to determine whether females in this situation revert behaviorally to an earlier stage of follicular development or “hold up” development. Another unresolved question with implications for synchrony is how the bird comes to associate a given hormonal state with a corresponding set of environmental stimuli, so that it responds properly when the combination of state and stimuli (hormonal and nonhormonal) reappears. For example, when pairs of doves treated with progesterone were provided with partners, nest, and eggs, the

118

MEI-FANG CHENG

reproductively experienced birds responded by sitting on the nest. Michel ( I 977) showed that this proper response to a given situation and hormonal state is not entirely preprogramrned. Michel was concerned with the question of what aspects of the previous breeding experience are relevant for progesterone-induced incubation. He found that previous breeding experience inclusive of at least the nest-building stage of the breeding cycle significantly facilitates the incubation response to progesterone treatment and introduction of a mate, nest, and eggs. It appears therefore that breeding synchrony involves several mechanisms: ( I ) hormonal synchrony between the pairs, (2) association of given hormonal states and corresponding environmental stimuli, acquired and enhanced through experience, and (3) “reading” of the partner’s behavior patterns with respect to their relevance to the individual’s behavior. For the most part, the importance of synchrony has been assumed rather than based on a hard evidence. A critical test should compare breeding success among the following groups: ( I ) males already at an advanced stage of the breeding cycle paired with females in an early stage, and vice versa, (2) males and females both at advanced stages paired for the first time. Latency to lay, fertility of eggs, and rearing of young should serve as measurements of breeding success.

IV. A.

NEW DIRECTIONS

BRAINRESEARCHWITH RESPECT REPRODUCTIVE FUNCTION

TO STEROID

ACTIONA N D

Until recently, progress made in this area was limited to identifying the area within the hypothalamus that mediates male courtship behavior. By direct implants of steroids into the brain, the preoptic and anterior hypothalamic areas have been identified as regions mediating androgen-dependent courtship behavior, such as bow-coo, nest-coo, and nest-carrying behavior (Barfield, 1971b; Komisaruk, 1967; Hutchison, 1967, 1970b; Erickson and Hutchison, 1977) and progesterone-dependent incubation (Komisaruk, 1967) in male ring doves. Since Hutchison (1976) has already dealt in detail with various aspects of androgen action in the hypothalamus, I shall devote this section to recent progress concerning the site of estrogen action in female dove. That hormones act in discrete areas of the brain to initiate chain reactions of neural and biochemical events which result in changes in behavior is demonstrated by the effects of direct implantations of androgen in the preoptic hypothalamic area mentioned above. However, for this type of result to have any implications for the natural condition, it must be shown that these areas concentrate and retain the steroid. I n male ring doves previously injected intravenously with radioactive androgen, the labeled androgen is concentrated more in the

RING DOVE RESEARCH

119

preoptic-hypothalamic area than in other parts of the brain (Stem, 1972; Zigmond et al., 1972), a finding consistent with the results of direct steroid implantations in various areas of the brain. More recently, Martinez-Vargas et al. ( 1973, employing radioautographic techniques which allow the precise mapping of steroid uptake in brain tissue, have provided a detailed map of estrogen retention in male and female ring dove brains. With this new information concerning estrogen retention in the female dove brain, we have begun a systematic study of !he function of the estrogen-retaining areas with respect to various components of female courtship behavior and endocrine systems. With the aid of stereotaxic instruments and the atlas of the pigeon brain by Karten and Hodos (1967), adjusted to dove brains (Cooper, 1974 unpublished observations), a double cannula (inner cannula measures 28 gauge in diameter) containing crystalline estrogen (estradiol benzoate) is unilaterally implanted in various areas of the hypothalamus and midbrain. The areas found reliably to elicit female behavior such as wing-flip, nest-coo, and the sexual crouch are the medial preoptic area, the anterior hypothalamus, the posterior medial hypothalamus and the nucleus intercollicularis. Similar implants in the region of the n. tuberis-infundibulum and in other areas of the hypothalamus and cortex do not have such an effect (Cheng, unpublished observations). The blockage of reproductive behavior after lesioning (electrolytically) various regions of the hypothalamus produces a somewhat different picture. Lesions in the anterior hypothalamus do not appear to block behavior, while lesions in the posterior medial hypothalamus and the anterior preoptic area produce a clear blockage of behavior (Gibson and Cheng, 1977). Interestingly, all of these birds eventually recovered. It is tempting to argue that the recovery of function in these birds involves areas such as the anterior hypothalamus which retains estrogen and is capable of eliciting behavior if stimulated directly by estrogen, but probably is not normally involved in the behavior since lesioning the area has no effect. Naturally, the validity of this argument has to be determined experimentally. Another unexpected but potentially exciting finding has come from a study of behavioral blockage after lesioning in the n . intercollicularis (KO) region of the midbrain. This is a region anatomically adjacent to n. mesecephalicus lateralis (MID) which receives auditory inputs (Karten, 1966). Electrical stimulation of ICO has been reported to produce vocalizations in the male of various avian species (Brown, 1965a; Phillips and Peck, 1975), and bilateral lesions of this structure mute both male chickens (Phillips and Peck, 1975) and male passerines (Brown, 1965b; Nottebohm et al., 1976). With bilateral lesions in the ICO region, intact female doves which nest-cooed prior to the operation became mute. More intriguing is the finding that these females also failed to show ovarian development after exposure to male courtship for a period longer than sham lesioned females, who showed significant follicular growth using a similar testing procedure (Cohen and Cheng, 1977). Analysis of male courtship data indi-

120

MEI-FANG CHENG

cates that this difference in ovarian development was not due to different levels of male courtship in lesioned versus sham-lesioned groups. The significance of this finding can best be appreciated in the light of the following: (1) Nest-cooing by female doves is estrogen dependent (Cheng, 1973b; (2) female doves nest-coo in response to male nest-coos; and (3) nestcoos by female doves are the most reliable behavioral predictor of ovarian development (Cheng, 1973a; Erickson and Martinez-Vargas, 1975; White, 1975). There are two possible interpretations of the negative effect of midbrain ICO lesions on follicular development: (1) The ICO region may be part of an important pathway mediating the stimulatory effect of male auditory courtship on the female’s hypothalamo-hypophyseal axis; and (2) emission of nest-coos by females may normally exert a stimulatory feedback to their own endocrine system; thus, when the ICO region is damaged, and muting follows, the expected ovarian development also is blocked. If the second interpretation is verified by future experimental testings, this will constitute the first solid evidence of an effect of behavior on the individual’s own endocrine system as conceived in Lehrman’s hypothesis. Contrary to popular impression, ring dove research has not demonstrated a direct effect of behavior on the individual’s own endocrine system. It is difficult to separate the effect of male courtship on ovarian development from that of the female’s behavioral response to male courtship, which might react back on her own endocrine system, since female behavior patterns cannot be elicited in the absence of males. This explains why we are excited about the potential significance of the ICO lesion results, that is, the blockage of male courtship induced ovarian development in the absence of the female’s own nest-coos. A N D REPRODUCTIVE BEHAVIOR B. PHOTOPERIODIC STIMULATION

Modem laboratory conditions, controlled lightdark cycles, ambient temperature, and noise-proof cages in some cases, provide us with ideal conditions for experimentation throughout the year and free us from concern about the possible interaction of these factors in experimental results. By our own design, therefore, we often overlook these factors. Work by Hinde and Steel (1978), however, points to the importance of including these environmental factors in the study of hormone actions on behavior. For example, a long day length was found to facilitate estrogen-induced nest-building activity in ovariectomized canaries. Liley’s (1976a,b) work with intact ring doves suggests a similar interaction between photostimulation and exogenous estrogen in influencing the responsiveness of females. In this context it is relevant that: (1) a small but consistent percentage of females in the isolation room, where they can hear but cannot see other doves, lay eggs in their individual cages; (2) random samples of female

RING DOVE RESEARCH

121

doves from isolation cages show various stages of ovarian development, although these birds have been kept in isolation rooms for about 5 weeks since the last exposure to male courtship. The prevalent view has been that in this species follicles do not develop beyond 2-3 mm in diameter (“resting stage”) under LD 14:10 photoperiodic stimulation. Barbiere and I have investigated: (1) the percentage of females showing spontaneous ovulation while in visual but not auditory isolation throughout the year, for 3 4 years and (2) the percentage of such ovulations in reproductively inexperienced vs experienced birds of matched age. Males and females were laparotomized at 5-6-week intervals to measure the diameter of,the largest follicle, or testis width and length, under two photoperiodic regimes LD 14:10 and LD 8: 16. We found (1) that a 14 hr light period has a stimulatory effect on ovarian development, beyond the “resting stage,” and (2) evidence for seasonal effects in the “well-controlled” laboratory conditions.

I.

Ovarian Development under Photoperiodic Stimulation

Under the photoperiod regime of LD 14: 10, follicles of reproductively experienced females developed from a size of 2-3 mm to 3-10 mm in diameter over a period of 12 weeks, and few of them ovulated (- 1%). The rate of follicular growth is extraordinarily slow; a similar follicular growth takes only 5 to 7 days if a courting male is present, and courted females almost always ovulate in 7-10 days. Reproductively inexperienced females behaved differently under the same photoperiodic regime; it took less time (9 weeks) for their follicles to grow from 2-3 mm to 8-10 mm, and a greater percentage of them ovulated (4%) in the isolation room. These observations, together with the finding that inexperienced pairs take significantly longer to ovulate than experienced pairs (Lehrman and Wortis, 1967), suggest the following: The female endocrine system is quite responsive to photosimulation, but once conditioned to male courtship, the system becomes selectively responsive to it. It is not clear whether there is a critical stage for this response (Cheng and Barbiere, in press). 2. Gonadal Development under Short Photoperiodic Stimulation Under short photostimulation (LD 8: 16), the gonads of both males and females regress (G. R. Guilfoyle, unpublished). With the procedure of laparotomy at 5-6 week intervals, we followed the process of regression for individual bird: and continued this procedure for more than 4 months. To our surprise, we found that follicles and testes recovered in size, and some were larger than the original measurements recorded at the beginning of short photostimulation (Fig. 7). To determine whether this was part of an endogenous rhythm, we continued the observation under a LD ?h:23% regime (constant dark is experimentally impossible since birds refuse to eat in the dark). It was early in February of 1974 when

122

MEI-FANG CHENG

r

9

20

AUG

SEPT

I W

13

24

MC

JAN

1973

1974 DPTE

Cf

LAPAROTMY

FIG.7. Ovarian regression and recrudescence under short photoperiodic regime (LD 8: 16). (From Cheng and Barbiere, unpublished observations.)

we started this study. After two months I was at a loss to explain data showing no sign of gonadal regression. It then occurred to me that seasonal variation may have been involved in these findings. We had conducted our first study, which clearly illustrates gonadal regression and recrudescence, during the fall of 1973. Subsequent control studies have confirmed that there are seasonal variations in the activity of the hypothalamo-hypophyseal axis which regulates gonadal activity (Cheng and Barbiere, in press). If the activity of the hypothalamo-hypophyseal-gonadalsystem shows seasonal change, as suggested in the preceding study, we would expect the same factors to operate in many related reproductive functions. The following observations and experimental findings suggest that this is the case. ( I ) The annual occurrence of spontaneous laying is consistent with seasonal changes outside the lab from year to year. (2) Gonadal regression induced by short photoperiodic regimes (LD 8:16; LD '/i:23%) was negligible in the spring season, but was prolonged in the fall and early winter. (3) The'minimum androgen dose required to induce postcastration courtship behavior was higher in the fall than in the summer reminiscent of Hutchison's (1 974) finding with hypothalamic sensitivity. (4) Male doves whose right testes were removed showed a compensatory testicular hypertrophy in 100% of the cases (see following section) when the surgery was performed in the spring, but only 75% of the males showed a good response in the fall. ( 5 ) Squabs (female) hatched in the spring reached reproductive maturity sooner than those hatched in the fall. These observations suggest the existence of a seasonal regulator that is not dependent on photoperiodic changes as a stimulator or as entraining agents (Cheng, 1977~).What cues

RING DOVE RESEARCH

123

inform the birds of seasonal changes outside the light-sealed rooms and thick brick walls and ceiling await future studies. 3. Interaction of Photostimulation and Courtship Stimulation We know a great deal about how courtship stimulates endocrine changes in females and males and how photostimulation affects the same endocrine systems. The next question is how these stimuli interact to produce species-specific endocrine responses. To investigate this problem, 1 removed the right testis (the larger of the two) from male ring doves and observed the compensatory testicular hypertrophy of the left testis under 5 conditions, characterized by daily photoperiod (LD 14:lOor LD 8:16) and courtship condition (isolation cage or breeding cage containing female, nest bowl, and nesting materials). At the end of 4 weeks, the left testis was removed from each bird. Since the left testes of intact male doves kept under LD 14:lO were about 80% the weight of the right testes, I used a left testis larger or equal to 80%of the right testis as evidence for compensatory hypertrophy in each bird. As expected, the compensatory response occurred in all birds kept under the long photoperiodic regime (LD 14:lO) but not in birds kept isolated and under a short photoperiodic regime (LD 8:16). To my surprise, however, a good compensatory response also occurred in birds kept under short daily photostimulation and exposed twice to stimulus females. Two brief exposures to a stimulus female (20 min each and 1 week apart) had the same effect on males as 6 additional hours of light per day (LD 14:lO) for 4 weeks. The stimulation of female courtship under this photoregime is more effective than is the longer light period without it, a finding that is reminiscent of the greater effect of male courtship than of long light period on the female system. I may also point out Hinde and Steel’s finding with female canaries and budgerigars that male courtship facilitates the ability of estrogen in inducing nest-oriented behavior (Hinde and Steel, 1976, 1978).

V.

CONCLUSION

It is fitting to end this paper with a chart (Fig. 8) that summarizes important known factors (hormonal and nonhormonal) and their interactions involved in controlling the reproductive cycle of ring doves. The main points are: (1) Changes in behavior during the reproductive cycle (indicated diagonally in the chart) are influenced by external stimuli and hormones. (2) The time course of behavioral changes is in close relation to that of hormonal changes. (3) External stimuli (social and environmental), acting through the hypothalamus-pituitarygonadal (HPG) system, cause hormonal changes which (a) influence behavior and thereby the pattern of external stimuli, (b) stimulate reproductive organs and

124

MEI-FANG CHENG

7-0

14-15

OUIATW4 OF T I E CYCLE H MY5

I

t

-42-46 Mls 1 TOTAL UR*TYM ff REP(*XXICTIVE CTW-E ff RNxi WVE

FIG.8. Interrelationship of hormones, external stimuli, and transitions in behavior during breeding cycle of ring dove (Cheng and Rosenblatt, unpublished observations). Each block specifies the time span relative to the total duration of reproductive cycle. The and "-"indicate stimulatory and inhibitory effects, respectively. The shaded signs arrow indicates possible effects of behavior on the individuals' own endocrine system.

"+"

tracts, and (c) react back to the HPG system. (4) The activity of the HPG and the ability of external stimuli and hormones to induce behavioral changes show seasonal variation. Acknowledgments I would like to take this opportunity to express my gratitude to Drs. F. A. Beach, R. A. Hinde, J. S. Rosenblatt, and P. Teitelbaum for their generous and continuous supporl for my work throughout my career. It goes without saying that my greatest debt goes to Danny Lehrman, my most unforgettable teacher. Finally, my thanks to Dr. C. Beer who helped me pick the title, and to Dr. A. Mayer who was able to give me valuable editorial assistance. My thanks go to C. Banas. W. Cunningham, and N. Jachirn for their tireless efforts in drafting and typing. The criterion I used in the selection of research reported was its relevance to the topic I chose to discuss. 1 have therefore not covered many contributions by other colleagues, Drs. F. Nottebohm. M. E. Nottebohm. D. M. Vowles, and by many former students of the late Professor Lehrman. This is Contribution No. 301 from the Institute of Animal Behavior, Rutgers University. This work was supported by NlMH Grant No, MH-02271 and by Research Scientist Development Award No. KO2 MH-708Y7.

References Barfield, R . J . 1971a. Gonadotrophic hormone secretion in the female ring dove in response to visual and auditory stimulation by the male. J. Endocrinol. 49, 305-310. Barfield, R. 1. 1971b. Activation of sexual and aggressive behavior by androgen implants in the brain of the male ring dove. Endocrinobgv 89, 1470-1476.

RING DOVE RESEARCH

125

Bates, R. W.. Riddle, 0.. and Lahr, E. L. 1937. The mechanism of the antigonad action of prolactin. Am. J . Physiol. 119, 610414. Beach, F. A. 1974. Retrospect and prospect. In “Sex and Behavior” (F. A . Beach, ed.), pp. 535-569. Krieger, New York. Beach, F. A. 1976. Sexual attractivity, proceptivity and receptivity in female mammals. Horm. Behav. 7 , 105-138. Beer, C. 1963. Incubation and nest-building of Black-headed Gulls. 111: The pre-laying period. Behaviour 21, 13-77. Blaustein, J. D., and Wade, G. N. 1978. Progestin binding by brain and pituitary cell nuclei and female rat sexual behavior. Brain Res. 140, 360-367. Brown, J. L. 1965a. Vocalization evoked from the optic lobe of a songbird. Science 149, 10021003. Brown, J. L. 1965b. Loss of vocalization caused by lesions in the nucleus mesencephalicus lateralis of the redwinged Blackbirds. Am. Zool. 5 , 693. Brown-Grant, K. 1977. Physiological aspects of the steroid hormone-gonadotropin interrelationship. In ”Reproductive Physiology 11” ( R . 0. Greep, ed.), Vol. 13, pp. 57-83. Univesity Park Press, Baltimore, Maryland. Buntin, J. D. 1977a. Stimulus requirements for squab-induced crop sac growth and nest occupation in ring doves (Streptopelia risoria). J. Comp. Physiol. Psychol. 91, 17-28. Buntin, J . D. 1977b. Prolactin levels in breeding pigeons as measured by radioreceptor assay. East. Reg. Reprod. Conf., Storrs, Conn. (Absrr.) Buntin, 1. D., Cheng, M.-F. and Hansen, E. W. 1977. Effect of parental feeding activity on squab-induced crop sac growth in ring doves (Streptopelia risoria). Horm. Behav. 8, 297-309. Cheng. M.-F. 1973a. Effect of ovariectomy on the reproductive behavior of female ring doves (Streptopelia risoria). J. Comp. Physiol. Psychol. 83, 221 -233. Cheng, M.-F. 1973b. Effect of estrogen on behavior of ovariectomized ring doves (Streptopelia risoria). J . Comp. Physiol. Psychol. 83, 234-239. Cheng, M.-F. 1974. Ovarian development in the female ring dove in response to stimulation by intact and castrated male ring doves. J . Endocrinol. 63, 43-53. Cheng, M.-F. 1975. Induction of incubating behavior in male ring doves: A behavioural analysis. J . Reprod. Fertil. 42, 267-276. Cheng, M.-F. 1976. Interaction of lighting and other environmental variables on activity of hypothalamo-hypophyseal-gonadalsystem. Nature (London)263, 148-149. Cheng, M.-F. 1977a. Role of gonadotrophin releasing hormones in the reproductive behaviour of female ring doves. J . Endocrinol. 74, 3 7 4 5 . Cheng, M.-F. 1977b. Egg fertility and prolactin as determinants of reproductive recycling in doves. Horm. Behav. 9, 85-98. Cheng, M.-F. 1977~.Seasonal factors in the function of hypothalamo-hypophyseal-gonadalsystems. Int. Congr. Psvchoneuroendocrinol,, 8th, Emory Univ., Atlanta. Ga.

Cheng, M.-F., and Barbiere, C. 1978. Short day induced gonadal regression: A case for seasonal variation. J. Endocrinol. In press. Cheng. M.-F.. and Follett, B. 1976. Plasma luteinizing hormone during the breeding cycle of the female ring dove. Horm. Behav. 7 , 199-205. Cheng. M.-F., and Lehrman, D. S . 1975. Gonadal hormone specificity in the sexual behavior of ring doves. Psychoneuroendocrinology 1, 95-102. Cheng, M.-F., and Porter, M. 1976. Do ring dove copulations serve other functions? Anim. Behav. Soc. Northeosr Reg. Meet.. Am. Mus. Nut. Hist.. New York. (Abstr.)

Cheng, M.-F., and Silver, R . 1975. Estrogen-progesterone regulation of nest-building and incubation behavior in ovariectomized ring doves. J . Comp. Physiol. Psychol. 88, 256-263. Cohen. J . , and Cheng. M.-F. 1977. Effect of midbrain lesions on female nest-coo behavior during the breeding cycle. Soc. Neurosc., Annu. Meet.. 7rh, Anaheim, Calf. (Abstr.)

126

MEI-FANG CHENG

Cooper, R . , and Erickson. C. 1976. Effects of septa1 lesions on the courtship behavior of male ring doves. Horm. Behuv. 7, 441450. Cox, C.. and Silver, R. 1977. Feral ring doves in Florida. Itit. Ethol. Soc. Meet., /5lh, Bielefeld. Cerrnuny. (Abstr.) Davies. S . J. J . F. 1974. Studies of the three coo-calls of the male Barbary dove. Elnu 74, 18-26. Erickson, C. J . 1970. Induction of ovarian activity in female ring doves by androgen treatnient of castrated males. J. Cump. fhvsiol. Psychul. 71, 210-215. Erickson, C . J . 1973. Mate familiarity and the reproductive behavior of ringed turtle doves. Auk 90, 780-795. Erickson. C. J.. and Hutchison. J . B. 1977. Induction of nest material collecting in male Barbary doves by intracerebral androgen. J. Roprod. Fo.t. 50, 9-16. Erickson. C . J.. and Lehrman, D. S. 1964. Effect of castration of malc ring doves upon ovarian activity of females. J. Comp. Physiol. Psycho/. 58, 164-166. Erickson. C . J . , and Martinez-Vargas, M. C . 1975. The hormonal basis of cooperative nest-building. In “Neural and Endocrine Aspects of Behaviour in Birds” (P. Wright, P. G . Caryl. and D. M. Vowles. eds.). pp. 92-109. Am. Elsevier, New York. Erickson. C . J . . and Moms, R. L. 1972. Effects of mate familiarity on the courtship and reproductive success of the ring dove (Streptopelia risoris). Anim. Behav. 20, 341 -344. Erickson, C . J . . and Zenone. P. G. 1976. Courtship differences in male ring doves: Avoidance of cuckoldry? Science 192, 1856-18.57. Etches. R. 1.. and Cunningham, J . F. J . 1976. The interrelationship between progesterone and LH during rhe ovulation cycle of the hen (Gallus domesticus). J. Endocrinol. 71, 5 1-58, Feder. H. H., Storey. A., Goodwin. D., Reboulleau, C . , and Silver, R. 1977. Testosterone and “5a -dihydrotestosterone” levels in peripheral plasma of male and female ring doves (Streptopelia risoria) during the reproductive cycle. Biol. Reprod. 16, 666-677. Follett. B. K.. Scanes, C. G., and Cunningham, F. J . 1972. A radioimmunoassay for avian luteinizing hormone. J. Endocrind. 52, 359-378. Friedman, M . B. 1977. Interactions between visual and vocal courtship stimuli in the neuroendocrine response of female doves. J. Cotnp. Physiol. Psychul. 91, 1408-1416. Furr. B. J . A., Bonney, R. C.. England, R. J . , and Cunningham, F. J . 1973. Luteinizing homione and progesterone in peripheral blood during the ovu latory cycle of the hen, Gallus domesticus. J. Endocrinol. 57, 159-169. Gerlach, J . L.. Heinrich, W., and Lehrman. D. S . 1975. Quantitative observations of the diurnal rhythm of courting, incubation and brooding behavior i n the ring dove. Verh. Drsc.h. Zoo/. Ges. 74, 351-357. Gibson, M. J . . and Cheng. M.-F. 1977. Posterior medial hypothalamic mediation of female counship behavior in the ring dove. Soc. Neurosc Annu. Met[., 7th. Anuheirn. C‘u/if,, p. 344. (Abstr.) Goodwin. D. 1967. “Pigeons and Doves of the World.” Br. Mus. Nat. Hist.. London. Hanebrink, E. L.. Hollander, W. F. and Skinner. J . L. 1977. “Pigeons and Doves in Rcscarch.” Am. Pigeon Fanciers Counc.. Madison. Wi\consin. Hansen. E. W. 1966. Squab-induced crop growth in ring dove foster parents. J. Cotnp. Physiol. Psycho/. 62, 120-122. . Hansen, E. W. 1971. Responsiveness of ring dove foster parents t o squabs. J. C ~ n i p Physiol. Psycho/. 77, 382-387. Hansen, E. W. 1973. A further analysis of the responsiveness of experienced and inexperienced ring dove foster parents to squabs. Drv. fsyc.hobio/. 6, 557-565. Hams, G. W. 1955. “Neural Control of Pituitary Gland.” Latimer. Trend. Plymouth. England. Heinrich. W. 1975. Quantitativ Untersuchungen iiber das Balzen urid Briiten bei unerfahrcnen und erfahrenen Lachtauben (Streptopelia risoria). Habilitationschrift, Math.. Naturwiss. Fak. Univcrsitlt, Giittingcn.

RING DOVE RESEARCH

127

Hinde, R. A. 1958. The nest-building behaviour of domesticated canaries. Proc. 2001.Soc. London 131, 1 4 8 . Hinde, R. A. 1965. Interaction of internal and external factors in integration of canary reproduction. In "Sex and Behavior" (F. A . Beach, ed.). pp. 381-415. Wiley, New York. Hinde, R. A., and Steel, E. 1976. The effect of male song on an estrogen-dependent behavior pattern in the female canary (Serinus canarius). Horm. Behav. 7 , 293-304. Hinde, R. A , , and Steel, E. 1978. The influence of day length and male vocalizations on the estrogen-dependent behavior of female canaries and budgerigars, with discussion of data from other species. Adv. Strrcly Behtrv. 8. 40-68. Hutchison, J. B. 1967. Initiation of courtship by hypothalamic implants of testosterone propionate in castrated doves. Nature (LondonJ 216, 591 -592. Hutchison, J. B. 1970a. Differential effects of testosterone and oestradiol on male courtship in Barbary doves. Anim. Behav. 18, 41-52. Hutchison, J . B. 1970b. Influence of gonadal hormones on the hypothalamic integration of courtship behavior in the Barbary doves. J . Reprod. Fertil., Suppl. 21, 1541. Hutchison, J . B. 1974. Differential hypothalamic sensitization to androgen in the activation of reproductive behavior. In "The Neurosciences" (0.Schmitt, and F. G. Worden, eds.), Vol. 3, pp. 593-597. MIT Press, Cambridge, Massachusetts. Hutchison, J. B. 1976. Hypothalamic mechanisms of sexual behavior, with special reference to birds. Adv. Study Behav. 6, 159-200. Hutchison. J . B.. and Lovari, S. 1976. Effects of male aggressiveness on behavioural transition in the reproductive cycle of the Barbary dove. Behaviour 96, 296-318. Karten. H. J . 1966. The organization of the ascending auditory pathway in the pigeon. Brain Res. 6, 409427. Karten, H. J . , and Hodos, W. 1967. "A Stereotaxic Atlas of the Brain of the Pigeon (Columba tivia)," Johns Hopkins Press, Baltimore, Maryland. Komisaruk, B. R . 1967. Effects of local brain implants of progesterone on reproductive behavior in ring doves. J . Comp. Physiol. Psycho/. 64, 219-224. Korenbrat, C. C., Schornberg, D. W., and Erickson, C. J . 1974. Radioimniunoassay of plasma estradiol during the breeding cycle of ring doves. Endocrinology 94, 1126-1 132. Leavitt, W. W.. Toft. D. 0.. Strott, C. A , , and O'Malley, B. W. 1974. A specific progesterone receptor in the hamster uterus: physiologic properties and regulation during the estrous cycle. Endocrinologv 94, 104 I - 1053. Lehrnian, D. S. 1955. The physiological basis of parental feeding behavior in the ring dove. (Streptopelia risoria). Behuviour 7, 241 -286. Lehrman, D. S. 1958a. Induction of broodiness by participation in courtship and nest-building in the ring dove. J . Comp. Phv.\iol. Pswhol. 51, 32-36. Lehrman, D. S. 1958b. Effect of female sex hormones on incubation behavinr in the ring dove. J . Comp. Physiol. Psychol. 51, 142-145. Lehrman. D. S. 1961, Hormonal regulation of parental behavior in birds and infrahuman mammals. In "Sex and Internal Secretions" (W. C. Young, ed.). pp. 1268-1382. Williams & Wilkins, Baltimore, Maryland. Lchrnian, D. S. 1964. The reproductive behavior of ring doves. Sc. Am. 211, 48-54 Lehrinan, D. S. 1965. Interaction between internal and external environments in the regulation of the reproductive cycle of the ring dove. IN "Sex and Behavior" (F. A. Beach, ed.), pp. 355-380. Wiley. New York. Lehrman. D. S . . and Brody, P. 1961. Does prolactin induce incubation behavior in the ring dove'? J . Entloc.rinol. 22, 269. Lehrnian, D. S .. and Brody. P. 1964. Effect of prolactin on establishing incubation behavior in the ring dove. J . Comp. Phy,siol. P s y h o l . 57. 161-165.

128

MEI-FANG CHENG

Lehrman, D. S . , and Wortis, R. 1967. Breeding experience and breeding efficiency in the ring dove. Anim. Behav. 15, 223-228. Lehrman, D. S . , Brody, P. N., and Wortis, R. 1961a. The presence of the mate and nesting material as stimuli for the development of incubation behavior and for gonadotropin secretion in the ring dove. Endocrinology 68, 507-5 16. Lehrman, D. S., Wortis, R. P.. and Brody, P. 1961b. Gonadotropin secretion in response to external stimuli of varying duration in the ring dove (Streptopelia risoria). Proc. Soc. Exp. Biol. Med. 95, 373-375. Liley, N. R. 1976a. Physiological maturation and reproductive behavior of female doves held under long and short photoperiods. Can. J. Zool. 54, 343-354. Liley, R. N. 1976b. The role of estrogen and progesterone in the regulation of reproductive behavior in female ring doves under long vs. short photoperiods. Can. J . Zool. 54, 355-360. Lovari, S . , and Hutchison, J . B. 1975. Behavioural transition in the reproductive cycle of Barbary doves (Streptopelia risoria L.). Behaviour 63, 126-150. Mairy, F. 1977. Studies of the three coo-calls of the male Barbary dove. Inr. Erhol. SOC.Meer.. 15rh. Bielefeld, Germany (Absrr.). March, G . L., and McKeown, B. S . 1973. Serum and pituitary prolactin changes in the band-tailed pigeon (Columba fasciata) in relation to the reproductive cycle. Can. J. Physiol. Pharmacol. 51, 583-589. Martinez-Vargas, M. C. Stumpf, W. E.. and Sar, M. 1975. Estrogen localization in the dove brain: Phylogenetic considerations and implications for nomenclature. In “Anatomical Neuroendocrinology” (W. E. Stumpf, and P. P. Grant, eds.), pp. 166-175. Karger, Basel. Martinez-Vargas, M. C., and Erickson, C. J. 1973. Social and hormonal determinants of nestbuilding in the ring doves. Behaviour 45, 12-37. Michel, G. F. 1977. Experience and progesterone in ring dove incubation. Anim. Behav. 25, 28 I -285. Miller, W. I . , and Miller, L. S. 1958. Synopsis of behavior traits of the ring neck dove. J. h i m . Behav. 6, 3-8. Nottebohm. F., Stokes, T. N., and Leonard, C. M. 1976. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165, 457-486. Patel. M. D. 1933. The physiology of the formation of pigeon’s milk. Physiol. 2001.9, 129-152. Phillips, R. E., and Peck, F. W. 1975. Brain organization and neuro-muscular control of vocalizations in birds. In “Neural and Endocrine Aspects of Behaviour in Birds” (P. Wright, P. G. Caryl, and D. M. Vowles, eds.). pp. 243-274. Am. Elsevier, New York. Robbins, C. S., Bruun, B., and Zinn, H. S . 1966. “Birds of North America.” Golden Press, New York. Rothchild, I., and Fraps, R. 1949. The induction of ovulating hormone release from the pituitary of the domestic hen by means of progesterone. Endocrinology 44, 141-149. Scanes, C. G . . Sharp, P. J., and Chadwick, A. 1977. Changes in plasma prolactin concentration during ovulatory cycle of the chicken. J. Endocrinol. 72, 401402. Silver, R., and Buntin, J . D. 1973. Role of adrenal hormones in incubation behavior of male ring doves (Streptopelia risoria). J. Comp Physiol. Psychol. 84, 453463. Silver, R., and Feder, H. H. 1973. Reproductive cycle of the male ring dove. 11. Role of gonadal hormones in incubation behavior. J. Comp. Physiol. Psychol. 84, 4 6 4 4 7 I . Silver, R.. Reboulleau, C., Lehrman, D. S . , and Feder, H. H. 1974. Radioimmunoassay of plasma progesterone during the reproductive cycle of male and female ring doves (Streptopelia risoria). Endocrinology 94, 1547-1554. Steel, E . , and Hinde. R. A. 1972. Influence of photoperiod on oestrogenic induction of nest-building in canaries. J. Endocrinol. 55, 265-278.

RING DOVE RESEARCH

129

Stern, J . M. 1972. Androgen accumulation in hypothalamus and anterior pituitary of male ring doves: Influence of steroid hormones. Cen. Comp. Endocrinol. 18, 4 3 9 4 9 . Stem. J. M. 1974. Estrogen facilitation of progesterone-induced incubation behavior in castrated ring doves. J. Comp. Physiol. Psychol. 81, 332-337. Stern, J. M., and Lehrman, D. S. 1969. Role of testosterone in progesterone-induced incubation behaviour in male ring doves. J. Endocrinol. 44, 13-22. White, S . J. 1975a. Effects of stimuli emanating from the nest on the reproductive cycle in the ring dove. I: Prelaying behaviors. Anim. Behav. 23, 854-868. White, S. J . 1975b. Effects of stimuli amanating from the nest on the reproductive cycle in the ring dove. 11: Building during the prelaying period. h i m . Behav. 23, 869-882. White, S . J . 1975~.Effects of stimuli emanating from the nest on the reproductive cycle in the ring dove. 111: Building in the post-laying period and effects on the success of the cycle. Anim. Behav. 23, 883-888. Wilson, C. S., and Sharp, P. J. 1976. The effect of progesterone on oviposition and ovulation in the domestic fowl. Br. Poult. Sci. 17, 163-173. Wortis, R. P. 1969. The transition from dependent to independent feeding in the young ring dove. Anim. Behav. Monogr. 2 , Part I, 3-54. Zigmond, R. E., Stem, J. M., and McEwen. B. S. 1972. Retention of radioactivity in cell nuclei in the hypothalamus of the ring dove after injection of H-testosterone. Gen. Comp. Endocrinol. IS, 450453.

This Page Intentionally Left Blank

A D V A N C t S I N THE STUDY OF B t H A V I O R . VOL Y

Sexual Selection and Its Component Parts, Somatic and Genital Selection, as Illustrated by Man and the Great Apes* R. V. SHORT MRC UNIT OF REPRODUCTIVE BIOLOGY EDINBURGH, SCOTLAND

1. The Concept of Sexual Selection. . . . . . . . , . , . . .. ..., .. . ....... 11. Reproduction in the Gorilla . . . . . . . . . . . . . . , . . . . . . . . . . . . . . .. . . . . . . . . A. Behavior . . . . . . . . . . . . . . . .. . . . . . . . ,

B. Anatomy o e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . C . Anatomy o ......... D. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. .. .... 111. Reproduction in the Orangutan . . . . . . . . . . . . . .. .. .. . . A. Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . ......... B. Anatomy of the Male . . . . . ......... C. Anatomy of the Female . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . D. S u m m a r y . . . . . _ _. . ......... IV. Reproduction in the Chimpanzee.. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .

................. . ...... B. Anatomy of the Male . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C . Anatomy of the Female . . . . . . . . . . . . . . .. . . . . . . . . V . Reproduction in Man A. Behavior . . . . . . . . . . . . . . , . , , . , . , . , . , . B. Anatomy of the Male . . . . . . . . . . . . . . . . . C. Anatomy of the Female . . . . . . . . . . . . . . . D. S u m m a r y . . . . . . . . VI. General Conclusions . . . , . . . . . . . . . . . , , . . . . References

I.

THEC O N C E I T

. . . . . . . . . . . . . . .. . . . . . . . . . . .... ... ........... . ....... . . . . .. . . . . ,.............. . . .... ... , . . . . . . . . . . . . . .. . . . . . . . . , . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .

131 135 135 136 138 139 139 139 1 40 142 142 143 143 144 145 146 147 147

149 151 151 152 155

OF SEXUAL SELECTION

In The Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (1859), Darwin saw evolution as a dynamic process made possible by natural selection and the survival of the fittest. *This is an abbreviated and amended version of an article entitled "Sexual Selection and the Descent of Man" first published in the Proceedings of the Canberra Symposium on Reproduction and Evolution, Australian Academy of Science, 1977. 131

Copyright 1'47'4 by Academic Press. Inc. All nghh 01 repriluutiim in any firm reserved ISBN 0- 124W5OY-5

I32

R.

V. SHORT

But unless the survivors were fertile and capable of contributing breeding stock to the next generation, the successful genotype would not be propagated and the species would not survive and evolve. Darwin came to realize that reproductive success must be the key to the origin of species. Darwin then went on to consider in particular the problem of human evolution. It was the existence of so many distinct races of the one species, Man, that led him to the concept of sexual selection, an idea that he developed at length in The Descent of Man, and Selection in Relation to Sex (1871). He defined sexual selection as “the success of certain individuals over others of the same sex, in relation to the propagation of the species,” whereas natural selection operated on “both sexes, at all ages, in relation to the general conditions of life.” He also appreciated that sexual selection could operate either within one sex, as in the case of intermale competition for access to females, or between the two sexes, as in the case where the male tries to make himself more attractive to females than his other male rivals. Darwin also realized that in polygynous species, in which the males mate with more than one female, the competition between males will be especially pronounced, leading to an exaggerated development of those secondary sexual characters used in intermale aggressive encounters. Under certain circumstances, these characters might be developed to the point where they acted counter to natural selection, instead of in concert with it. Darwin’s ideas on intra- and intersexual selection were developed further by Fisher (1930). Fisher was intrigued by the genetic control of sexual dimorphism. Although an obvious solution might seem to be to locate all the genes for male secondary sexual characteristics on the Y chromosome, Fisher was quick to see that Nature had adopted a far more subtle strategy. The Y chromosome has been used by all mammals just to determine the presence of a testis, and the whole of sexual differentiation has been delegated to testicular hormones. Thus the genes for sexually dimorphic characters only have to be sex limited, not sex linked, thereby opening up the entire autosomal complement of chromosomes for exploitation in sexual dimorphism. No wonder we see such spectacular and diverse forms of male secondary sexual characteristics in different species and a Y chromosome that appears to be almost devoid of genetic information apart from the testis-determining gene or genes. Just as Fisher championed and expanded Darwin’s view of sexual selection, so Julian Huxley (1938) was able to use his wide practical experience as an.ornithologist and field naturalist to clothe the theories of Darwin and Fisher with practical examples. He realized that all aspects of the male and female reproductive tract were likely to be involved in intersexual selection, from the gametes themselves to the gonads, the male and female copulatory organs, ducts, and accessory glands, any structures facilitating the discovery or recognition of one sex by the other, and any behavioral display that stimulated reproductive activity.

SEXUAL

SELECTION: SOMATIC

AND GENITAL

133

Huxley commented on Darwin’s modesty in not referring to the copulatory organs themselves, and introduced the term “psychological penis” to emphasize the dual role of the male organ in intersexual display and in copulation. He also re-emphasized the point made by Darwin and Fisher that polygynous mating systems would maximize sexual dimorphisms, whereas monogamous systems would minimize them. Trivers (1972) pointed out that an animal’s reproductive strategy in terms of the type of mating system it adopts is dictated by the relative energy investment of the two parents in rearing their young. Thus, in birds, in which in the absence of lactation both sexes can play an equal role in feeding the young, monogamous mating systems are generally desirable, so that sexual dimorphisms in body size are unlikely to develop. However the sexes may still be distinguishable by plumage characteristicsdeveloped through inter- as opposed to intrasexual selection. It is of interest that in birds, where the male is the homogametic sex (XX), the “neuter” state appears to be the gaudy plumage of the male, on which femaleness is superimposed by ovarian estrogens. In spectacularly dimorphic species like the pheasants, an ovariectomized female will develop the male’s brilliant colors, which are normally suppressed in the female by her estrogens (Vevers, 1977); her dowdy appearance may also provide better camouflage when she is sitting on the nest. The testosterone secreted by the male’s XX testes is nevertheless still responsible for his aggressive and sexual behavior and for the development of such male secondary sexual characteristics as the comb and spurs. In many herbivorous mammals, the male plays no part in the care of the young. This favors a new reproductive strategy4opulation with as many females as possible. Thus, polygyny, intense male intrasexual selection, and pronounced sex dimorphisms in body size and development of weapons are the result . If these theories about the correlation between sexual dimorphism and mating system are put to the test in birds (Selander, 1972) or primates (Crook, 1972), they generally appear to hold true. However, Rails (1976) has pointed out a number of important exceptions where the female is appreciably bigger than the male; such exceptions do not appear to be examples of polyandrous or matriarchal social systems where the female is dominant to the male. In birds of prey and some carnivores such as the spotted hyena (Crocutu crocufa), the female may have had to become larger than the male in order to defend her offspring from his predatory attacks. It is therefore fascinating to discover that the female spotted hyena has testosterone levels that are at least as high as the male’s, if not higher (Racey and Skinner, 1978). In some bats, whales, and seals, the smaller size of the male might be a positive advantage affording greater speed and maneuverability in inter-male combat, or it may be advantageous for the female to be

134

R. V. SHORT

large if she has to give birth to a particularly large infant, as in whales, or fly while carrying one, as in bats, or to compete with the male for scarce food resources. These ideas about sexual selection are summarized diagrammatically in Fig. 1 . It is important, however, to realize that there may be considerable overlap between inter- and intrasexual selection; the large body size of the male may at one and the same time intimidate his rivals, and render him more attractive to females. As far as intersexual selection is concerned, it may be extremely difficult to determine which particular bodily characteristics of the female render her attractive to the male, and which of the male’s characteristics she finds most appealing. It is hard enough to give definitive answers to these questions even for our own species. In some polygynous mating systems where the number of females held by a male may be determined more by the area of female territory that can be defended against other males, rather than by the attributes of the individual females within it, there may have been little selection pressure for the female to become attractive to the male, and almost none for the male to become

MONOGAMY

IWTIIASUWL

XLLWL

POLYGYNY INlRlSfXUAl

WCTW

I

FIG. 1 , Effects of sexual selection in a monogamous and a polygynous mating syhtem. In the latter, competition betwccn males is enhanced. leading to bexual dimorphism in body size, and maybe the development of offensive weapons. lntrasexual selection may also lead to the development of adornments aimed at attracting the opposite sex.

SEXUAL

SELECTION: SOMATIC

A N D GENITAL

135

attractive to the female, since she would never be given an opportunity to exercise any choice in the matter of mate selection. The determination as to whether a particular character has evolved as a result of inter- or intrasexual selection is always bound to be rather arbitrary and presupposes a detailed understanding of the animal’s courtship and mating behavior. The subdivision of sexual selection into these two component parts may be an interesting intellectual exercise, but the anthropomorphic nature of the distinction places severe limitations on its scientific validity. A simpler and more objective alternative would be to divide sexual selection into two components: somatic selection, the evolution of general body shape, size, color, etc., and genital selection, the evolution of the male and female reproductive tracts. Such a distinction would be in accord with the view of soma as the vehicle for the transmission of sex from generation to generation. In what follows the extent of the known somatic and genital differences between Man and his closest living relatives, the Gorilla, Orangutan, and Chimpanzee is discussed. These might be accounted for by differences in reproductive behavior, and hence it may be possible to gain some new insights about the probable role of sex in human social evolution.

11.

A.

REPRODUCTION I N THE GORILLA

BEHAVIOR

Studies of the Mountain Gorilla (Gorilla gorilla beringei) in its natural habitat in Central Africa by Schaller (1963, 1965), Fossey (1974), and Harcourt and Stewart (1977, 1978) are enabling us to build up a detailed understanding of its behavior. Schaller has described gorillas as rather amiable vegetarians, primarily terrestrial and quadrupedal. They live in small groups of from 2-30 individuals; group composition changes with time, although the groups may remain stable for months on end. Every group contains at least one fully mature silverbacked male and a female. A marked dominance hierarchy exists among the males, dominance rank being related to body size; silverbacks are dominant to the younger blackbacked males. There is no stable hierarchy among the females, although mothers with young infants tend to be the more dominant. Schaller found that dominance was frequently expressed (0.23 times per hour of observation), although with a minimum of actions, so that overt strife between males was not observed in 466 hours of direct observation. However, fierce fights do occasionally occur between rival males, leading to severe wounding or even death of one of the antagonists (Harcourt and Stewart, 1977). The dominant male remains with the group the whole time, and leads it in all activities; the group is therefore cohesive around him. Several different groups share a common home range, and

136

R.

V.

SHORT

the abundance of vegetation means that competition over food is not a cause of strife. Although copulation is confined to the daytime, Schaller only saw two copulation attempts during all his observations. Harcourt and Stewart carried out over 2000 hours of observation during a 244-year period on two groups of animals, each containing a dominant silverbacked male, a young adult blackbacked male, 3 4 adult females, and 5-7 immature young, and they only witnessed 98 copulations. The average duration of copulation was about one minute. Only the silverback mated with the parous females, but blackbacks occasionally mated with pubescent females. Estrus normally lasted 1-2 days and this was the only time when copulation occurred. There was no male courtship display; the female initiated the copulations, which were all dorsoventral, with the male sitting upright holding the female round her waist, while she sat in his lap, leaning slightly forward. Copulations occurred at a median rate of 0.4 times per hour on the days when the female was in heat. In captivity, gorillas have been seen to copulate ventroventrally (Nadler, i975a, 1976). There are obviously relatively few occasions during the year when one of the 3-6 females in a male gorilla’s troop would be in estrus. The first signs of puberty (perineal tumescence) begin at about 7 years of age; copulation with the silverback starts at about the age of 7% and then there is about a year of adolescent sterility, with cycles once a month before the female conceives. The mean cycle length for eight adult lowland gorillas in captivity was 3 1.1-32.5 days, and the mean duration of maximum labial tumescence was 1.8 days (Nadler, 1975b); however, it should be noted that this tumescence is not particularly conspicuous, in contrast to the situation in the chimpanzee. Some females may continue to show one or two estrous cycles during pregnancy [duration of gestation approximately 246-256 days (Nadler, 197%; Martin, 1976)l. Since the birth interval from Schaller’s observations is 3444% years, this suggests that, following parturition, there is a period of 2%-3% years of lactational anestrus before the female will come back into heat again. She may have 2 or 3 estrous cycles before embarking on a further 3 4 years of sexual quiescence. In view of the group size and age structure, the male could easily go for up to a year without having an opportunity to copulate with a single estrous female.

B. ANATOMY OF THE MALE 1 . Body Size

Accurate measurements of the body weights of wild gorillas are understandably lacking, and data from captive animals may be deceptive because they are often obese. Schaller estimated the weight of wild silverbacked males of 10 years or more to be 136-204 kg, blackbacked males of 6-10 years 68-1 13 kg,

SEXUAL

SELECTION: SOMATIC

A N D GENITAL

137

and adult females of 6 years or more also 68-1 13 kg. My own observations on the gorillas in Bristol Zoo showed that the 13-year-old silverbacked male “Samson” weighed 175 kg and the 13-year-old parous female “Delilah” weighed 77 kg. Thus the adult male is at least twice the size of the female, and facially distinct from her by the massive development of a saggital and nuchal crest. This size dimorphism begins at puberty, and since body size is clearly related to dominance and access to females, it is reasonable to assume that it is a consequence of sexual selection. 2 . The Testes

In spite of being by far the largest of all the Great Apes, the gorilla has the smallest testes. They are concealed from view in a barely perceptible scrotum, which consists of a postpenial bulge of the hair-covered integument. Wislocki (1942) commented that “the genitalia were so much concealed that it was only upon palpation that all doubt regarding the sex of the animals was removed.” He was able to examine a formalin-fixed pair of testes, weighing 36 g, from a mountain gorilla weighing approximately 204 kg, which was shot in the Eastern Belgian Congo; thus the testesbody weight ratio in this animal was 0.018%. Hall-Craggs (1962) examined one testis from a 134-kg animal found dead from acute enteritis in South Uganda. The testis plus epididymis weighed 20.6 grams, and the testis alone 1 I .6 grams, to give a combined testesbody weight ratio of 0.017%. These are the lowest known values for any primate (Schultz, 1938a). Both Wislocki and Hall-Craggs noted that histologically the seminiferous tubules were small in diameter, few in number, and widely separated by masses of interstiti.al tissue, although there was active spermatogenesis present. This is interesting in relation to my own observations on Samson at Bristol Zoo, a silverback of proven fertility whose testes measured 3.8 X 1.8 cm and 3.5 X 2.2 cm on palpation, but whose peripheral plasma testosterone level was 644 ng/100 ml, which is within the normal human male range. Although there are numerous other reports of body weights and testes weights of adult male gorillas dying in zoos, they generally relate to animals that had become sterile as a result of degenerative testicular changes, with testicular shrinkage. Such data therefore cannot be used in calculating testesbody weight ratios. It seems reasonable to conclude that the gorilla has a low rate of sperm production and little sperm storage, which is in accord with the low copuiatory frequency. However, the endocrine activity of the testis, which is ultimately responsible for the marked sex dimorphism in body size, is probably comparable to that of man. 3.

The Penis

The gorilla’s penis has been described in detail by a number of authors. Some of the early accounts were inaccurate, due no doubt to the difficulties of working

138

R.

V.

SHORT

with fixed material. The most accurate descriptions are those of Osman Hill and Harrison Matthews (1949), and Raven (1950). Like the other Great Apes, the gorilla has an 0s penis; it appears to be absent at birth. In the adult male the penis is normally invisible, and the penile orifice which is flush with the body wall is barely discernible amongst the hair. On extrusion from the prepuce, the penis is seen as a short, black, conical structure, flattened laterally. We were able to produce a full erection in the male gorilla, Samson, at Bristol Zoo by anesthetizing him and inserting an electroejaculator into the rectum. The fully erect penis was only 3 cm long, and because of its black color it was still inconspicuous. The genitalia of the gorilla are so small and well camouflaged that they can have no part to play in attracting the female, and have not been developed to any degree under the influence of sexual selection. The structure of the penis also means that intromission would be much easier in a dorsoventral position.

4 . The Seminal Vesicles The seminal vesicles were 4.5 cm long and 0.5-0.8 cm in diameter in the adult male dissected by Raven, and 3 . 5 4 cm long and 0.4-1.1 cm in diameter in the 130-kg silverbacked male dissected by Hosokawa and Kamiya (1961). This suggests that the gorilla’s seminal vesicles are slightly smaller than man’s; thus testis size and vesicular size would appear to be correlated and presumably related to ejaculatory frequency.

5 . The Semen The mean volume of the ejaculate when obtained by electroejaculation was 0.3 ml (range 0.2-0.6 ml) and the sperm density in the liquid portion of the ejaculate was 171 X 1@/ml(Warner ef a l . , 1974). Gorilla semen, like that of man and the other Great Apes, contains large amounts of 19-hydroxyprostaglandin E, as the principle prostaglandin constituent (Kelly ef a l . , 1976). The spermatozoa are morphologically very similar to human spermatozoa and show a high degree of pleomorphism in the size of the sperm head (Martin et al., 1975; Seuanez er al. , 1977). In contrast to the single fluorescent Y chromosome that is visible in human sperm, gorilla sperm contain a number of fluorescent spots, apparently due to fluorescing autosomes (Seuanez et al.; 1976).

c.

ANATOMY OF THE FEMALE

There have been no obvious developments of female secondary sexual characteristics in the gorilla. No breast development occurs until toward the end of the first pregnancy. Perineal tumescence at the time of estrus, although present, is relatively inconspicuous (Noback, 1939; Nadler, 1975). This lack of accentuation of anatomical characteristics to make the female particularly attractive to the male at estrus may be a result of the polygynous structure of the community,

SEXUAL SELECTION: SOMATIC A N D GENITAL

139

where a dominant male is always in attendance, and where it is the female rather than the male who initiates copulation. The ovaries of the female gorilla are somewhat similar in size and shape to those of the human (Wislocki, 1932): the ovaries of a mature 64-kg female autopsied at Regent’s Park Zoo were 0.012% of the animal’s body weight, in other words, almost the same relative size as the testes of the male.

D.

SUMMARY

The gorilla demonstrates very clearly how two different types of sexual selection have been at work. Somatic selection has led to extreme development of body size in the male, who has become twice as big as the female, and by far the largest of all the primates. Body size is clearly a major factor in determining dominance rank within the group, and hence access to females. His great bulk is only possible because of his terrestrial existence. Genital selection : The low annual frequency of copulation, which is always initiated by the female, and takes place with the single dominant male of a stable troop, means that there has been no need to develop the male or female external genitalia for purposes of intersexual display. Furthermore, there has been no need to develop large sperm reserves in the male, so the testes and accessory organs have remained small, and the testes are, relatively, no larger than the ovaries. Sex does not seem to have been a cohesive force in the social life of the gorilla; it is a rare treat for these amiable vegetarians.

111.

A.

REPRODUCTION IN

THE ORANGUTAN

BEHAVIOR

Rodman (1973), MacKinnon (1974), and Rijksen (1975) have studied the behavior of wild Bomean and Sumatran orangutans (Pongo pygrnaeus) in their natural habitats and have shown that they are almost exclusively arboreal, feeding on fruits in the forest canopy. The relatively low density of fruiting trees in the tropical rain forests, coupled with the comparatively large body size of the orang, has meant that each individual requires a large home range to provide sufficient food resources. This has presumably resulted in a need to diminish sexual bonding, so that the adult male and female can live apart from one another for most of the time. In fact, MacKinnon never found two adult males together, or even two adult females. Instead, the adult male formed a temporary consortship with an adult female and her offspring. The adult males were markedly aggressive toward one another even when unaccompanied by females. Females

140

R. V. SHORT

tended to try and hide from males on first encounter, whereas the males often attempted to rape the females. MacKinnon thought that the normal birth interval was probably about 3 years, although in one area it appeared to be as long as 8 years. In zoos, female orangs seem to permit copulation at all stages of the menstrual cycle, although they are most receptive at mid-cycle; the mean duration of copulation is about 15 min (Nadler, 1975, 1977). The short duration of male-female consortships in the wild suggests that the female cannot be continuously sexually attractive to the male, and is therefore likely to have an estrous cycle. The duration of estrus is not known, but the mean length of the cycle is 30.5 days (Nadler, 1977), with a gestation period of 8-9 months (Asdell, 1965). Unfortunately, nothing is known about the copulatory frequency of individual males in the wild. It will obviously depend to a large extent on the number of females in the vicinity, their reproductive status, and the male’s success in warding off his rivals. B.

ANATOMY OF THE MALE

1 . Body Size

MacKinnon (1974) estimated that in the wild, adult males aged over 15 years weighed between 45-100 kg, although excessively obese zoo specimens have been known to exceed 200 kg. By contrast, he estimated that adult females of over 8 years weighed 35-50 kg. Eckhardt (1975) has reviewed the existing information on the body weights of wild Bornean and Sumatran orangs, and has shown that the males weigh 72.8 2 S.D. 17.7 kg (Bornean) or 66.0 k 17.3 kg (Sumatran), whereas the females weigh 37.4 2 4.1 kg (Bornean and Sumatran). At Bristol Zoo, a 14-year-old fully mature fertile male Sumatran orang named “Henry” weighed 114 kg, an 1 I-year-old subadult male Bornean orang named “Abang” weighed 58 kg, and an I 1-year-old postpubertal nulliparous female Bornean orang named “Dyang” weighed 45 kg. Thus the adult male is about twice the size of the adult female; he also differs from her in the massive development of lateral facial skin folds. This size dimorphism begins at puberty, and since body size is probably related to dominance and access to females, it is presumably a consequence of sexual selection. 2 . The Testes

The testes are concealed from view by a barely perceptible scrotum, which consists of a postpenial bulge of bare black skin, concealed by the long, ragged, red body hair. Schultz (1938a) showed that the average weight of the two testes in one captive and one wild adult orang was 35.3 g, giving a combined tes-

SEXUAL SELECTION: SOMATIC AND GENITAL

14 1

tes:body weight ratio of 0.048%.The testes of Henry at Bristol Zoo measured 5.3 x 3.0 cm and 5.0 X 2.9 cm on palpation, whereas those of Abang were 4.5 X 2.9 cm and 4.5 X 3.2 cm. The peripheral plasma testosterone level was 2367 ng/100 ml in Henry and 1606 ng/100 ml in Abang, which is somewhat above the normal human male range (see below). Subsequent studies on the blood of other adult male orangs have confirmed these high testosterone concentrations. It seems that the testes of the orang are about the same absolute size as those of the gorilla, although relative to body weight they are proportionately larger. Nevertheless, compared to other primates, the orang’s testes are still exceedingly small (Schultz, 1938a). The high plasma testosterone levels are presumably responsible for the sexual dimorphism, and could also account for the very aggressive nature of these animals. 3. The Penis

There are excellent descriptions of the anatomy of the orang’s penis by de Pousargues (1895) and by Pohl (1928), showing the location of the welldeveloped 0s penis. Studies on Henry and Abang at Bristol Zoo showed that the flaccid penis is invisible since it is concealed by the prepuce, and the penile orifice is flush with the body wall and only just discernible by its dark color amid all the surrounding long red hair. When pulled out, the penis is about 4 cm long and pink in color; this is also the length on erection. The flaccid penis of the orang, like that of the gorilla, is so inconspicuous that it is unlikely to be important in display; however, the erect penis of the orang is clearly visible at a distance. Its relatively short length probably accounts for the fact, as noted by MacKinnon, that intromission is achieved with difficulty in the wild. However, the animal’s great agility may make a number of copulatory positions possible, especially since copulation occurs while both animals are hanging from the branches. In captivity, copulation is usually ventroventral, but can also be dorsoventral (Nadler, 1977). 4 . The Seminal Vesicles

These appear to be larger than those of man or the gorilla. De Pousargues 10.0x2.5x 1.2cmforeach (1895)gives measurementsof8.0~2.5~1.2cmand gland in two adult orangs. When unraveled, the gland is seen as a single blindending convoluted tube with no side branches or diverticuli, quite unlike the branched duct of man.

5 . The Semen The mean volume of the ejaculate when obtained by electroejaculation was 1.1 ml (range 0.2-3.2 ml) and the mean sperm density in the liquid portion of the ejaculate was 61 x 106/ml (Warner et ul., 1974). The first illustrations of the

142

R. V. SHORT

spermatozoa of the orang were provided by Retzuis (1910). More recently, Martin et a l . (1975) and Seuanez et al. (1977) have carried out a detailed quantitative study which emphasizes the marked lack of pleiomorphism in sperm head size, clearly distinguishing the ejaculate from that of the human or gorilla. The spermatozoa also lack a fluorescent “F” body (Seuanez et al., 1976).

c.

ANATOMY OF

THE

FEMALE

There have been no obvious developments of female secondary sexual characteristics in the orang. No breast development occurs until toward the end of the first pregnancy. Perineal swelling appears to be absent, except during pregnancy (Schultz, 1938b). Thus there appear to be no anatomical features to make the female particularly attractive to the male. In a dense arboreal habitat, visual cues would be of little value to these solitary apes. One might predict that the male and the female respond to vocal and perhaps pheromonal cues to locate one another if the female comes into estrus. The ovaries are relatively small (Wislocki, 1932), and the ratio of the weight of both ovaries to body weight was 0.006 in two adult females autopsied at Regent’s Park Zoo.

D. SUMMARY I n the absence of more detailed information on the sexual behavior of orangs in the wild, it is difficult to ascribe a functional significance to all the structural changes that are observed. Somatic selection has led to extreme development of body size in the male, who has become twice as big as the female. However, the arboreal habitat must have placed certain restrictions on absolute body size. We do not know how the increased size of the male confers a reproductive advantage; the males are certainly very aggressive, but we do not know how frequently or by what means they compete for females. Genital selection: The restricted food supply has forced the orang, a treetop frugivore, to become a desocialized ape with diminished sexual bonding, so that the male and the female spend the greater part of their lives living apart from one another. The low density of animals and the long interbirth intervals presumably mean that the frequency of intercourse must be relatively low; hence the testes are small, although 8 times as big as the ovaries on a relative body weight basis. The poor visibility in the dense forest canopy and the need to keep the sexes apart has minimized the importance of visual cues, so that the external genitalia of the male and female are not conspicuous. Genital selection does not seem to have been of great importance in the evolution of the orang.

SEXUAL SELECTION: SOMATIC AND GENITAL

Iv. A.

143

REPRODUCTION IN THE CHIMPANZEE

BEHAVIOR

Van Lawick-Goodall ( 1968) has documented the behavior of free-living, wild chimpanzees (Pan troglodyres) in the Gombe Stream reserve in Tanzania. Quantitative information on their sexual activity was obtained by McGinnis (1973) and Tutin (1973, and this has given us much new insight into the social and sexual behavior of these animals. Chimpanzees live in large, multimale, multifemale social groups with an equal sex distribution and a total population of maybe 30 adults. Although there is competition between males in a variety of social situations, and group defense by the males of a communal temtory in which the females reside, there is little or no relationship between male rank or body size, and access to females; all males in the troop may take turns copulating with any estrous female, so the mating system is a promiscuous one. But in addition to these group matings, temporary consortships may be established between a male, not necessarily the most socially dominant, and an estrous female. There is a suggestion that conceptions are more likely to occur during such consortships than following group matings (Tutin, 1975). Estrus occurs in the middle of the 34-day menstrual cycle, and is accompanied by a most pronounced perineal tumescence. This is maximal for about 10 days, and copulations are concentrated in this period (McGinnis, 1973). Cycles of swelling precede the first menstruation by several months (Graham, 1970), and menarche is followed by 1-29'2 years of regular cycles, which are presumably anovulatory , before conception can occur. The duration of gestation is 227.5 days 2 S . D . 12.6. Two or three additional swelling cycles usually occur after conception. Thus each young female chimpanzee is in estrus for 10 days a month for 2 or 3 years before her first infant is born. Tutin (1975) found that the average birth interval in the wild was 5 years and 10 months. Following the 8-month pregnancy there were several years of lactational amenorrhea, and then a median number of 3.6 swelling cycles before the animal conceived again. Thus an individual female might have about 50 cycles of sexual swelling during her lifetime. Half would occur prior to the first pregnancy; only about seven would result in conception. Penile erection was sometimes seen as a component of feeding and greeting behavior, but not during aggressive encounters. Males almost always took the initiative in courtship, and on 50% of such occasions they merely approached the female with generalized piloerection and an erect penis, and no further behavioral display prior to copulation; on other occasions, the courtship display was much more elaborate (van Lawick-Goodall, 1968).

144

R. V. SHORT

Copulation normally occurs in the conventional mammalian dorsoventral position, and only during the daytime; the male and female never share a communal nest at night (van Lawick-Goodall, 1969). The frequency of copulations in chimpanzee communities is obviously high, in contrast to the situation in the gorilla and the orang. In 1200 hours of observation, mainly of estrous females, Tutin (1975) observed 1137 copulations, three-quarters of which were in noncompetitive situations. The average duration of copulation is only about 8 sec. It seems probable that the frequent availability of estrous females and the lack of sexual competition among males have been important factors in maintaining this cohesive multimale, multifemale group structure.

B. ANATOMY OF THE MALE 1 . Body Size

There is good information on the body weights of chimpanzees maintained in the Yerkes Primate Research Laboratories (Gavan, 1971). Between the ages of 12% and 13M, weights approach the asymptote; the average weight of 5 males was 46.6 2 S.D. 5.58 kg, whereas the average weight of 5 females was 41.6 2 2.82 kg. Thus, although the males are significantly heavier than the females, the difference is not nearly so pronounced as in the gorilla or the orang. Also in contrast to the gorilla or the orang, it is extremely difficult to tell the sex of a chimpanzee from facial characteristics. Somatic selection has presumably been of some importance, since increased body size presumably helps the males to defend their group territory. However, the promiscuous mating system, in which social rank is apparently of little significance in determining mating success, will tend to minimize individual selection for large body size. This may be the reason why the chimpanzee shows the least sexual dimorphism in body size of man and the Great Apes. 2.

The Testes

The scrota1 region of the male is rendered conspicuous by a hairless, unpigmented patch of skin. Although the scrotum is pendulous, this is not as pronounced as in man. Schultz (1938a) found that the average weight of the two testes in three captive chimpanzees of mean body weight 44.34 kg was 118.8 g, giving a testes:body weight ratio of 0.269%, which is high for primates. Wislocki (1942) noted that, on histological sectioning, most of the chimpanzee’s testis was composed of seminiferous tubules, with few Leydig cells, in marked contrast to the situation in the gorilla. Observations on a fertile 25-year-old male chimpanzee named ‘‘Buttons” at Bristol Zoo, weighing 66 kg, gave testis measurements on palpation of 8.0 x 5.5 cm and 8 . 0 ~ 6 . 5cm. Martin el al. (1977) have reported normal serum testos-

SEXUAL SELECTION: SOMATIC A N D GENITAL

145

terone levels of 4092S.E. 45 ng/l00 ml in adult 11-13-year-old chimpanzees. Thus the large testicular size of the chimpanzee is presumably due to the increased mass of the seminiferous tubules, reflecting the increased spermatogenic capacity required to cope with such high copulatory frequencies, whereas the relatively low testosterone levels suggest a paucity of Leydig cells. 3 . The Penis

This has been described in detail by Pohl (1928). As in the other Great Apes, the flaccid penis is normally invisible, since it is concealed by the prepuce, whose orifice is flush with the body wall. On extrusion from the prepuce, the penis is seen as long, thin, and filiform, tapering to a point; the small 0s penis is just palpable near the tip. The erect penis of Buttons was 8 cm in length. Its relatively large size and its pink color, seen against the bare white skin of the preputial area, make it very conspicuous. The penis of the chimpanzee may have increased in size because the erect organ is used in display in a variety of situations. However, it should also be remembered that without such a long narrow penis, it would be impossible for the male chimpanzee to achieve intromission, because of the tumescent region surrounding the vulva of the estrous female. 4 . The Seminal Vesicles

These are extremely large, relatively larger than those of the other Great Apes or man. Sonntag (1925) has provided a crude drawing and a descriptive account, but unfortunately no measurements are given. He states that, as in the orang, the gland is composed of a highly convoluted blind-ending tube without the diverticuli seen in man. Graham and Bradley (1972) showed that the dissected seminal vesicles of an 1 I-year-old male measured about 8 cm in length. 5 . The Semen

The mean volume of the ejaculate when obtained by electroejaculation was 1.1 ml (range 0.1-2.5 ml) and the mean sperm density in the liquid portion of the ejaculate was 548 x I@/ml (Warner et a l . , 1974). The spermatozoa of the chimpanzee are remarkably uniform in shape, with somewhat more elongated heads than in the orang (Martin et ul., 1975; Seuanez et ul., 1977). They also lack a fluorescent “F” body (Seuanez et ul., 1976); they are therefore quite unlike the spermatozoa of the gorilla or man. C.

ANATOMY OF T H E FEMALE

Although, as in the other Great Apes, there is no breast development in the female chimpanzee until toward the end of the first pregnancy, the female does advertise her sexual state to the male by means of the pronounced swelling of the

146

R. V. SHORT

labial and circumanal region. This is due to the accumulation of intercellular fluid, and the gross volume change in the tissues may amount to as much as 1400 ml during the course of the menstrual cycle (Graham, 1970). The swelling is maximally developed in the middle of the menstrual cycle, around the time of ovulation, and subsides rapidly thereafter. Cycles of swelling commence some time before menarche, and continue during the early months of pregnancy. Females will normally only permit copulation during the swelling phase of their cycle, when they are most attractive to the males. Since chimpanzee communities often indulge in “group sex,” there is presumably nothing to be lost by this flagrant visual advertisement of female sexual receptivity. The ovaries of the chimpanzee are smaller than the human (Wislocki, 1932). The ratio of the weight of both ovaries to body weight was 0.010% in one adult female autopsied at Regent’s Park Zoo.

D. SUMMARY The chimpanzee is a group-living, promiscuous, arboreal and terrestrial omnivore. Somatic selecrion has presumably led to some increase in body size in the male, since males indulge in group defense of a territory that contains the home ranges of numerous females. However, sex dimorphism in body size is not nearly as pronounced as in the gorilla or the orang, probably because social rank is not related to reproductive success in a mating system that is essentially promiscuous. Genital selection has been most pronounced in the chimpanzee, especially with respect to the male gonads. The promiscuous mating system will have led to intense gamete selection among different males, favoring the male who produces most spermatozoa and hence has the largest testes. Male gonadal development will have been further enhanced by the high copulatory frequency resulting from ( i ) the promiscuous mating system, ( i i ) the large number of females in the group, ( i i i ) the extended duration of estrus, and (iv) the large number of estrous cycles preceding the first pregnancy. Thus the testes of the male are 26 times as big as the ovaries of the female when expressed as a percentage of body weight. In contrast to gonadal development, which has been accentuated only in the male, the external genitalia have developed in both sexes. The male has developed a relatively large and conspicuous erect penis that is used in courtship displays, and it is the male that usually initiates copulation. The brevity of the act itself may have minimized intermale competition over the estrous female. The female flagrantly advertises the fact to all and sundry that she is in estrus by the pronounced tumescence of the perineal region. Thus, sex may serve as a major cohesive force in maintaining these large, multimale, multifemale social groups.

SEXUAL

SELECTION: SOMATIC

V. A.

AND GENITAL

147

REPRODUCTIONIN MAN

BEHAVIOR

The innumerable cultural variants of present-day human behavior are so diverse as to make it almost impossible to uncover a basic common plan. It is probably more meaningful to try to reconstruct the situation as it was prior to the agricultural and industrial revolutions and urbanization. The few surviving hunter-gatherer communities of the present day are probably the best guide to our prehistory. We can best describe ourselves as terrestrial, polygynous omnivores. In an anthropological review of 185 contemporary “primitive” human societies (i.e., not contaminated by Western culture), Ford and Beach (1952) found that only 16% were exclusively monogamous. In the remainder, polygynous marriages were permitted, although economic considerations and a shortage of women meant that monogamy was practiced in half of them. Serial monogamy may have been more the norm for our hunter-gatherer ancestors, representing a compromise between our polygynous natures and the need to maintain a parental pair bond for the benefit of the children (Short, 1976). The transmission of learning from generation to generation, coupled with our immaturity at birth and slow rate of postnatal development, have necessitated a prolonged period of contact between parents and offspring. A dependent infant, unable to fend for itself, placed severe constraints on the freedom of movement of its mother, who in turn became dependent on the father to do the hunting. Thus it was clearly important to reinforce the bonds that kept the parents together, and it seems probable that we exploited sexual behavior for this very purpose. We are apparently the only mammal in which the female has forsaken the periodic behavioral phenomenon of estrus, when she is instinctively attractive and receptive to the male, and exchanged it for a situation in which she is potentially attractive and receptive at all times from adolescence to old age. If women came into estrus, it would be socially disruptive for the community unless we adopted chimpanzee-style promiscuity. We seem to have exchanged estrus for love, thus bonding man and woman together. This was perhaps the critical factor that enabled us to be more successful than any other animal in transmitting acquired experience from generation to generation, thereby leapfrogging the blind, groping, trial-and-errorof Darwinian selection, in which only genes are transmitted. If prolonged mother-infant contact is so important, it follows that a prolonged interval between the birth of successive children was essential. In present-day hunter-gatherer communities the birth interval is about 4 years, made possible by the long duration of lactational amenorrhea. But even when a woman begins to

148

R. V. SHORT

ovulate again, the probability of conception in a given menstrual cycle never seems to exceed 28% (Short, 1976); maybe this low inherent fertility rate has been highly advantageous in helping to prolong the birth interval still further when lactation starts to fail. Although a woman’s reproductive life is ended by menopause at the age of 50, a phenomenon that has yet to be observed in any of the Great Apes which do not live that long, this still gives her about 35 fertile years. A relatively low fertility at each ovulation is therefore something that she can easily afford. One fact that seems to characterize the sexual behavior of all known human communities is that intercourse normally takes place in private. Thus it is very difficult to obtain accurate information on copulatory frequencies. A recent study in the United States gives coital frequencies of 11 times per 4 weeks when the couple are less than 19 years of age, declining to 5 times per 4 weeks in the mid-forties (Westoff, 1974). Copulatory frequencies in rural India appear to be considerably lower than this (Nag, 1972). It is interesting to note that if ejaculation occurs more frequently than once every 2-3 days, the semen volume and sperm density of the ejaculate will decline, suggesting that we are physiologically ill-adapted to high copulatory frequencies (Freund, 1963). In primitive communities, intercourse usually begins at puberty, although several years may elapse before the girl conceives, because the menstrual cycles following menarche tend to be anovulatory (Short, 1976). This makes it easier to understand why several primitive communities such as the Trobriand Islanders and the Australian Aboriginals failed to associate intercourse with conception. It was probably not until man began to domesticate animals, which came into estrus, copulated, and gave birth to young at predictable times thereafter, that the “facts of life” dawned on him (Abbie, 1969). The first act of intercourse is usually preceded by an extremely long period of courtship, lasting weeks, months, years, or even decades, depending upon the culture. Once pair bonding has become established, the period of precopulatory courtship is markedly reduced. The male usually initiates courtship and penile erection occurs in its later stages. Since this usually takes place in private, it is unlikely that the erect human penis is used for any display other than to the opposite partner. The widespread practice of circumcision, often performed in an initiation rite at puberty, may originally have been a means of enhancing the male’s sex appeal by permanently uncovering the most erotic part of the penis, namely the glans (Ucko, 1969). Penis sheaths were widely used by primitive tribes in South America, Africa, and Oceania, and many people have mistakenly interpreted these as some form of erotic phallic display. However, Ucko’s detailed analysis of the practice suggests that the sheath was worn out of modesty and decorum by tribes who practiced circumcision in order to conceal the glans from view. Since the wearing of the sheath often made erection either impossible or extremely

-

SEXUAL

SELECTION: SOMATIC

AND GENITAL

149

painful because of the way in which the penis was threaded through it, the penis sheath could have had little erotic significance. Ucko could find no support for the view advanced by Wickler (1966) that the penis sheath, or even the erect human penis itself, was used in aggressive displays among rival men. If the penis sheath was used to prevent erection and intercourse, the present-day condom may even be a logical development of it. The great size of the erect human penis, in marked contrast to that of all the Great Apes, makes one wonder what particular evolutionary forces have been at work. Undoubtedly, increased penile length has made a wide variety of copulatory positions not only possible, but enjoyable, and may have increased female satisfaction from intercourse by increasing the probability of female orgasm. We have ample testimony to the erotic significance of the erect human penis from the sculptures, paintings, and carvings of many civilizations (Webb, 1975). In English law, indecent exposure is an offense that can be committed only by a male against a female, and it relates exclusively to the exposure of the penis, regardless of whether it is flaccid or erect (Samuels, 1976). It is one of the commonest sexual offenses, and it seems significant that even in these days of sexual equality, proposed amendments to the law suggest that it should remain an exclusively male offense (Leigh, 1975).

B.

ANATOMY OF THE MALE

1 . Body Size

It is difficult to obtain representative body weights by age for a random cross section of any human population, and the most detailed information comes from the United States (Stoudt et al., 1960). At the age of 20, the average weight of men is 72 kg and 58 kg for women. This difference increases still further until the age of 30, when men weigh 77 kg and women 61 kg, a 20% difference. Men reach an asymptotic weight of 78 kg between the ages of 35 and 54 years, declining thereafter, while women continue to increase in weight to 68 kg at the age of 60. Thus, at any given age, men are appreciably heavier, and taller, than women. Although this weight difference between the sexes is not as great as in the gorilla or the orang, it is much more than in the chimpanzee. These differences are reflected by the fact that men have a greater proportion of muscle to body weight than women. Analysis of the male-female differential in Olympic track, swimming, and cycling events suggests that this is now about lo%, although the difference is in fact decreasing (Dyer, 1977). The differential would probably be much greater in feats of strength such as weight lifting, wrestling, and boxing. There are also marked facial and somatic differences between men and women, so that in our naked, unshaven, and unshorn state one could tell an

150

R. V. SHORT

individual’s sex at a glance from a considerable distance. All these facts added together would surely lead a stranger to our species to conclude that we were much more likely to be polygynous than monogamous.

2 . The Testes These are contained in a pendulous scrotum which is conspicuous. Schonfeld (1943) has presented a comprehensive review of human testicular growth and development, showing that the average weight of one testis in Caucasians after the age of 18 is 14.5-16.5 g, whereas in Orientals it appears to be only 12 g. Measurement of testis size by palpation, using a graded series of models for comparison, shows that the volume starts to increase from I ml at the age of 11, to reach an asymptote of 16 ml by the age of 20, with 80% of the observations lying between 11 and 21 ml. Schultz (1938a) found that the average weight of one testis in three Negroes aged 31-41 years was 25.1 g, giving a testes:body weight ratio of 0.079%, somewhat higher than the gorilla or orang, but considerably lower than the chimpanzee. These differences in relative testis size between man and the Great Apes would seem to be in accord with the different copulatory frequencies of the four species. The normal plasma testosterone level in adult men in our studies was 598 ? S.D. 219 ng1100 ml, which is lower than the orangutan, comparable to the gorilla, and slightly higher than the chimpanzee. 3 . The Penis This has been described anatomically by many authors, and Pohl (1 928) compared its structure to that of other primates and the Great Apes. The most distinctive features of the human penis are its large size and conspicuousness, even when flaccid, due to the fact that the shaft protrudes from the body wall. Unlike the Great Apes and most primates, man lacks an 0s penis. The penis begins to increase in size at puberty, achieving adult dimensions by about the age of 20. Since the size of the flaccid organ is influenced by factors such as ambient temperature, it has been found more reliable to measure the length of the flaccid organ when fully stretched, as this closely approximates to the length when erect. The mean length of the penis of adult men was found to be 13 cm, with 80% of the penises between 1 1 and 15 cm. It is interesting that penis size is in no way related to general body build (Schonfeld, 1943); the fact that all the growth occurs at puberty also suggests that size is unrelated to frequency of erection or intercourse. 4 . The Seminal Vesicles

These measure about 5 x 2 cm each, and when unraveled can be seen as a pair of ducts of about 10 cm in length, with a number of diverticuli (de Pousargues,

SEXUAL SELECTION: SOMATIC A N D GENITAL

151

1895). Thus they are larger than those of the gorilla but smaller than the orang and chimpanzee. These size differences are presumably related to the volume of the ejaculate, and also to the frequency of ejaculation. 5 . The Semen The normal volume of an ejaculate is 2.5-6.0 ml, with a sperm density of 60 x 10”ml (Eliasson, 1975). The spermatozoa exhibit a high degree of pleiomorphism in the size and shape of the head, and are grossly similar to those of the gorilla and quite unlike those of the orang or chimpanzee (Martin et al., 1975; Seuanez er a l . , 1977). It is possible to distinguish Y-bearing from X-bearing human spermatozoa by the presence of a fluorescent “F” body (Seuanez et al., 1976).

c.

ANATOMY OF THE FEMALE

One characteristic that sets woman apart from the Great Apes, or indeed from all other primates, is that full anatomical development of the breasts occurs at puberty, well in advance of the first pregnancy (Short, 1976). If the breasts are organs of sexual attraction, it makes sense for them to develop at this time. Changes in breast volume occur during the menstrual cycle (Milligan et al., 1975). somewhat akin to the changes in the perineal skin of the chimpanzee (Graham, 1970), although maximal breast volumes occur just prior to menstruation rather than around ovulation. Indeed, there has been a total disappearance of all external indications of ovulation, presumably as part of the process whereby the female’s attractiveness and receptivity to the male have become continuous rather than cyclical. Wehefritz ( 1 923) has provided extensive information on human ovarian weights throughout life, and mean ovarian weights expressed as a percentage of body weight during the reproductive years would appear to be about 0.01496, roughly comparable to the ratio found in all three Great Apes.

D. SUMMARY Sex has undoubtedly been extremely important in our evolution, since it has been the cohesive force maintaining the integrity of the pair bond, thereby allowing the children to receive the acquired experience of their ancestors by the written and spoken word. The disappearance of estrus and the development of a bond of love between the man and the woman have also allowed us to live in relative harmony in large, mixed-sex communities. Somatic selection at some stage in our evolution has accentuated the differences in body size and shape between the male and female, suggesting that in

152

R. V. SHORT

the past we must have adopted a polygynous (or serially monogamous) mating system. Perhaps the rising divorce rate in the Western world is just a reflection of this. Genital selection has resulted in the development of a relatively small testis, consistent with a low but sustained copulatory frequency. The penis has become conspicuous even when flaccid, and an extremely large organ when erect. It is not clear whether a large penis makes the male visually more attractive to the female, or whether it enhances the satisfaction and success of intercourse.

VI.

GENERAL CONCLUSIONS

The various consequences of somatic and genital selection in man and the Great Apes are summarized diagrammatically in Fig. 2, the female's view of the male, and in Fig. 3, the male's view of the female, and in Table I. An anatomist, presented with the bodies of a gorilla, orangutan, chimpanzee, and human to dissect for the first time, would conclude that the differences in the anatomy of their limbs were due to different types of locomotion. A paleontologist would be quite happy to deduce the diet of the four species from their dentition. In a similar teleological vein, it would be surprising if the marked differences in their reproductive anatomy did not reflect major differences in their sexual behavior. When Darwin first put forward the concept of sexual selection, he considered the way in which it acted on the development of general bodily characteristics,

c ORANG

- UTAN

CHIMPANZEE

P?

w

FIG.2. The female's view of the male, indicating the degree of sexual dimorphism in body size, the size and position of the testes, and the size of the erect penis.

SEXUAL SELECTION: SOMATIC AND GENITAL

GORILLA

-

ORANG UTAN

0

153

WOMAN

CHIMPANZEE

P

FIG. 3. The male’s view of the female, indicating the degree of sexual dimorphism in body size, and the relative development of the mammary glands and the perineum prior to the first pregnancy.

but was presumably too modest to extend his argument to the genitalia themselves. A study of man and the Great Apes emphasizes the fact that somatic size and genital development are not necessarily related to one another; witness the giant male gorilla and his minute testes, and the small male chimpanzee with his enormous testes. It therefore seems helpful to subdivide sexual selection into two components parts: somatic selection, the factors determining general body size, and genital selection, the factors determining the size of the gonads and external genitalia. Somatic selection is apparently related to the mating system (monogamy, polygamy, promiscuity), and is concerned with successful competition for access to a mate. Genital selection is far more complex; although influenced by mating type, it is ultimately a reflection of copulatory frequency. In the male, this leads, among other things, to the development of the largest testes, and hence the greatest sperm reserves, in the species with the highest copulatory frequencies. Copulatory frequency in its turn is determined by the presence or absence of estrus in the female, and the frequency of its occurrence. It is interesting to note that there are marked differences in relative testis size between Man and the Great Apes, reflecting differences in the volume of tubular rather than endocrine tissue. However, no such differences are seen in the female, where ovarian size bears a rather constant relationship to body weight. This is not surprising when one remembers that the germinal component of the ovary represents a relatively

GONADWEIGHTSAS

A

TABLE I PERCENTAGE OF TOTAL BODY WEIGHTIN THE GREATAPESAND MAN

Mating system

Social structure

Testes:body weight ratio (8)

0varies:body weight ratio

Species Gorilla Gorilla gorilla Orangutan Pongo pygmaeus Chimpanzee Pan troglodytes Mall Homo sapiens

Polygynous

Small one-male groups

0.017

0.012

Polygynous

Solitary

0.048

0.006

Promiscuous

Large mixed-sex troops

0.269

0.010

Serially monogamous

Family groups

0.079

0.014

W)

~

SEXUAL SELECTION: SOMATIC AND GENITAL

155

small proportion of its total volume; since the oocytes of all mammals are similar in size, and since very few of the finite population of oocytes will ever be ovulated, regardless of the ovulation rate of the species concerned, there is no reason why an elephant should have more (or less) germinal tissue in its ovaries than a mouse. Thus, variations in ovary size between species can be expected to reflect only changes in the volume of endocrine tissue, and will therefore be related to the total body mass and hence the volume of distribution of the ovarian hormones. Changes in testicular size, on the other hand, although being dependent on total body size as far as the endocrine tissue is concerned, will be predominantly determined by differences in the volume of germinal tissue. Since there appears to be a gene on the Y chromosome that determines the amount of tubular tissue laid down in the prepubertal gonad (Hayward and Shire, 1974), testis size might be expected to respond rapidly to selection pressures. One of the most intense forms of selection will be found in promiscuous mating systems; if several males are allowed to copulate with one female, gamete selection will favor the male who deposits the most spermatozoa. Genital selection has also led to the development of organs of sexual display, such as the penis in the male, and the perineum or the mammary gland in the female. Both can be expected to be enhanced in promiscuous situations, whereas in polygynous systems the need for female display is less apparent. Man poses a particular problem if we are to understand the pronounced development of the flaccid and erect penis of the male, and of the breasts of the female. The most plausible explanation is that these characteristics, together with the suppression of estrus in the female, have enabled sexuality to be exploited for social purposes by constantly reinforcing the strength of the pair bond. In conclusion, perhaps the most telling anatomical clues to the reproductive behavior of man and the Great Apes are the relative body sizes of the male and the female, and the relative sizes of the testis and the ovary. It remains to be seen whether the significance of these simple anatomical clues will be confirmed by examination of a far wider range of species.

References Abbie, A. A. 1969. “The Original Australians.” Rigby, Sydney. Asdell, S. A. 1965. “Patterns of Mammalian Reproduction.” Constable, London. Crook, J . H . 1972. Sexual selection, dimorphism and social organisation in the primates. In “Sexual Selection and the Descent of Man 1871-1971” (B. Campbell, ed.). pp. 231-281. Aldine, Chicago, Illinois. Darwin, C. 1859. “The Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life.” John Murray, London. Darwin, C. 1871. “The Descent of Man, and Selection in Relation to Sex.” John Murray, London. de Pousargues, E. 1895. Note sur I’appareil genital male des orangoutans. Now. Arch. Mus. Hist. Nar. Paris, Ser. 3 7, 8-82. 117-1 18.

156

R. V. SHORT

Dyer, K. F. 1977.The trend of the male-female performance differential in athletics, swimming and cycling 1948-76. J. Biosocial Sci. 9, 325-338. Eckhardt, R. V. 1975.The relative body weights of Bornean and Sumatran orangutans. Am. J. Phys. Anthropol. 42, 349-350. Eliasson, R. 1975. Analysis of semen. In “Progress in Infertility’’ (S. J . Behrman and R. W . Kistner, eds.), 2nd Ed., pp. 691-713.Little, Brown, Boston, Massachusetts. Fisher, R. A. 1930. “The Genetical Theory of Natural Selection.” Clarendon, Oxford. Ford, C. S., and Beach, F. A. 1952. “Patterns of Sexual Behaviour.” Eyre & Spottiswoode, London. Fossey, D. 1974.Observations on the home range of one group of mountain gorillas (Gorilla gorilla beringei). Anim. Behaw. 22, 568-581. Freund, M. 1963. Effect of frequency of emission on semen output and an estimate of daily sperm production in man. J. Reprod. Fertil. 6 , 269-286. Gavan, J. A. 1971. Longitudinal, postnatal growth in chimpanzee. I n “The Chimpanzee” (G. H. Bourne, ed.), Vol. 4, pp. 46-102.Karger, Basel. Graham, C. E. 1970. Reproductive physiology of the chimpanzee. I n “The Chimpanzee” (G. H. Bourne, ed.), Vol. 3, pp. 183-220.Karger, Basel. Graham, C. E., and Bradley, C. F. 1972.Microanatomy of the chimpanzee genital system. I n “The Chimpanzee,” Vol. 5, pp. 77-126.Karger, Basel. Hall-Craggs, E. C. 9 . 1962.The testis of Gorilla gorilla beringei. Proc. Zool. SOC. London 139, 5 1 I -5 14. Harcourt, A. H.,and Stewart, K. J . 1977. Apes, sex and societies. New Scientist 76, 160-162. Harcourt, A. H., and Stewart, K. J. 1978.Sexual behaviour of wild mountain gorillas. Proc. Congr. Int. Primarol. SOC., 6th, Cambridge, Eng.. 1976 (D. L. Chivers and E. H. R. Ford, eds.). Academic Press, New York. In press. Hayward, P., and Shire, J. G. M. 1974.Y chromosome effect on adult testis size. Nature (London) 250, 499-500. Hosokawa, H., and Kamiya, T. 196 I. Anatomical sketches of visceral organs of the mountain gorilla (Gorilla gorilla beringei). Primates 3, I -2I. Huxley, J. S. 1938.The present standing of the theory of sexual selection. I n “Evolution” (G. R. de Beer, ed.), pp. 1 142. Clarendon, Oxford. Kelly, R. W . , Taylor, P. L., Hearn, J. P.,Short, R. V.,Martin, D. E., and Marston, J . H. 1976. 19-Hydroxyprostaglandin E, as a major component of the semen of primates. Nature (London) 260, 544-545. Leigh, L. H. 1975.Indecency and obscenity: indecent exposure. Criminal Luw Rev. pp. 413-420. McGinnis, P. R. 1973.Patterns of Sexual Behaviour in a Community of Free-Living Chimpanzees. Ph.D. Thesis, Cambridge Univ., Cambridge, England. MacKinnon, 1 . 1974. The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Anim. Behav. 22, 3-74. Martin, D. E., Could, K. G., and Warner, H. 1975. Comparative morphology of primate spermatozoa using scanning electron microscopy. I. Families Hominidae. Pongidae, Cercopithecidae and Cebidae. J . Hum. Ewol. 4, 287-292. Martin, D. E.,Swenson, R. B., and Collins, D. C. 1977.Correlation of serum testosterone levels with age in male chimpanzees. Steroids 29, 47 1-48 1. Martin, R. D. 1976.A zoologist’s view of research on reproduction. Symp. Zool. SOC. London 40, 283-319. Milligan, D., Drife, J. 0..and Short, R. V. 1975. Changes in breast volume during normal menstrual cycle and after oral contraceptives. Br. Med. J. IV, 494496. Nadler. R. D. i975a. Sexual cyclicity in captive lowland gorillas. Science 189, 813-814.

SEXUAL SELECTION: SOMATIC AND GENITAL

157

Nadler, R. D. 1975b. Cyclicity in tumescence of the perineal labia of female lowland gorillas. Anur. Rec. 181, 791-797. Nadler, R. D. 1 9 7 5 ~Second . gorilla birth at the Yerkes Regional Primate Research Center. Int. Zoo Ybk. 15, 134-137. Nadler, R. D. 1976. Sexual behavior of captive lowland gorillas. Arch. Sex. Eehaw. 5, 487-502. Nadler, R. D. 1977. Sexual behavior of captive orangutans. Arch. Sex. Eehaw. 6, 457475. Nag, M. 1972. Sex, culture and human fertility: India and the United States. Curr. Anrhropol. 13, 231-237. Noback, C. V. 1939. The changes in the vaginal smears and associated cyclic phenomena in the lowland gorilla (Gorilla gorilla). Anat Rec. 73, 209-225. O m a n Hill, W . C., and Harrison Matthews, L. 1949. The male external genitalia of the gorilla, with remarks on the 0 s penis of other Hominoidea. Proc. Zool. Soc. London 119, 363-378. Pohl, L. 1928. Zur Morphologie der mannlichen Kopulationsorgane der Saugetiere; insbesondere der Versuch einer vergleichend-anatomischen Studie iiber den Penis der Primaten, einschlieblich des Menschen. 2. Anat. Entwicklungsesrh. 86, 71-1 19. Racey, P. A., and Skinner, J. D. 1978. Endocrine aspects of sexual mimicry in spotted hyaenas (Crocuru crocutu). J . Zoo/. In Press. Ralls, K. 1976. Mammals in which females are larger than males. Q. Rev. Eiol. 51, 245-276. Raven, H. C. 1950. Reproduction System: Male. In “The Anatomyofthe Gorilla”(W. K. Gregory, ed.), pp. 86-88. Columbia Univ. Press, New York. Retzius, G. 1910. Uber die Form der Spermien bei den anthropoiden Affen. Eiol. Untersuch. 15, 83-87. Rijksen, H. D. 1975. Social structure in a wild orang-utan population in Sumatra. In “Contemporq Primatology” (S. Kondo, M. Kawai, and A. Ehara, A. eds.), pp. 373-379. Karger, Basel. Rodman, P. S. 1973. Population composition and adaptive organisation among orang-utans of the Kutai Reserve. In “Comparative Ecology and Behaviour in Primates” (R. P. Michael, and J . H. Crook, eds.), pp. 171-209. Academic Press, London. Samuels, A. 1976. Indecent exposure. Solicitors’ J. 120, 260-261. Schaller, G . B. 1963. “The Mountain Gorilla: Ecology and Behavior.” Chicago Univ. Press, New York. Schaller, G . B. 1965. The behaviour of the mountain gorilla. In “Primate Behavior. Field studies of Monkeys and Apes” (I. De Vore, ed.), pp. 324-367. Holt, New York. Schonfeld. W. A. 1943. Primary and secondary sexual characteristics. Study of their development in males from birth through maturity, with biometric study of penis and testes. Am. J . Dis. Child. 65, 535-549. Schultz, A. H. 1938a. The relative weight of the testes in primates. Anat. Rec. 72, 387-394. Schultz, A. H. 1938b. Genital swelling in the female orang-utan. J. Mammal. 19, 363-366. Selander, R. K . 1972. Sexual selection and dimorphism in birds. In “Sexual Selection and the Descent of Man 1871-1971. (B. Campbell, ed.), pp. 180-230. Aldine, Chicago, Illinois. Seuanez, H., Robinson, J . . Martin, D. E., and Short, R. V. 1976. Fluorescent (F) bodies in the spermatozoa of man and the great apes. Cytogenet. Cell Genet. 17, 317-326. Seuanez, H. N . , Carothers, A. D., Martin, D. E.. and Short, R. V. 1977. The spermatozoa of man and the great apes. Nature (London) 270, 345-347. Short, R. V . 1976. The evolution of human reproduction. Proc. R. SOC., Ser. E 195, 3-24. Sonntag, C. F. 1925. 48. on the pelvic muscles and generative organs in the male chimpanzee. Proc. 2001.Soc. London 3, 1001-101 I . Stoudt, H. W., Damon. A . , McFarland, R., and Roberts, J . 1960. “Weight, Height, and Selected Body Dimensions of Adults,” Nat. Cent. Health Stat., Ser. I I , No. 8, 1-24. U.S. Dep. Health, Educ. Welfare, Washington, D.C.

158

R. V. SHORT

Trivers, R . L. 1972. Parental investment and sexual selection. In “Sexual Selection and the Descent of Man 1871-1971” (B. Campbell, ed.), pp. 136-179. Aldine, Chicago, Illinois. Tutin, C. E. G. 1975. Sexual Behaviour and Mating Patterns in a Community of Wild Chimpanzees ( f u n troglodytes schweinfurthii). Ph.D. Thesis, Univ. of Edinburgh, Scotland. Ucko, P. J . 1969. Penis sheaths: A comparative study. Proc. R . Anthropol. Inst. pp. 27-67. Van Lawick-Goodall. J . 1968. The behaviour of free-living chimpanzees in the Gombe Stream reserve. Anim. Behav. Monogr. 1, Part 3 . Van Lawick-Goodall, J . 1969. Some aspects of reproductive behaviour in a group of wild chimpanzees, Pan rroglodytes schweinfurfhi, at the Gombe Stream chimpanzee reserve, Tanzania, East Africa. J. Reprod. Ferril., Suppl. 6 , 353-355. Vevers, H . G. 1977. The influence of the ovaries on secondary sexual characters. In “The Ovary,” 2nd Ed., Vol. I, pp. 447473. Academic Press, New York. Warner, H., Manin, D. E., and Keeling, M . E. 1974. Electroejaculation of the Great Apes. Ann. Biomed. Eng. 2, 419432. Webb. P. 1975. “The Erotic Arts.” p. 514. Secker & Warburg, London. Wehefritz. E. 1923. Systematische Gewichtsuntersuchungen an Ovarien rnit Beriicksichtigung anderer Driisen mit Innerer Sekretion, sowie iiber ihre Beziehungen zum Uterus. Z. Konstirut. 9 , 161-171.

Westoff, C. F. 1974. Coital frequency and contraception. Fam. flann. Perspecr. 6 , 136-141. Wickler, Von W. 1966. Ursprung und biologische Deutung des Genitalprasentierens mannlicher Primaten. Z . Tierpsychol. 23, 422437. Wislocki. G. B. 1932. On the female reproductive tract of the gorilla, with a comparison of that of other primates. Conrrib. Embryo/. Curnegie Inst. Washington 23, 165-204. Wislocki, G. B. 1942. Size, weight and histology of the testes in the gorilla. J. Mammal. 23, 28 I -287.

ADVANCES IN THE STUDY OF BEHAVIOR. VOL. Y

Socioecology of Five Sympatric Monkey Species in the Kibale Forest, Uganda THOMAS T.

sTRUHSAKER* A N D

LYSALELAND*

NEW YORK ZOOLOGICAL SOCIETY AND THE ROCKEFELLER UNIVERSITY NEW YORK, NEW YORK

I. 11. 111. IV.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Summary of Ecology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Time Budget . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Social Organization . . . . . . . . . .

D. Group Spread . . . . . . , . F. Section Summary V . Social Behavior

, ,

..,

B. Aggression ( Agonism) , . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ..... ... C. Grooming . . . . . . . . . . . . . . . . . . . . . D. Sexual Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. Social Interactions of Neonates (Aunt Behavior) . . . . . . . . . . . . . . . . . . . . F. Intergroup Relations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . .. . . . . . . . . . . . . . . . . . . . . . VI .

............... VII.

A. Summary of Results . . . . . . . . B. Summary of Conclusions and Research . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I.

159

i62 162 166 166 167 169 170 173 176 177 177 181 189 195

197 199

20 I 20 1 20 I 209 21 1 218 218

220 223

INTRODUCTION

One of the central themes in primate field studies since their resurgence in the 1960's has been the relation between behavior and ecology. More specifically, *Present address P 0 Box 409, Fort Portal, Uganda, East Afnca 159

Copyright (L) 1979 by ALddernlL P r e w InL All nghts of repduction in any form reserved ISBN 0 I2 lW5W 5

160

THOMAS T . STRUHSAKER AND LYSA LELAND

emphasis has been placed on the ecological parameters affecting social organization. Correlations between behavioral and ecological variables have been invoked to develop hypotheses on the evolution and adaptive significance of primate social systems (e.g., Crook and Gartlan, 1966; Struhsaker, 1969; Crook, 1970, 1972; Kummer, 1971; Eisenberg et al., 1972). Many of the attempts to construct a theoretical framework relating phylogeny, ecology, and social organization are hindered by the comparison of data from a wide range of studies that lack standardized methods and are often variable in duration, precision, and detail. Interpretation and examination of the hypotheses offered are further confounded by the use of vague terms lacking operational utility. A major problem is that of reducing extraneous variables in order to extract and understand the significant relationships and the relative importance of the factors involved. This problem can be overcome to a large extent through comparison of several species living in the same area at the same time. The ecological variables are thereby minimized so that the relationship of phylogeny and anatomical and physiological adaptations to habitat exploitation and social organization and behavior can be examined more precisely. Contrasting closely and distantly related species further clarifies the issue of phylogeny. However, only a few primate studies have placed emphasis on interspecific comparisons within the same or similar habitats (e.g., Crook and Aldrich-Blake, 1968; Clutton-Brock, 1974; Klein and Klein, 1975; Struhsaker and Oates, 1975; Hladik, 1975; Sussman, 1974; Charles-Dominique, 1977; Struhsaker, 1978b,c). Many of the problems of extraneous variables have been overcome through the integrated studies of five sympatric monkey species living in the Kibale Forest of Western Uganda. These studies were begun in 1970 and are continuing at present. They are particularly valuable in that they were all carried out in the same part of the forest, methods were standardized as much as possible, and the species studied cover a variety of phylogenetic lines. The five species are red colobus, Colobus badius (Struhsaker 1974, 1975, 1978a,b); black and white colobus,' Colobus guereza (Oates, 1974, 1977,a,b,c, 1978; Oates et al., 1978; for a comparison of the two colobus, see Struhsaker and Oates, 1975); mangabey, Cercocebus afbigena (Waser, 1974, 1975a,b, 1976, 1977a,b, 1978; Waser and Floody, 1974; Waser and Waser, 1977); blue monkey Cercopirhecus rniris (Rudran, 1976, 1978); and redtail monkey, Cercopirhecus ascanius (Struhsaker, 1977, 1978b,c). Although all studies covered several social groups of each species, this comparison is based primarily on information from the main study groups of each species. The studies were made in the forest adjacent to the Kanyawara Forest Station. A description of the forest and methods is given in Struhsaker (1975). Unless otherwise stated, the generali'Hereafter designated as bw colobus.

TABLE 1 A SUMMARY OF IMPORTANTPHYSICAL A N D SOCIOECOLOGICAL CHARACTERS OF FIVEMONKEY SPECIESFROM THE KIBALEFOREST, WESTERNUGANDA Mangabey (Cercocebus albigena)

Redtail (Cercopithecus arcanius)

Blue (Cercopkhecus ) rnitis)

Red colobus (Colobus badius)

bw Colobus (Colobus guereza)

10.5/7

10.5/7

10.5/7

413

6/34

Folivore Diversified diet Cohesive 50 Multimale 1 :2

Folivore Monotonous diet Cohesive 9 One male 1:3-5

Omnivore Superabundant fruits Widespread

Omnivore Mobile insects Widespread 30-35 One male I :9

Omnivore “Opportunistic” Widespread 24 One male 1:lO

Yes Males Juvenile and subadult females

No Females Adult and subadult males

Yes Females Adult males

Rank order of neonate handling by nonmothers Home range size (ha) Biomass density (kdkm’) Intergroup relations

5

1

2

No Females Adult and subadult males 3

No Females Adult and subadult males 4

35

16

410

24

61

I760

64-570

60

328

I27

Complete range overlap

Mutual avoidance with much overlap

Territorial

Territorial

Defenders of social space or territory

Males (adult and subadult)

“Territorial” with much range overlap Males (adult and subadult)

Males and females (except infants)

Males and females (except infants)

Males and females (except infants)

Body weight (kg) rnale/female Food: gross specialty lntragroup spacing Mean group size Social structure Adult male: female ratio Sexual swelling Core of group Migrators

15

Multimale I :2

162

THOMAS T. STRUHSAKER A N D LYSA LELAND

zations presented here are believed to be representative of the Kanyawara populations of these five species. This paper is intended to ( I ) summarize the major behavioral and sociological features of these five sympatnc species based on data in the above listed references, (2) present hypotheses relating their social organization and ecology, (3) examine the applicability of these hypotheses to other primates, especially other cercopithecids, and (4) suggest testable hypotheses and fruitful areas for future research.

11. SUMMARY OF ECOLOGY

Important ecological features of these five species have been compared in Struhsaker (1978~)and will be summarized briefly here (Table I). The two colobus species with their enlarged sacculated stomachs are essentially leaf eaters (279% of annual diet). Both prefer young leaves, buds, and flowers, but only the bw colobus subsists on mature leaf blades at certain times of the year. The red colobus have a much more diversified diet in terms of species than the bw colobus, have much larger home ranges, and achieve greater biomass densities. The other three species (mangabeys, redtails, and blues) are omnivores who rely heavily on fruit ( 3 44%) and arthropods (319%). At certain times of the year, blues are primarily leaf eaters. Differences in home ranges and biomass densities among the omnivores are related to their degree of dependence on superabundant fruit resources and the types of arthropods exploited. Mangabeys have the largest home ranges and lowest biomass density. Blue are intermediate, and redtails have the smallest home ranges but highest density of the omnivores. Mangabeys and the two colobus species are similar in body size (adult male 10 kg and adult female 7 kg); blues are intermediate (adult male 6 kg and adult female 3-4 kg); and redtails are the smallest (adult male 4 kg and adult female 2.9 kg). 111. TIMEBUDGET An analysis of how different species distribute their time among various activities is essential to any characterization of their life styles, and lays a foundation for interrelating their ecology and behavior (see Table 11). The categories include all activities observed, and results are based on latitudinal samples. Feeding (ingestion): bw colobus fed considerably less than the other four species which correlates most notably with its propensity to rest more. This low feeding score cannot be related to the leafy diet alone because the red colobus, also folivorous, spent more time feeding than any of the others. Bw colobus,

163

SOCIOECOLOGY OF FIVE SYMPATNC MONKEY SPECIES

TABLE I1 TIMEBUDGETPERCENTAGE'

Activity

Red colobus

bw Colobus

Feed Forage Scan Restc Climb Self-clean Groom Cling Play Miscellaneous

41.0 4.3 I .8 32.4 9.0 0.7 4.5 3.4 2.7 0.3

19.9 ? ? 57.4 5.4 0.7 6.2 5.7 4.6 0.2

N:

Mangabey

Redtail

Blue

36.6 7.4

33.5 0.6 20.5 10. I

33.3 4.8 4. I 29.0 16.5

?b

20.5 22.2 0.5 5.8 4.5

I .8 0.6

17.4 I .6 5.6 8.7 1.8 0.3

d

6. I d d d

6983

6OOo

17,430

3275

18,325

Aug. 1970Aug. 1971'

Feb. 1971Jan. 1972'

Apr. 1972Apr. 19739

Nov. 1973June 1974'

Mar. 1973Feb. 1974h

'Data were collected during latitudinal samples at half-hour or quarter-hour intervals. The first behavioral pattern sustained for at least 5 seconds was scored for each individual observed. *Not scored by Waser; 0.5% in another group (S. Wallis, personal communiation). 'Includes sitting and standing. dThese categories were lumped together with several other social and nonsocial activities which together totaled 6. I % of the time budget. 'Struhsaker (1978b). 'Oates (1974). "P. M. Waser (personal communication). *R. Rudran (personal communication).

however, concentrated heavily on only one food species (Celris durandii), and, in particular, the young leaves of this species that contain one of the highest concentrations of crude protein for leaves of any species (34.9%, Struhsaker, 1975; see also section on Rest below). In view of the striking anatomical and physiological differences in digestive systems and food habits between the leaf-eating red colobus and the three omnivores, it is surprising that the amounts of time each spent feeding are very similar. The next two categories deal essentially with methods of capturing arthropod prey and therefore relate primarily to the three omnivores. Forage (manipulation of substrate in search of food, usually arthropod prey): Red colobus spent a large amount of time in this activity considering their infrequent ingestion of free-living arthropods. The high score for mangabeys and blues are interpreted as a reflection of their heavy dietary reliance on relatively immobile forms of arthropods. Mangabeys may have the highest score because

164

THOMAS T . STRUHSAKER AND LYSA LELAND

the microhabitats they most commonly exploited (i.e., dead wood and bark, and hollow twigs) required considerable manipulation before the prey living in them could be procured. This type of foraging is more time consuming than examination of clumps of moss and other epiphytes which was the main foraging pattern of blues. Scan (slow back and forth movement of the head; visual examination of substrate without manipulation): Redtails spent much more time scanning than any of the other species. This high score related both to their greater consumption of mobile arthropods, which were hunted and caught by stealth rather than by substrate manipulation, usually from the surface of foliage and bare branches, and to searching for sparsely distributed fruits. Rest (inactive): Bw colobus had a higher resting score than the other four species. However, it remains to be determined if they rest more (a) because their food is so highly nutritious that they do not need to spend more time feeding, (b) because their food requires a longer time for digestion andor detoxification, or (c) as a means of conserving energy and thereby reducing their food requirements. There is a rough correlation between the amount of time spent resting and the degree of folivory. The two colobus rested more than the three omnivores, and the most folivorous of the omnivores (blues) rested more than the other two. The greater reliance on arthropods, especially mobile forms. probably requires that redtails spend more time scanning than the other species, and consequently less time resting. Furthermore, when redtails do rest, they are often in the middle of very dense liana thickets where observation is difficult, thus creating observer bias. Climb (all forms of locomotion): The omnivores spent more time climbing than the folivores. They also covered greater distances each day. As argued elsewhere (Struhsaker, 1978c), this is probably related to the differences in the density and dispersion patterns of their food. For example, foliar foods generally occur in greater densities than fruits and insects. Self-clean (autogroom): This activity was infrequent for all species and not obviously related to ecological factors. Groom (allogroom): The proportion of time spent on this activity was similar in all species regardless of gross differences in ecology, group size, composition, and intragrouphnterindividualspacing patterns. We suggest that a certain level of grooming is necessary because (1) some areas of the body can be cleaned only through grooming (e.g., Struhsaker, 1967b) and (2) grooming may be critical to the maintenance of the group’s social cohesion. Cling (infants clinging to mother or other monkey): Since the frequency of this activity could be directly dependent on the number of infants, it is necessary to correct for interspecific differences in proportions of infants in the group (Table 111) by comparing these figures with the proportion of the time budget devoted to clinging (Table 11). When these corrections are made it is apparent that redtail

v

a

"Q'

F

"N,

I

-2

166

THOMAS T. STRUHSAKER AND LYSA LELAND

infants cling slightly more than red colobus, and much more than infant bw colobus and mangabeys. Mangabey infants cling only slightly more or about the same as do bw colobus. Thus, we can rank these four species, from greatest to least clinging, as follows: redtails, red colobus, mangabeys, and bw colobus. Blues are not considered in this analysis because precise figures for this activity are not available. We offer the following interpretation of these results. When mothers are not moving about, infants often leave the clinging position and climb about in an exploratory manner and play. Because the redtails spend more time moving about than the other species, the infants have less opportunity to leave their mothers. The red colobus infants cling more than one would expect on the basis of this species’ time budget and this may be related to their apparently slower maturation rate and the more possessive nature of their mothers. Play: The amount of play seen may be dependent on the proportions of infants and young juveniles present in the group, as these are the age classes that account for most of this activity. Correlations similar to the ones above were made in which the proportions of these age classes (Table III) were compared with the proportions of play activity (Table II). The four species for whom precise data are available can be ranked as follows, from greatest to least amount of play: bw colobus, red colobus, mangabeys. and redtails. Play, then, seems to be more prevalent in folivores than in omnivores. This could be related to the relative inactivity of folivores: they tend to move about less both in search of food and while feeding, and they rest more. Therefore, young juveniles and infants would have more opportunity to play. The feeding scores for the three omnivores were similar. They spent more time moving than the folivores, presumably in search of ripe fruits and arthropods. The folivores, on the other hand, spent more time resting than the omnivores, possibly because their diet of foliar foods required less search time or perhaps more time for digestion. Frequency of the principal social activity, grooming, was similar for all five species. In some aspects then, the time budget reveals gross differences between the omnivores and folivores in terms of their ecology, but in others, such as grooming, it does not. The following section, however, shows that there is no clear correlation between gross feeding ecology and social organization except in group and interindividual spacing.

IV. SOCIAL ORGANIZATION A.

GROUPSIZE A N D COMPoSlTlON (TABLEIll)

The main study group of red colobus, although typical in its proportional age-sex composition, was smaller in size (circa 20) than the usual group in

SOCIOECOLOGY OF FIVE SYMPATRlC MONKEY SPECIES

167

Kibale which numbered about 50 individuals. Counts of five mangabey groups averaged 14 members, with a range of 6-28; the main study group was of typical size and composition (Waser, 1974). Definitive counts of redtail groups were extremely rare, but available data indicate that the main study group was of normal size and composition, ranging from 30 to 35 individuals. The main study groups of bw colobus and blues were representative of these species (Oates, 1977~; Rudran, 1976, respectively). Average group size decreased in magnitude in the following sequence: red colobus, redtails, blues, mangabeys, and bw colobus, the widest differences occurring between the two folivorous species. Harems having only one fully adult male constituted the modal group of bw colobus, redtails, and blues; multimale bisexual groups typified red colobus and mangabeys. Thus, as with average group size, there was no obvious correlation between social structure and the divisions of gross feeding ecology (folivores and omnivores). Some of the differences between species in age composition (based on body size) may be the result of interobserver discrepancies in age classification, interspecific differences in maturation rates, and the small sample size.

B. GROUPDYNAMICS Most changes in group membership for all five species were due to births and presumed deaths. Red colobus males were usually permanent members of the group in contrast to the other four species where adult males left and joined groups relatively frequently (Table IV). Adult females were the most stable elements of the social groups of bw colobus, mangabeys, redtails, and blues, but less so for red colobus. Only one definite case has been observed of an adult female transferring between groups. This was an old female who temporarily joined the main study group of red colobus for about two to three months. She greatly resembled an adult female who disappeared from the group some three years previously. Female transfers have not been observed in any of the other species. The red colobus were also exceptional in that members of the juvenile class were the most mobile social element, whereas they were never known to transfer between groups in the other species. Juvenile female red colobus were readily accepted into the main study group on several occasions, both on a temporary and long-term basis (Struhsaker, unpublished observations). Only on oile occasion did an old juvenile male attempt to join the main study group of red colobus. Although eventually tolerated and groomed by a few of the adult females, he was often threatened and chased by the adult males. He finally disappeared after remaining on the periphery of the group for several months. Juvenile and subadult male red colobus must leave groups in view of their occurrence as solitaries. However, no juvenile male has yet left the main study group.

168

THOMAS T . STRUHSAKER AND LYSA LELAND

TABLE 1V FIRSTESTIMATES OF RATESOF HAREM-MALE REPLACEMENT” OR MULTIMALE GROUP^'^ Species

Rate

OF AN

ADULTMALEJOINING

A

Based on

Red colobus

0 in 84 months

bw Colobus

I in 3 6 4 8 months

3 groups (3, 4, and 2); Oates ( 1 9 7 7 ~ during ) 48 months

Mangabey

I in 24 months

2 groups (M and S); Waser (1974 and personal communication); 2 3 males joined M group during 42 months (1/14 months); no males joined S group during 30 months; (3/72 group-months)

Redtail

I in 22.5 months

2 groups ( I T K and S); Struhsaker (1977 and unpublished data); no male replacements in ‘ITK group during 23 months; 2 male replacements in S group during 22 months (U11 months); (2/45 group-months)

Blue

I in 22.7 months

2 groups (I and 11); (Rudran, 1976, 1978, and personal communication; 2 I male replacement in group I; 2 2 male replacements in group I1 during 34 months; (23/68 groupmonths)

I group; Struhsaker (1975 and unpublished data) during 84 months

“Includes bw colobus, redtail, and blue. bIncludes red colobus and mangabey. “These are minimal estimates because in some of the estimates there were long intervals between the initial study and the subesequent and relatively brief observation periods which revealed the changes in male membership.

Mangabeys, who also form multimale bisexual groups, differ from the red colobus in that the adult males appear to be the unstable element of the group. Although transfers between groups have not been observed directly, P. M. Waser (1974 and personal communication) noted that four adult and subadult males left, and three joined his main study group in a period of 42 months (table IV). S . Wallis (personal communication) observed one adult male transfer between neighboring groups. In all species with harem-male groups, males born in the group apparently leave the group as subadults. From the Kibale studies, harem-male replacement appears to occur approximately every two years. Harem-male replacement among bw colobus appears to involve from one to five other males “joining” the group, or at least being on the periphery. Aggression among these males was infrequent and of low intensity. Indirect evidence suggests that eventually all the males leave except the new harem male who then drives out the remaining subadult males and may kill newborn infants. This hypothesis of the mechanics of male replacement is based on group counts and

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

169

recognition of individuals made on three different occasions over a period of four years (Oates, 1977~). R. Rudran (personal communication) observed the initial stages of male replacement in one group of blues. This involved frequent aggression between the resident male and the newcomer over a period of at least two months. When Rudran returned two years later, there was a new harem male in each of the two main study groups. The same redtail male retained the harem position in the main study group at Kanyawara for at least 23 months. In a second major redtail study in the Ngogo area of Kibale, a harem-male replacement occurred after the first four months of study during a 4-week period between the monthly samples of the group. The new male was seen to kill two newborn infants in the group within two months of the takeover (Struhsaker, 1977). Eight months later, five other adult and subadult males joined the group. There was frequent aggression among all these males who remained in the group for at least two and possibly as long as four months. It is not certain how or why these males left, but eventually only the original harem male remained. Two months later he was replaced by another male, although again the process was not observed. Both cases of redtail male replacement, however, occurred much more rapidly than in the one case of blue male replacement.

c.

SOLITARIES A N D

ALL-MALEGROUPS

Solitary adult and subadult males were relatively common throughout the home ranges of bisexual groups. Although red colobus was the most abundant species at Kanyawara, solitary males were seen infrequently in comparison to the other species, and these males were usually old juveniles and subadults. No solitary females have been seen. The extremely peripheral position commonly assumed by some male mangabeys who belong to the group makes equivocal the case for solitary mangabeys at Kanyawara (Waser, 1974). However, at the Ngogo study area in Kibale, S. Wallis (personal communication) has confirmed the existence of a solitary adult male mangabey who remained in this status for at least several months. It would appear that, unless the transfer of males between groups is immediate, those making such a move must spend some period of time in a solitary state, albeit temporary. The density of most species in this part of Kibale is sufficiently high that the majority of so-called solitary males were usually within audible range of conspecifics, and often within visibility. We had the impression that these solitaries spent a considerable amount of time moving about from the periphery of one social group to another, possibly as a means of monitoring the social situation and locating a “vacancy.” This would appear to be the case particularly among

170

THOMAS T . STRUHSAKER AND LYSA LELAND

the solitaries of harem-male groups. Thus, these males were solitary more in a social than in a spatial sense. All-male groups have not been observed in red colobus, mangabeys, redtails, or blues. Two males were seen together once each in red colobus and redtails (Struhsaker 1975 and unpublished observations). The occurrence of two bw colobus males together, however, was fairly common as were “solitary” males on the periphery of harems. A temporary association of six adult and subadult male bw colobus was seen once (Oates, 1977~).In the rain forest, the pressure to establish all-male groups as a defense against predation appears minimal as compared to the African Savanna (Struhsaker, 1969). In Kibale, there is only one predominant predator, the crowned eagle (Stephanoaetus coronarus), and detection and concealment are a more efficient means of avoiding its predation than coordinated defense. The rare cases of all-male groups among bw colobus may be an example of phylogenetic inertia reflecting the evolutionary history of this species which is presumed to be adapted to the more open habitats of gallery forests (Struhsaker and Oates, 1975) where predation pressure would act against a solitary existence and in favor of all-male groups. Solitary male red colobus often associated with social groups of other species, particularly with bw colobus. Solitary male redtails tended to associate temporarily with groups of red colobus who often groomed them. D. GROUPSPREAD Precise measurement of the spatial distribution of group members is difficult in the rain forest because of poor visibility (Table V). Furthermore, there were the limitations of only one observer, particularly when group spread was wide. In a few samples of the main groups of blues and redtails, however, two observers using walkie-talkies were able to make relatively accurate measures of maximum group spread (Fig. 1). Within a species, the data indicate that group dispersion appears to be a direct function of group size, at least up to some maximum spread. Folivores were more cohesive than omnivores, although some very large groups of red colobus may have typical spreads similar to those of small groups of omnivores. The maximum group spread of omnivores, however, was usually much greater than that of folivores even when group size is considered. Among the two folivorous species, the red colobus had a greater group spread than the bw colobus. Differences in group size between the two species may account for much of this. In addition, the more diversified diet of red colobus exposed the group to a greater variety of food-dispersion patterns than the more monotonous diet of bw colobus. Among the three omnivores, mangabeys showed the greatest group spread (Waser, 1974, 1977a; Rudran, 1976; Struhsaker, unpublished observations).

TABLE V SPREAD ( I N METERS)

INTRAGROUP

Species group size (name) Red colobus 20 (CW)" -80 (ST)

Typical

c50

Maximum

Minimum

100

- 10

Method and source

Single observer. rough estimate, not systematic; Struhsaker ( 1975)

75-100

bw Colobus 12.3 (4)

17

100

5

Mangabey 15.5 (M)

I27*

48d'

10

3 2 observers, measured from map plottings, systematic, over 16 days; Waser and Floody ( 1974)

15.5 (M)

91*

27d'

-

2 observers. measured from map plottings. systematic (N 1974)

Single observer, rough estimate, systematic ( N 1977c)

=

447); Oates (1974,

=

25); (Waser,

2000'

5 (S) Redtail -35 (TTK) -35 (TTK)

Blue 24 (1)

Mode: 36-50 Median: 5 1-55 3 100

common

Mode and median 46-50

105*

5*

Same as above (N = 82); (Waser, 1974)

226-230

6-10

2 observers, measured from map plottings, systematic (N = 79) during 4 mornings; Struhsaker and Rudran (unpublished observations)

-

116-120

I25

-

0-5

Single observer, rough estimate, not systematic; over 65 days in 13 months; Struhsaker (unpublished observations) 2 observers, measured from map plottings, systematic (N = 49) during 2 mornings and 2 afternoons; Struhsaker and Rudran (unpublished observations) Single observer, rough estimate, not systematic; Rudran (1976)

Sample group designation. bDoes not include single isolated individuals (temporarily peripheral). Includes single isolated individuals (temporarily peripheral).

P 8 c 0

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

173

Maximum spreads were due to the propensity of some males to be extremely peripheral for most of a day, or even for several days. Excluding these temporarily peripheral males from the computations reveals that the group spread of mangabeys was still greater than that of either redtails or blues. Since mangabeys had the smallest group size of the omnivores, this can be discounted as a contributing factor. Mangabeys commonly exploited microhabitats of dead wood, etc. for arthropods (Waser, 1975b). These were widely dispersed and often destroyed in the process of exploitation. Mangabeys also were more dependent on superabundant fruit than the other omnivores. Mangabeys appeared to have a wider group spread as a consequence of food dispersion and methods of foraging. Redtails appeared to have a slightly greater spread than blues (Fig. 1). To some extent this may be dependent on differences in group size but it may also be related to the more peripheral nature of the redtail harem male (see next section). Furthermore, redtails relied more heavily on mobile arthropods which may necessitate wider group spread as a means of maximizing hunting efficiency. Directly related to group spread were the frequency of occurrence and loudness of cohesion vocalizations. All group members of the omnivorous species commonly gave conspicuous grunt calls which enhanced group cohesion (Marler, 1973; Waser, 1974). Mangabeys, with the widest group spread, correspondingly gave the loudest grunts (personal observations and Waser and Waser, 1977). Adult males of these three species also gave loud calls audible over great distances and which played some role in group cohesion. Although female and immature red colobus seldom vocalized, the adult males gave various calls that were relatively loud and related to the initiation of group progressions and thereby enhanced cohesion. These vocalizations were given very frequently throughout the day, about 285 bouts per 12-hour day (Struhsaker, 1975). In contrast, the bw colobus infrequently, 11 to 12 times per day (Oates, 1974), gave a low-amplitude, soft grunt which at times appeared to be related to group movement. This low incidence was probably related to the infrequent moves of the group, and the low amplitude due to their relatively small and cohesive groups. E.

INTERINDIVIDUAL SPACING

Spatial distribution of group members was studied through a series of samples in which the distances between a focal animal and all its neighbors within 5 FIG. 1 . Estimates of maximum group spread based on map records made at fixed time intervals by two observers simultaneously following one monkey group and maximizing the distance between the two observers by use of walkie-talkies. The data for the blue monkey group I were collected during two mornings and two afternoons (14-18 April 1974): n = 49 estimates. The data for the redtail monkey group "K were collected during four mornings (14-17 May 1974): n = 79 estimates (Struhsaker and Rudran, unpublished observations).

TABLE VI INTERINDIVIDUALSPACING“ Focal animalb

Subadult male

Adult female (excluding clinging young as neighbors)

Adult female (including clinging young as neighbors)

Species

Adult male

Red colobus

0.54 (3,74)b

0.45 ( I ,201

0.95 (3.61)

I .32 (3.61)

Struhsaker (1975 and unpublished observations)

bw Colobus

2.6 (1.20)

0.60 ( 1 , l I )

2.2 (2.31)

3.14 (5.81)

Oates ( 1974, I977c)

Mangabey

0.50 (3.10)

0 (2.1 I )

0.62 (6.42)

0.86 (6,42)

Struhsaker (unpublished data on M group, 29 and 30 Jan. 1973)

Redtail

0.10 (1.82)

0.31 (1.26)

0.85 (10.344)

I . 15 (10,344)

Struhsaker (unpublished data on ‘ITK group, 13 mos. 1973-1974)

Blue‘

0.22 ( I , 176)

0.24 (3,505)d

-

0.32 (10.1213)

Rudran (unpublished Progress Repon No. 2, Table 4)

OMean number of neighbors within 2.5 meters of focal animal per sample. bParentheses include the number of individuals sampled and the number of samples. “Includes only neighbors G 2 meters. dIncludes males and females.

Source

175

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

meters were estimated. The results in Table VI demonstrate that folivores have more neighbors within 2.5 m than omnivores. These data are consistent with the conclusions in the previous section where it was shown that folivores were more cohesive than omnivores, and best explained in terms of food density and dispersion patterns. Near neighbor data also reflect basic differences in group structure. Despite the pronounced differences in group spread, there was a surprising similarity in numbers of neighbors of adult male red colobus and mangabeys. This could be due partly to observer bias in that peripheral mangabey males were rarely sampled. The common neighbors of focal-male mangabeys, however, were primarily adult females, while those of the red colobus were both adult males and females. Adult male red colobus were more permanent and cohesive members of the group and formed a distinct subgroup, as opposed to the adult male mangabeys who were more transient and widely spread. The contrasts between adult male redtails and blues are unexpected in view of similarities between these two species in overall group spread. These data suggest that the harem male redtail was more peripheral to the group than the harem male blue. There is no apparent explanation for this, although the much greater density of redtails (groups and numbers of individuals were three to four times more abundant than blues) may have required the male to patrol the periphery of his group against intruding solitary males much more frequently than was necessary for the harem male blue. Although the data and comparisons between adult females of the five species are confounded by variable numbers of clinging infants and semidependent young, there are clear indications that folivorous females had more close neighbors than omnivorous females. Female blues apparently had fewer TABLE VII NEIGHBORS OF ADULTFEMALE FOCALANIMAL

Species Redtai I" ( S 2 . 5 meters) Blue' (C2 meters)

Adult male

Adult female

Subadult (male and female)

Juvenile

-b

--r(

-

-

-

-

-

-

-

" Struhsaker (unpublished observations). b-:

Less than expected based on group composition.

'=: Equal to expected. Less than or equal to expected. +: Greater than expected.

d-/=:

'Rudran (unpublished Progress Report No. 2 and 1976, Table 1.5).

Young juvenile

-/=d

+

Infant

+c

t

176

THOMAS T . STRUHSAKER AND LYSA LELAND

TABLE VIlI INTERINDIVIDUAL DISTANCE" Focal animal Species

Adult male

Subadult male

Adult female

Red colobusb

35.5

35.0

11.8

bw Colobus"

15.0

36.4

4.9

Mangabey"

70 58.1

27.3 41.0

35.7 30.7

85.2

16.9

29.4

Y

Redtailsd

"Percentage of samples having no neighbors < 5 meters. Same sample as Table VI. bStruhsaker(1975). Oates (personal communication). dStruhsaker (unpublished observations). 'Waser(persona1 communication, 3 adult males, 2 15 samples, 2 subadult males, 144 samples, and 6 adult females, 427 samples).

neighbors than female redtails, even accounting for dependent young. During the sample period, five to seven of the ten adult female redtails had dependent young while only two to four of the ten blue females did. If dependent young were the major variable accounting for this interspecific difference, then one would predict female redtails to have only twice the number of near neighbors than female blues rather than the difference of 3.6-fold (Table VI). The interspecific differences seem to be related in part to contrasts in the spatial relations among adult females (Table VII). Adult females were the neighbors (a2m) of focal-adult female blues in only 16.7% of the cases, versus the expected proportion of 41.7%. In contrast, adult females were the neighbors ( G 2.5m) of focal adult female redtails in 27.5% of the cases, essentially equivalent to the expected value of 29% based on group composition. Interspecific comparison of the proportion of samples in which the focal animals had no neighbors within 5 meters (Table VIII) supports most of the preceding conclusions. Again, the folivores appear more cohesive than the omnivores. Adult and subadult male redtails and adult male mangabeys were the most peripheral.

F. SECTION SUMMARY Group members of omnivorous species differed from the folivores in their spacing patterns, with the latter tending to be more cohesive. In terms of phylogeny, the two Cercopithecus species have the most similar social organiza-

SOCIOECOLOGY OF FIVE SYMPATIUC MONKEY SPECIES

177

tion; but the two colobus differ greatly in group size, composition, and dynamics. The mangabey forms multimale groups like the red colobus but differs in that the females rather than the males are the permanent element. Its group size is most similar to the bw colobus. Except for the Cercopirhecus species then, there is little correlation between basic social organization and gross feeding ecology. Group dynamics, or more specifically, the socially mobile element in each species, can be related to many of the interspecific differences in social behavior, as discussed in the next section. V.

SOCIALBEHAVIOR

A. RELATIONS AMONG ADULTMALESA N D THEIRSOCIAL ROLES IN THE GROUP Red colobw: A dominance hierarchy based on priority of access was clearly discernible among the adult males of a red colobus group. Correlated with this hierarchy was a stylized form of presentation (present type 11) which was given by dominant males to subordinate males. Dominance rank was positively correlated with copulatory success: the dominant male usually performed 80% or more of the copulations. Adult males were the most permanent members of the group; they were usually spatially closer to each other than to other group members, except for estrous females; and both grooming and aggression occurred more frequently among them than expected by chance. Acceptance into the male subgroup seemed to be restricted to males that were born into the group, and was achieved only after a prolonged period of harassment and counter-harassment (occasionally resulting in wounding) between the adult males of the subgroup and the young males attempting to join. The adult males prevented an extragroup subadult male from joining by chases and threats. Available indirect evidence suggests that adult males of a red colobus group are closely related. Because of their larger size and more aggressive nature, the adult males were clearly dominant to other group members; this in turn contributed to their ability to terminate fights among the other members. The adult males apparently played an important role in maintaining group cohesion, initiating group progressions, and affecting intergroup spacing through vocalizations. They were also the main defenders of the group’s social space against neighboring groups of red colobus with whom they shared their home range, although intergroup relations varied from tolerance to physical aggression. Adult males were instrumental in threatening the principal predator, the crowned eagle (Srephnoaerus coronatus), when it landed near the group. Mungabeys: At Kanyawara, P. M. Waser (personal communication) did not find a Dominance hierarchy among males based on priority of access even

TABLE IX SUMMARY OF RELATIONS AMONGADULTMALESA N D THEIRSOCIAL ROLESIN BISEXUAL GROUPS Red colobus

bw Colobus

Very long

Moderate to 'long

Tenure Male-male relations: Tolerance Aggression Subgroup formation

Very tolerant Little to moderate Well developed

Male-male grooming

Spatial cohesion

Dominance hierarchy

Redtail

Blue

Moderate to long

Shon

Shon

Usually intolerant Moderate to much

Moderately tolerant

Very intolerant

Very intolerant

Moderate

Much

Much

Absent

Absent Very rare Poorly to moderately developed Weakly developed

Absent

Absent

Absent Absent

Absent Absent

Absent

Absent

Very Common Well developed Well developed

rare Very poorly developed Absent

Mangaky

Copulation success

Based on hierarchy and very unequal

Harem male

Somewhat related to hierarchy and unequal

Harem male

Harem male

Present

Present

Present

Probably present

Probably present

Probably present

Present

Present

Possibly present

Possibly present

Exclude extragroup males

Strongly

Strongly

Weakly'?

Strongly

Strongly

Defend group's social space or territory

Moderately to strongly

Strongly

Weakly to moderately

Moderately

Moderately

Present

Present

Present

Present

Present

Weak

Weak to moderate

Absent

Absent

Vocalizations related to group cohesion or progressions Vocalizations to maintain intergroup spacing

Threaten predators Spatial proximity and friendly social involvement with other group members

Moderate

Moderate

Weak to moderate

Intervenes and terminates fights among other group members

Present

'?

'?

180

THOMAS T. STRUHSAKER AND LYSA LELAND

though some males copulated more than others. Adult male mangabeys in the Ngogo study group, however, apparently had a dominance hierarchy based on priority of access that was positively correlated with copulatory success, but this hierarchy was much more dynamic than that of the red colobus (S. Wallis, personal communication). Adult male mangabeys were relatively transient members of the group who transferred between groups rather frequently. In contrast to the red colobus males, they were probably not closely related; they did not form any apparent subgroup within the social group, and they tended to remain more peripheral than the other members of the group. They rarely groomed one another and apparently lacked a stylized display of status. Male-male aggression was most frequent and hierarchial structure most apparent in the presence of estrous females ( S , Wallis, personal communication). All adult male mangabeys gave the individually distinctive and loud whoopgobble call, important in both intra- and intergroup spacing. One particular male in the group tended to give this call more frequently than the other adult males. This same male also differed from the other males in a statistical, but not absolute, sense in the greater frequency with which he led group progressions, moved away from the group (presumably patrolling for other groups), approached other groups, and copulated within his group. Waser (1976, 1977a) has termed such males as rapid-approach (RA) males due to their response to neighboring groups’ whoop-gobble calls, and concludes that there is only one per group. The two top-ranking males participated in the defense of Wallis’ main study group against the crowned eagle (S. Wallis and L. Leland, personal communication). Groups of mangabeys tended to avoid one another, but when they did meet and aggressive encounters ensued, all members participated, not just the adult and subadult males as with the red colobus. BW colobus (Oates, 1974, 1977~):The harem male was spatially cohesive with and proximal to other group members. He did not initiate or lead group progressions, in contrast to red colobus and mangabey males. Although intragroup aggression was infrequent, the adult male was dominant to other group members and had priority of access to spatial position and food. Infrequently, he was aggressive to the old subadult male in his group. Oates (1974) surmised that for this species the harem male eventually drives the subadult males from his group as they approach maturity, although there also may be a propensity for subadult males to leave their parental group. The harem male defended his group against neighboring harem males but on occasion appeared to tolerate one or several extra-group males who remained on the periphery of his group. Infrequent, low-intensity and usually subtle aggression occurred among these peripheral males, but occasionally these males groomed one another. As discussed earlier, these multimale groups were probably a transitory stage in the process of harem-male replacement. The regular loud calls of the harem male probably affected spacing between groups and between solitary males. He also threatened raptors when they perched near the group.

SOCIOECOLOGY OF FIVE SYMPATIUC MONKEY SPECIES

181

Redtails: In contrast to the harem male in a bw colobus group, the harem-male redtail was less integrated and more peripheral to the group. There was no evidence that he intervened in fights among other group members. He aggressed against subadult males of his group more than expected by chance and presumably drove them out when they approached maturity, although the course of events has not yet been observed. Adult males were usually intolerant of each other. Spatial separation between them was maintained through aggression and possibly through their loud calls (hacWpop) which may have functioned in intra- as well as intergroup spacing. In addition, more than one source of this call within a group possibly communicated the existence of an unstable social situation which could then be “exploited” by solitary males. During a temporary influx of several adult and subadult males in the Ngogo group, there was much intensive fighting among them. Harem-male replacement was once accompanied by infanticide in which the new harem male killed two neonates sired by his predecessor, a strategy presumed to enhance the new male’s reproductive success and also affecting intrasexual competition among adult males (Struhsaker, 1977). The harem-male redtail participated in defense of the group’s territory, but no more so, and perhaps less, than the females and immatures. He was once seen to defend the group against a crowned eagle. Blues (Rudran, 1976): Relations among males and their social roles in the harem are essentially like those of redtail males. Harem-male blues may be less peripheral and have somewhat longer tenure in the group than harem-male redtails.

B.

AGGRESSION (AGONISM)

Any attempt to make a summary comparison of agonistic encounters in these five species necessitates considerable simplification. The limited visibility afforded by the rain forest makes difficult the observations both of many group members at any one time and of an entire sequence of an aggressive interaction. The analysis is restricted to dyadic encounters, and data represent only minimal estimates of frequency of occurrence. Behaviors considered include: chases, grabbing, hitting, biting, supplantations, threat, and submissive gestures. These behaviors were lumped together and, therefore, neither distinguish between the variations of intensity nor take into account variation due to reproductive states of sampled females. The sample for redtails is extremely small and may not be representative. All data were collected opportunistically. Approximate estimates of frequency of aggressive encounters can be made for all the Kanyawara study groups: mangabeys, one per 5.5 hours (Table X); red colobus, one per 7.8 hours (Table X); bw colobus, one per 8.7 hours (Oates, 1974); redtails, one per 20 hours (if encounters that were heard but not seen are included, the rate is one per 10 hours. Struhsaker, unpublished

TABLE X DYADIC AG~NISTIC ENCOUNTER^ Aggressee (recipient)’ Age-sex class and representation in group (mean percentage)

-m

N

Adult male

Adult female

Possible subadult male

Subadult male

Subadult female Subadult Juvenile

Juvenile male

Juvenile Young female juvenile

Infant

?

N of

row

Percentage of total N

Aggressor

Red colobusb Adult male (16.0%) Adult female (33.5% Subadult male (2.56) Juvenile

(22. 1%) Young juvenile (13.16)

Infant (8.6%)

N of column Percentage of total N

+

-

+I=

+I=

+

-

26.3 4.8

19.5

3.4 0 0 -

27.1

21.2

2.5

28.6

52.4

-

-

0

0

0

33.3

0

-

-

-

0

0 -

-

9.5 0 33.3 -

0

0

-

-

0

0

32

26 18.3

-

0 -

0

+

22.5

+ I18

83.1

4.8 0

21

14.8 0

33.3 -

3

2.1 -

0

0

0

0

-

-

0

0

0

0

0

4 -

39

36

+

5

+I=

2.8

27.5

25.4

0

+

+

+

-

-

+

3.5

-

0

-

142 total N

-

'4

ri

5:

3

f?

z : " u l o o 0

0

0

0

9

9

N

o C

1 0 1 0 1 0 1 0 1 0

o 0

0

f ? - 9 m - g N

0

5:

d

0

0

0

8

1 0 1 0 1 0 1 0

183

TABLE

X

(Continued)

Aggressee (recipient)' Age-sex class and representation in group (mean percentage) ~~

e

W P

Mangabey" Adult male (19.4) Adult female (38.7) Subadult male (12.9) Juvenile female (12.9) Infant (16.1) N of column Percentage of total N

Adult male

Adult female

Possible subadult male

Juvenile Juvenile Young Subadult Subadult male female Subadult Juvenile male female juvenile

Infant

?

N of row

Percentage of total N

+

--/=

+

27.5

34.4

36.6

1.5

131

60.4

50.8

31.7

+I= 15.9

+

63

29.0

-

0

25.0

8

3.7

6.7

15

6.9

-

1.6

+

-

+

0

75.0

+

-

-

+

6.7

20.0

66.7

-

-

0 38

+

-

-

-

-

-

0

0

0

-,=

86

78

+

15

=

17.5

39.6

35.9

-

6.9

0

2 17:total N

0

I85

TABLE X (Continued) Aggressee (recipient)' Age-sex class and representation in group (mean percentage) Blue monkeyh Adult male (4.2) Adult female (41.7) Subadult (12.5) Juvenile (14.6) Young juvenile (16.7) Infant (10.4)

N of column Percentage of total N

Adult Adult male female

-

Possible subadult Subadult Subadult male male female Subadult Juvenile

+

+

11.1 -I=

33.3

9.7

35.5

38.7

+

Juvenile Juvenile Young male female juvenile

Infant

?

N of row

+

Percentage of total N

+

50

18

22.0

6.5

31

37.8

-

-I=

-I=

+I=

+

11.5

34.6

15.4

30.8

26

31.7

33.3

0

33.3

33.3

6

7.3

+

+ -

0

-

+ 100

+

-

0

+ -

0

I

-

-

-

-

0

0

0

0

0

0

8

23

24

5

1

-

+

21

9.8

28.0

29.3

25.6

6.1

1.2

+

+

+

-

-

-

-

I .2 -

0

0

82:total N

a Expected values are the mean percentage representation in the group of each age-sex class which are then compared with the observed percentages of ( I ) the row totals. and (2) the total sample of the group. + is greater than expected by chance; = approximately equal to expected value; - is less than expected by chance; -/= is equal to or slightly less than expected by chance; +/= is equal to or slightly greater than expected by chance. bN = 142; Aug. 1970-Mar. 1972 (1 112.5 hr); Struhsaker (1975). Percentage of row total. d N = 76; Feb. 1971-Jan. 1972 (720 hr); Oates (unpublished observations) "N = 217; May 1972-Apr. 1973 (= 1200 hr); includes only supplantations and chases for mangabeys; Waser (unpublished observations). 'N = 14; Mar. 1973-June 1974 (552.8 hr); Struhsaker (unpublished observations). "Includes approximate adult. hN = 82, t m p I; Mar.-Dec. 1973 all samples (910.8 hr); Rudran (unpublished Report No. 2 and 1976, Table 1.2).

SOCIOECOLOGY OF FIVE SYMPATNC MONKEY SPECIES

187

observations); and blues, one per 11 hours (Table X). Accepting the many limitations of these figures, it appears that the two species living in multimale groups have rather greater frequencies of aggression than the three species living in harems. Most of the intragroup aggression of mangabeys and red colobus was initiated by adult males, and often involved males against males. The contrast between multimale and harem species becomes even greater when one considers that the agonistic encounters in bw colobus groups were generally of lower intensity than in the other species. The closer spacing of the folivorous bw colobus group members may lead to a higher incidence of aggression than in the omnivorous redtail and blue harems where members are more widely spaced. The data in Table IX summarize the results and compares the expected with the observed proportional participation in aggressive episodes for each age-sex class. Adult males were aggressors more than expected in all five species. Male red colobus and blues were recipients of aggression more than expected: the red colobus due to male-male interactions, and the male blue due to aggression from adult females, subadults, and juveniles. In the latter case, one wonders to what extent this aggression against the harem male was in the form of so-called “false” chases as described for vervets (Struhsaker, 1967b). In contrast, the harem-male redtail was the recipient of aggression less than expected which may be related to his more peripheral position in the group as compared to the male blue. But this was clearly not the case with the harem-male bw colobus who was aggressed against less than expected in spite of his close proximity with other group members. Adult male mangabeys were aggressees less than or equal to that expected by chance, a pattern typical of most other age-sex classes in this species. In spite of gross differences in social structure (multimale versus harem male), the adult males of these five species are strikingly similar in their social patterns of aggression. Aggression among adult male red colobus and mangabeys was greater than expected. Likewise, in exceptional groups of bw colobus having more than one fully adult male, aggression between males was common and more than expected by chance (Leskes and Acheson, 1971; Dunbar and Dunbar, 1976). Adult males in all five species aggressed against females less than expected and against subadults and juveniles more than expected. The latter generalization applies to bw colobus only if one combines the data for the recipient classes of subadult male and possible subadult male (Table X). The greater aggression of adult males toward immatures may be related to the potential threat of young males reaching maturity. There seems to be a greater propensity for the subadult males of a harem social system to leave the group, while those in a multimale red colobus group tend to become integrated in the adult male subgroup. Only male red colobus aggressed against young juveniles more than expected. This was most likely related to retaliation of adult males against the sexual and general harassment by the young juveniles. Although harassment of the adult male dur-

188

THOMAS T . STRUHSAKER AND LYSA LELAND

ing copulation was also present in all the other species, it was rare in mangabeys (S. Wallis, personal communication),* and copulation was seen much less frequently in the three harem species. General harassment was peculiar to red colobus. The adult females of these five species had pronounced differences in their agonistic relations. Red colobus, bw colobus, and mangabey females were aggressors less than expected, female blues much as expected, or slightly less, and redtail females more than expected. It is not clear why female blues aggressed against their harem male more than expected, but it does correlate with his greater proximity to them, as revealed by the interindividual distance data, and contrasts with the more peripheral position of the harem-male redtail who was less involved in female aggression. However, the harem-male bw colobus was also spatially proximal to other group members, but was never aggressed against by adult females. Aggression among adult females was uncommon and less than or as much as expected by chance, except in redtails and mangabeys. Adult female red colobus were aggressive toward juveniles and young juveniles more than expected; female bw colobus and mangabeys only slightly more than expected; and female redtails and blues less than expected. This interspecific difference may be related to the more restrictive nature of red colobus mothers with respect to their neonates, they would drive off by threats juveniles and young juveniles who approached their infants. Bw colobus, redtail, and mangabey mothers, and, to a lesser extent, blues were more permissive in this regard (see neonate section below). In addition, it was our impression that weaning necessitated a more forceful effort on the part of the female red colobus. The young juveniles of the other four species tended to move away from their mothers more readily and at an earlier age. Little can be concluded about subadults because few data on the red colobus are available and these are from one subadult male only. The data for subadult blues are not segregated according to sex, and the sample for redtails is exceedingly small. The mangabey sample comprised only two subadult males. Inadequate as this information may be, it does suggest that subadult blues and redtails engage in agonistic encounters more than expected. Subadult male mangabeys are aggressed against more, but are aggressors less than expected. Subadult male bw colobus and red colobus might be involved in aggression less than expected. The latter case, however, may depend on group composition, e.g., whether or not there are other subadult or old juvenile males in the group. Subadult male bw colobus definitely appear to aggress against juveniles and possibly other subadults more than expected. Juveniles of all five species were aggressors less than expected. As with the 'P. M . Waser (personal coinmunication) did

not observe harassment in mangabeys.

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

I89

adult females and subadults, juvenile blues aggressed against the harem males more than expected. One requires further details before this situation can be fully understood, but the pattern stands in striking contrast to the other four species in which aggression against adult males was notably lacking. To summarize then, male-male intolerance has restricted the redtail, blue, and most bw colobus groups to one adult male. Aggression was most frequent in the multimale groups of red colobus and mangabeys due primarily to aggression among adult males, and often related to the presence of estrous females. Half the aggression in redtail and blue groups was over food. Adult males of all five species aggressed against adult females less than expected and subadults and juveniles more than expected. Aggression among adult females was relatively uncommon and only in redtails and mangabeys was it more than expected. C.

GROOMING

Grooming data, collected opportunistically, demonstrate that, regardless of ecology, group size and composition, adult males of all five species were groomees more than, or as much as, expected by chance, and groomers less than expected (Table XI). Adult females of all species were groomers more than expected, and all except for red colobus were groomees more than, or as much as, expected (for similar data in other Cercopithecinae, see Bernstein, 1971; Chalmers, 1973). Immature monkeys in all species groomed less than or as much as expected. There was considerable interspecific variatioq in their role as groomees; but, in the majority of cases, they were groomed less than expected. Of all infants, only the bw colobus was groomed more than expected. This was probably related to the fact that aunt behavior was more pronounced and more frequent in this species than in any of the others (see below). Of the species with multimale groups, the adult male mangabeys groomed one another less than expected while adult red colobus groomed one another more. This is probably related to the more transient and peripheral nature of male mangabeys and the extreme rarity of any cohesive or coordinated effort among them, such as in group defense. The red colobus males, on the other hand, were the permanent and cohesive element of the group and demonstrated coordinated aggressive efforts against neighboring groups. All adult males except red colobus groomed adult females more than expected. Waser (Table X) found that adult male mangabeys virtually never groomed adult females. In contrast, S. Wallis (personal communication) found that adult male mangabeys groomed adult females frequently and much more than expected by ~ h a n c e .It~ appears that in species where the males are transient they groom 31n a sample of 194 grooming bouts. Wallis found that 168 involved an adult male grooming an adult female. Of the bouts in which an adult male was the groomer, 82% involved an adult female as the grwniee.

TABLE XI DYADIC GROOMING BOUTS~

Groomee (recipient)b

Age-sex class' Groomer Red colobusd Adult male (16.0) Adult female (33.5) Subadult (2.5) Juvenile (22. I ) Young juvenile (13.1) Infant (8.6)

N of column Percentage of total N

Adult male

Adult female

Subadult

Juvenile

-

+

-

-

53.1

35.8

2.5

33.4

13.1

12.6

36.4

45.5

18.2 2.6 0 0

+ + +

26.3 -/=

13.6

+ +

51.3

+

78.0 -

0

0

226

178

+

33.2

-

26.1

+

+

63

+

9.3

~

~

~~~

~

8.6 12.4 -

0 -

17.1 -

5.1

+

100

81 -

11.9

Young juvenile

Infant

0

0

-

+I=

-/=

17.3 0 1.3 1.7 0

11.3 0

80

53

-1:

-1:

11.7

N of row

-

81

11.9

452

66.4

7.8

+

-

I1

-

1.3 I .7 0

Percentage of total N

1.6 -

76

11.2

59

8.7

2

0.3

-

-

681 total N

Groomee (recipient)

Age-sex class'

Adult male

Black and white Colobus' Adult male (8.1) Adult female -

(40.5) Subadult male' (23.7) Juvenile male (8.1) Infant (19.6) N of column Percentage of total N

Mangabeyg Adult male (19.4) Adult female (38.7) Subadult male (12.9) Juvenile female

Adult female

Subadult male

Juvenile male

Infant

+/=

-

-

27.3

0

0

II

2.0

31 .O

416

71.3

I05

19.5

I

0.2

+I=

-

-

4.6

13.5 -

+

13.3

59.1

10.5

13.3

+

+ 3.8

+

-

-

-

0

100

0

-

+

0

0

-

-

-

0

100

0

0

0

34

268

70

33

I33

+

49.8

-

-

13.0

6. I Juvenile female

+

+

-

-

-

0

100

0

0

0

+ -

1.1 -

-

-

-

47.4

5.8

13.2

8.2

68.2

10.2

+

+

-

10.2

11.9

15.9

11.1

-/=

+

+

-

-

+

0

75

0

0

25

342

748

100

+

20 I

131

-

-

-

6.6

13.2

8.6

49.1

-

5

0.9

538 total N

-

0.07

I

+

1303

85.6

88

5.8

126

8.3

4

0.3

-

-

-

22.5

-

-

10.2

(16. I )

+/=

52.4

-

(12.9) Infant N of column Percentage of total N

8.7

+

+

24.7

-

25.3

-

-

-

6.3

Percentage of total N

+ 46.2

-/=

N of row

12.1

4.9

+

Young juvenile

-

1522 total N

(Continued)

TABLE XI (Continued) Groomee (recipient)

Age-sex class" Redtailh Adult male (2.9) Adult female (29.0) Subadult (8.7) Juvenile (19.8) Young juvenile (19.8) Infant (19.8) N of column Percentage of total N

Adult male

Adult female

+ + 5.5 -

0 +I=

3.2

+

20

100

+

50.8

+

Subadult

Juvenile

Young juvenile

Infant

-

-

-

-

0

0

0

0

-

-

-/=

-

2.8

+

12.7

16.6

11.6

-

-

-

0

0

0

83.3

16.7 -

-

-

-

87.1

0

6.5

3.2

-

-

0

60

0

0

+ +

-

20

-

0

-

-

-

-

-

-

0

0

0

0

0

0

12

130

6

25

31

22

+

5.3

+

57.5

-

-

2.7

11.1

~

13.7

-

9.7

N of row

Percentage of total N

-

3

I .3

+

181

80.1

6

2.7

31

13.7

5

2.2

0

0

-

-

-

226 total N

Groomee (recipient)

Age-sex class'

Adult male

Blue monkey (troop 11)' Adult male

+

(16) Juvenile

Subadult

-

Juvenile

-

100

0

+/=

-/=

+/=

0 -/=

10.5

34.5

19.5

19.9

-

-

57.0

10.1

8.8

(8.0)

Adult female (36) Subadult

Adult female

-

I .3

+

-

+

(24) Young juvenile

4.0

68.0

-

+

8.0

(8) Infant (8)

0

66.7

33.3

-

-

-

-

0

0

0

31

I87

66

N of column Percentage of total N

-

7.5

+

45.2

-

+

Young juvenile

Infant

-

-

0

0

+

3.7

20.3

2.5

-

-

-

2.0

2.0

-

-

-

0

0

0

-

-

0

0

0

68

49

13

-

+

15.9

16.4

11.8

-

12

2.9

267

64.5

79

+/= 19.1

50

12. I

+

-

16.0

-

Percentage of total N

-

12

+

N of row

-

6

1.4

0

0

-

414 total N

-

3. I ~~~

~

"Expected values are the mean percentage representation in the group of each age-sex class which are then compared with the observed percentages of ( I ) the row totals, and (2) the total sample of the group. is greater than expected by chance; = approximately equal to expected value; - is less than expected by chance; -I= is equal or slightly less than expected by chance; +I= is equal or slightly greater than expected by chance. bPercentage of row total. In brackets, the mean percentage representation in group. 'IN = 681; Struhsaker (1975, Tables 16 and 17). N = 538; modified from Oates (1974. Table 42). 'Includes two males who might be classed as juveniles. ' N = 1522; Waser (unpublished observations; bouts of >I5 sec duration). " N = 226; Stmhsaker (unpublished observations). ' N = 414; Rudran (Unpublished Progress Report No. 2, and 1976, Table 1.2).

+

1

194

THOMAS T . STRUHSAKER AND LYSA LELAND

females more than expected by chance in contrast to species with nontransient males. The functional aspect of this relationship is unclear, although it is possible that transient males groom the stable and more cohesive females in order to gain or maintain familiarity which may be of subsequent importance in reproduction. Adult females, except for bw colobus, groomed adult males more than, or as much as, expected, possibly as a function of difference in body size and dominance status. Only in redtails did adult females groom one another much more than expected by chance (Table XI). Blue and bw colobus females groomed one another much as expected. Adult female mangabeys groomed each other somewhat more (P. M. Waser, personal communication), or rather less than expected (S. Wallis, personal communication), while red colobus females groomed one another considerably less. These patterns generally reflect the interspecific differences in basic social structure. Female redtails frequentlyjoined together to defend their group’s territory; female blues less so, probably because of their larger home range and lower group density. Bw females did not defend their territories, and mangabeys rarely fought other groups. However, all of these females were the permanent core of their groups. Female red colobus, on the other hand, did not participate in group defense and seemed to be more socially mobile than the adult males. Grooming, then, appears to serve an important role in maintaining social cohesion within the group, and probably reinforces social bonds important in coordinating group defense. A perplexing question is why dependent young were not groomed more than expected (Table XI). Except for the bw colobus, most mothers were rather protective of their infants and did most of the infant grooming themselves. As a consequence, this limited the number of potential groomers and, therefore, frequency scores of any one infant. Correspondingly, bw colobus mothers were most tolerant of “aunt” behavior and their infants were groomed more than expected. Among the young juvenile class, only blues were groomed more than expected. This may be related to the fact that mother blues became more tolerant of other group members interacting with their offspring when they reached this age class, while bw colobus of this age were less attractive to other group members than when they were infants. Only subadult red colobus were groomed more than expected. Most of the data, however, concerned a subadult male who was approaching physical maturity. He was groomed very frequently by adult females, much as though he were an adult of high rank (a status he soon attained). All subadults, juveniles, and young juveniles groomed adult females more than expected (Table XI).‘ This was probably a reflection of mother-young ties, and perhaps a means of gaining familiarity with other group members. Immatures interacted less frequently than expected with the harem male, probably ‘In contrast to Waser’s data, S. Wallis (personal communication) found that juvenile mangabeys groomed adult females rather less than expected.

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

195

because of his more transient and peripheral nature. Young juvenile redtails were an apparent exception in regard to grooming, but this could be an artifact of the small sample. Juvenile mangabeys groomed adult males less than expected, and one another more than expected (also S. Wallis, personal communication). This latter relationship is in contrast to the other four species in which immature animals tended to groom one another less than expected. Only in the colobines did the subadults groom adult males more than expected. Among red colobus, this mostly involved subadult females and can be explained in much the same way as for adult females. A similar pattern may exist between juvenile and adult male red colobus, but in most cases it was not possible to distinguish between male and female juveniles. For bw colobus, however, it was the subadult male who groomed the adult male more than expected. This relationship is not readily explicable in view of the probable aggressive potential between these two classes, but it conceivably was a form of appeasement. A major point emerging from these grooming data is that the red colobus contrast markedly with the other four species. Only adult male red colobus groomed other adult males more than expected and groomed adult females less than expected. Only adult female red colobus were groomees less than expected and groomed other adult females considerably less than expected. These patterns reflect the social organization and dynamics of this species, unique in that the adult males rather than females were the stable element of the group.

D.

SEXUAL BEHAVIOR

Copulations between adult males and adult females were seen very infrequently in the harem groups (Table XII). They were possibly seasonal in redtails and blues, but apparently not in bw colobus. Most of the females in the main bw colobus group were either pregnant or lactating during the study and this probably contributed to the low incidence of copulation seen in the group. Copulation was relatively common in the multimale groups of red colobus and mangabeys. The distinction is often made between single and multiple mounters, referring to whether the adult male ejaculates on nearly every sexual mount (single mounters) or whether a series of nonejaculatory mounts precedes the ejaculatory mount (multiple mounter^).^ Of the five species, only mangabeys tended to be single mounters, although they appear intermediate to the two extremes. Harassment by immatures of the copulating pair was observed in all species. Adult females never harassed copulating pairs. Only in red colobus did adult males regularly harass the pair through approaches and vocal displays. Physical 'An example of a single mounter: of 6 I mounts, 95% ended in ejaculation (vervets, Stmhsaker, 1967b); a multiple mounter: ejaculation preceded by 3 to I 0 0 incomplete mounts, i.e., one to 25% of the mounts included ejaculation (rhesus, Carpenter, 1942).

196

THOMAS T. STRUHSAKER A N D LYSA LELAND TABLE XI1 SUMMARY OF SEXUAL BEHAVIOR Red colobus"

bw Colobusb

Mangabey'

Redtailn

Harem

No

Yes

No

Yes

Yes

Multimale

Yes

No

Yes

No

No

Sexual swelling

Yes

No

Yes

No

No

Relative frequency of copulation complete and incomplete

117 h r N = 1113 hr 20 nio

Percentage of adult male/ adult female copulations with pause (presumed ejaculation)

18.7% N = 160

Multiple mounters

1/81 hr

- 1/10 hr

1/102 hr

N

N

N

=

888

=

557 hr

=

609 hr

Blue'

11228 hr N = 911 hr

hr 15 mo

10 mo

16 mo

10 nio

9.1%

N =II

77.3% N = 54

16.790 N = 6

42.9% N = 21

Yes

Yes'?

No

Yes

Yes

Harassment by adult males

Yes

N0

No

No

NO

Harassment by immatures

Yes

Yes

Yes

Yes

Yes

"Slruhsaker (1975). hOates (1974. 1977~). "FF group; Wallis (personal communication) rl Struhsaker (unpublished observations) "Rudran (unpublished Progress Report No. 2 and personal communication).

contact with the copulators was made only by immature harassers, sometimes resulting in a forced dismount. There was no perineal swelling or other visible morphological feature associated with estrus in the harem-living species-bw colobus, redtails, and blues. Females in the multimale species of red colobus and mangabeys did, however, have sexual swellings of the perineum associated with estrus. The harem male did all of the copulating in the main study groups of bw colobus, redtails, and blues. In another study group of redtails in the Ngogo area of Kibale, there was a partial exception to this generalization during a multimale influx when five extra-group males temporarily immigrated into the group and copulated with females, most of whom were immature (Struhsaker, 1977).

SOCIOECOLOGY OF FIVE SYMPATRlC MONKEY SPECIES

197

The copulation frequency of the adult male red colobus was directly related to their dominance status (priority of access to space and food) and agonistic relationships with other males. Both this relationship and differential reproductive success among the adult male mangabeys were less prominent than in the red colobus or lacking (P. M. Waser and S. Wallis, personal communication). However, in times of instability or transition in the dominance hierarchy, the distribution of copulations among male red colobus was less skewed than when the hierarchy was established and stable. During one unstable situation, two to three male red colobus copulated with the same female in the same estrous period. Among mangabeys, Waser (1977a) reports that one particular male out of the three in his main study group was the principal copulator (66% of all copulations). Both P. M. Waser and S. Wallis (personal communication) have found that at least two to three males can copulate with the same female in the same estrous period. Females in estrus may create an unstable situation in multimale groups as aggression between males is most prominent at this time (S. Wallis, personal communication). The role of chief copulator has shifted from one male to another in the main study group of red colobus and in both Waser’s and Wallis’ main study groups of mangabeys. In the case of the red colobus, this role was assumed by a young male who was born in the group; among mangabeys. it involved older males whose parental groups were not known (P. M. Waser, personal communication).

E.

SOCIALINTERACTIONS OF NEONATES (AUNTBEHAVIOR)

The infants of all five species have a neonatal appearance distinct from that of adults in terms of color, pelage texture, and in having pink faces and ears. This appearance, however, differs in degree, with bw colobus infants having the most distinct coloration, and mangabeys and blues the least. Nonmother females and immatures in all species showed some interest in neonates, but whether they contacted the infant and the extent to which they interacted with it depended on the degree of permissiveness on the part of the mother. The five species can be ranked according to the degree of friendly social interaction (handling, grooming, muzzling, pulling, and carrying) between the neonate and other group members as follows, from greatest to least: bw colobus, mangabey, redtail, blue, and red colobus. Much attention and contact was given to the white newborn bw colobus infant by females other than the mother. Neonates were taken away from the mother, groomed, handled, etc. most frequently in the first two weeks of life. Attention was given primarily by other adult females, but subadult males and females, juveniles, and young juveniles also attended neonates. A minimal estimate of the frequency of incidents of extramother handling of neonates was one per every two hours, and may be as high as three to five incidents per hour (Oates, 1977~).

198

THOMAS T . STRUHSAKER AND LYSA LELAND

Mangabey infants are black at birth but have distinct pink faces and ears. P. M. Waser (personal communication) never saw infants being carried by nonmothers within two weeks of birth although attempts to carry and groom the infants clinging to the mother were common during this period. An important qualitative distinction from the other four species is that adult males sometimes ventrally carry infants of one month or older and, occasionally, in situations apparently involving agonistic buffering (P. M. Waser, personal communication; T. T. Struhsaker, personal observations). Chalmers (1968) also reports extensive contact and carrying of infants 2.5 to 5 months old by adult males. Infants were neither carried nor contacted by adult males in any of the other species. Newborn redtails commonly had physical contact with other group members in the first month of life and sometimes in the first week. In 16 clearly observed cases involving 18 nonmothers and infants aged one month or younger, adult females were attendants in 34.4% (more than expected) of the cases, subadult females 5.6% (as expected), juveniles 45.5% (much more than expected), and young juveniles 16.7% (slightly less than expected). The neonate was taken away from the mother in 31.3% of the above cases. Adult female redtails also defend one another’s neonates against the attacks of a new harem male following male replacement in the group (Struhsaker, 1977). The following account for blues has been kindly provided by R. Rudran (personal communication): ‘‘Infants under two weeks old are generally tended to only by their mothers. Other members of the group (mainly subadult females) sometimes attempt to muzzle and groom the infants, but this is resisted by the mother either through threat gestures or vocalizations. Mothers of young infants tend to associate more closely together than with adult females without infants. In these associations infants may make contact and sometimes wrestle and grapple with each other. At about two months of age the infant may be groomed by adult females other than its mother and older siblings, but it still remains very close to the mothei. The mother sometimes allows one of its older offspring to carry the infant a considerable distance away when it is about six months or older. Play between the infant and small juveniles is also common during this time.” Only juveniles and young juveniles approached and attempted to touch red colobus neonates, but the mothers drove them off by threats, which mostly consisted of facial gestures and lunges. Not until the infant was 1 to 2, or even 3.5 months old did it make physical contact with other group members, usually with age peers when playing, and, even then, it was infrequent. Those species in which the females constituted the most permanent membership in the group and who were presumed to be closely related tended to show the greatest degree of aunt behavior. Presumably, neonate handling by adult and young females relates to their greater solidarity and enhances the social bonds between them. This increased familiarity may not only contribute to greater

199

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

stability in their group membership, but in some species may also contribute to the social bonding important in defense of territory or of one another’s infants against potential infanticide by new harem males. These arguments, however, do not explain some of the interspecific differences in the degrees of aunt behavior, or why, among adult males, it is only the mangabeys who handle and carry infants.

F.

INTERGROUP RELATIONS

The main study group of red colobus had extensive to complete range overlap with two other groups, and partial overlap with another two to five groups of red colobus (Table XIII). Relations between these groups varied from extreme intergroup tolerance at close quarters to intense aggression. Among the three groups having complete range overlap, interactions included subtle and slow forms of spatial supplantation of one group by another; occasionally it appeared that one group was simply following the other. There was a dominance hierarchy among these three groups which seemed to be based on the number of adult males in the group, their physical condition, and their fighting ability and propensity. These relations were independent of spatial parameters and there was no indication of territoriality. Adult males of adjacent groups exchanged vocalizations in apparent bouts of counter calling which may have influenced intergroup spacing. Only the adult and subadult males played offensive roles in intergroup conflicts; adult females and immature monkeys usually avoided these episodes. TABLE XllI SUMMARY OF INTERGROUP RELATIONS

Overlapping ranges Defended boundaries Areas of exclusive use in range Participants in conflicts

Usual nature of encounters

Red colobus

bw Colobus

Mangabey

Redtail

Blue

Complete No N0

Extensive Yes Perhaps

Extensive No Yes

Very little Yes Yes

Very little Yes Yes

All

All

All

Adult and Adult and subadul t subadu It males males Variable: Aggressive tolerant to aggressive ? Yes

Adult male loud call important in spacing Adult male counterYes calling (excluding response to predators)

Yes

Mutual Aggressive Aggressive avoidance Yes

?

Yes?

Yes

NO

N0

200

THOMAS T . STRUHSAKER A N D LYSA LELAND

The bw colobus study group had extensive home range overlap (at least 74%) with five neighboring groups. The core area of this group, although defended, was also used by other groups (Oates, 1974, 1977~).Thus, in the sense of defending an area in its home range, this group can be considered territorial, but not in the sense of exclusively occupying an area. The main study group may have been atypical in this respect as most other (shorter-term) studies (e.g., Schenkel and Schenkel-Hulliger, 1967; Marler, 1969, 1972; Dunbar and Dunbar, 1974) found that social groups occupied near-exclusive territories. A large swamp in their home range accounted for much of the intergroup overlap and appeared to be a “neutral” area which apparently contained an essential resource in the form of aquatic plants (Oates, 1978). This resource was required at relatively long intervals in small amounts and was of sufficient quantity to satisfy the needs of several groups. The majority of intergroup interactions were aggressive and involved only the adult and subadult males. The main study group interacted differently with different groups at the same site, but there were apparent “dominance” relations between them. Neither group size nor the number of adult males in the group influenced the outcome of these encounters. The “contagious” adult male loud calls were probably important in intergroup spacing (Oates, 1977~). There was extensive home range overlap between adjacent mangabey groups. These groups.tended to avoid each other throughout their home ranges. Although there was a central area of exclusive use in the home range, this was the result of avoidance rather than defense. There was not a single core area of intensive use, but rather several such sites scattered throughout the home range. Only six intergroup encounters were observed in more than 2500 hours of observation. Three of these consisted only of an adult male from one group approaching another group; there was no overt aggression in two cases, and once the approaching male was chased away by several group members. In the other three cases, two groups actually came together; once they remained 50-100 m apart without visible threats, and twice there were prolonged (for at least three hours) aggressive interactions with chases, counter-chases, many loud calls, and possible physical contact but no decisive outcome. Adult male loud calls played a major role in effecting intergroup spacing (Waser, 1976). The intergroup relations of redtails and blues were very similar. They differed primarily in that redtails fought with other groups more frequently, perhaps as a consequence of a smaller home range and a higher density of groups. Only 13 aggressive interactions were observed between groups of blues in 2 100 hours of observation (Rudran, 1976). All independent group members of both species participated in the defense of rigid territories against neighboring groups. The harem male was no more prominent in this activity than any other group member, contrary to the claim of Clutton-Brock and Harvey (1976) that “. . . in most territorial primates, it is the male who is largely responsible for defense. . . .” These encounters involved threat gestures, chases, and aggressive vocalizations;

SOCIOECOLOGY OF FIVE SYMPATRlC MONKEY SPECIES

20 1

physical contact was not seen. Groups did range outside of their defended boundaries, but there was little home range overlap. The loud calls of adult males may have effected intergroup spacing, but neither this nor counter calling between groups was prominent.

G. SECTION SUMMARY Several of the interspecific differences presented in this section on social behavior appear to be related to the extent of male-male tolerance. For example, female-female cohesiveness, especially in terms of grooming and tenure in the group, is least pronounced in the red colobus where male-male tolerance is greatest. Grooming among adult males is prevalent in red colobus but not in mangabey groups where males tended to be more transient. Aunt behavior toward neonates is very rare in the red colobus compared to the other 4 species.

VI. DISCUSSION A.

FOODIN RELATIONTO GROUPSIZEA N D SPACING

Food is generally cited as one of the principal factors influencing group size and spacing. The various aspects of food, however, must be clearly delineated before there is any chance of discerning detailed relationships. Food availability is usually seen as determined by the environment. However, it is important to take into account both the physiology and anatomy of the consumer species concerned (Klein and Klein, 1975). For instance differences in the digestive system will strongly influence what kinds of food an animal can eat, in terms of detoxification and digestion (e.g., polygastric vs monogastric). Nutritional requirements and dietary complement will dictate the variety of foods essential to the animal. Furthermore, body size will influence both the type of food an animal can exploit and the amount consumed. Learning capabilities and manipulative dexterity have also been related to food availability (e.g.. Japanese macaques, Itani, 1958; chimpanzees, Goodall, 1965; capuchin monkeys, Struhsaker and Leland, 1977). Food availability must also be viewed in terms of its distribution in time and space. The temporal considerations should include both annual and superannual fluctuations of different food sources, and irregular and infrequent periods of food scarcity. Relevant spatial parameters include not only how the resource unit is distributed in the habitat, but, as Klein and Klein (1975) have pointed out, how the food items are distributed on the resource unit (e.g., leaves vs a small clump of fruit) and the size of the unit itself (e.g., tree crown).

202

THOMAS T . STRUHSAKER A N D LYSA LELAND

1 . Food and Intraspecijic Variation in Group Size

Within some monkey species, there is strong indirect evidence that group size is primarily related to food density and availability in a gross sense. For example, populations of red colobus living in marginal habitats, such as gallery forests or guinea savanna with relatively low food density and diversity (Struhsaker, 1975; Gatinot, 1975; C. Marsh, personal communication), have groups about half the size of those in rain forests. Chacma baboons living in the food-rich Okavango Swamp have groups two to four times larger than those living in the impoverished Namib Desert (Hamilton et a l . , 1976). When food resources in a habitat are drastically altered due to artificial or natural conditions, changes in group size are particularly evident. Essentially unlimited provisioning of semiwild macaques has resulted in enormous increases in group size (Koford, 1956; Itani et a l . , 1963). Although the data are few, counts of redtail, blue monkey, and mangabey groups in selectively timbered parts of Kibale show them to be nearly half the size of groups living in adjacent but undisturbed forest (Rudran, 1976; Struhsaker, unpublished observations; P. M. Waser, personal communication). A natural increase in the mortality rate of major food trees in Amboseli, Kenya has led to a decline in the vervet populations and group size (Struhsaker, 1973, 1976). In the case of the vervets, much of the decline appears due to poor suvivorship in the young juvenile class, apparently suffering high mortality in the year after they are weaned. This also appears to be the case for blues, the Senegal red colobus (Gatinot, 1973, and possibly for redtails and the Tana River red colobus (C. Marsh, personal communication). Fecundity remains high in all these populations. A reduction in food supply andor quality is responded to, not by a reduction in reproductive effort, but rather by an increased mortality in the young juveniles. Under ecologically poor conditions, the Amboseli baboons suffer high infant mortality during the first year (Altmann et a l . , 1977). Homewood (1976) has suggested that reduced fecundity may occur in the Tana River mangabey (Cercocebus g . galeritus) under natural conditions of overcrowding or poor nutrition. 2. Food and Interspecijic Differences in Group Size and Spacing

Klein and Klein (1975) have compared the socioecology of four sympatric neotropical primates: the spider monkey (Ateles belzebuth), the squirrel monkey (Saimiri sciureus), the capuchin monkey (Cebus apella), and the howler monkey (Alouatta seniculus). This comparison has several parallels with that made of the five Kibale species. The following section will compare the food habits of these sympatric species and attempt to show how they relate to differences in group size and spacing. In both of these forest habitats, predation pressure was minimal and considerably less than in African savannas. Sleeping sites and water supplies were unlimited and therefore were not considered in the comparisons.

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

203

The smallest Kibale monkey, the redtail, resembles the squirrel monkey: both live in relatively large groups (25-35 for the squirrel monkey), achieve high biomass densities, and heavily rely on catching mobile arthropods. The small body size of these two species may be related to their foraging efficiency and food requirements: They are quick, agile, and alert and spend much of their time continuously moving in search of insects. Reliance on such small but highprotein food sources commonly found on foliar substrates may allow small monkeys to form large groups in a relatively small area. These food sources also seem to be uniformly distributed, and in such a manner as to enable all members of a group to forage together with a medium to wide group spread (over 46 to 91 meters for the squirrel monkey). The largest Kibale omnivore, the mangabey, is most comparable to the spider monkey in terms of body size, social group size (1 7 to 22 for the spider monkey), wide group spread, and heavy reliance on fruit. Larger, and therefore heavier, monkeys appear more restricted in the foods they exploit than the smaller omnivores and require greater amounts. They are more dependent on fruit resources. A larger body size, however, does have distinct advantages: both mangabeys and spider monkeys (Klein, 1974) have been observed to supplant smaller species from fruiting trees; and mangabeys were able to exploit arthropods in microhabitats, such as dead wood and bark, often requiring a great deal of strength. These microhabits are widely dispersed, small in size, and therefore usually exploited by only one individual, and generally destroyed in the process of exploitation. These microhabits are similar in nature to palm fruit which was a common food of the spider monkey, especially when other fruits were scarce. This fruit was found in small clusters in trees which were widely dispersed rather than clumped, and had small crowns. As a result, only one monkey could feed in a tree at a time, and would usually consume all the ripe fruit. Aggression was most likely to occur over such small food units. Sussman and Richard (1974) in their study of Malagasy lemurs also point out that aggression was more likely to occur when food units were of limited size and not necessarily related to overall food availability. The Kleins concluded that palm fruit was a central factor in understanding the spacing patterns and social organization of the spider monkey which appears to avoid aggression by “maximal dispersion and minimal association. ’* Spider monkeys are usually found singly or in subgroups of two to three animals with a group spread of over 800 m. Mangabeys, on the other hand, although often having a wide group spread and medium to wide interindividual distance for foraging and searching for food (e.g., arthropod microhabitats) were more dependent on superabundant fruit which often occurs in trees with large crowns (e.g., figs) allowing all or most members of a group to feed in one tree simultaneously. Thus, the size of the basic resource unit and the distribution of both the unit in the habitat and the food in the unit itself will play an important role in group spacing and accounts for the principal difference between the group struc-

204

THOMAS T . STRUHSAKER A N D LYSA LELAND

ture of mangabeys and spider monkeys, i.e., whether the group can forage together or must maintain small widespread subgroups. In the case of spider monkeys, potential aggression over food (quantity) appears to be an important factor in determining spacing. Mangabeys were rarely seen to aggress over food except in an area of recent and extensive timber removal and thus, presumably, of food depletion (Chalmers, 1968). The third Kibale omnivore, the blue monkey, is intermediate in body and group size to the redtail and mangabey. It depends more heavily on relatively immobile insects than the redtail and less heavily on superabundant fruits than the mangabey, but is more folivorous than these two omnivores. Similarly, the capuchin monkey is intermediate to the squirrel and spider monkeys, both in body and foraging group size (6 to 12), in group spread (183 m), and in its more opportunistic diet which consists of immobile insects and fruit, including palm fruit. In contrast to the more specialized spider monkey, however, the capuchin can forage in larger units because of its more diversified diet which allows its members to feed on different foods in the same location. Aggression over food, when occumng, appeared to be over quality rather than quantity. Of the Kibale omnivores, the redtails and blues tended to aggress more in the context of food, and like the capuchin, this may have been related to food quality. The howler monkey has the smallest social group size (3 to 6), the smallest group spread (15 to 30 m), and is the most folivorous of the four species in the Kleins’ study. Aggression was infrequent and not seen in the context of food. Although fruit was an important component of the diet, the predominant fruit were figs which were found in superabundance in trees of large crowns. The howler, then, appears most similar to the folivorous bw colobus which also has the smallest group size and spread of the Kibale species. The density and dispersion of their food allows the members of a group to feed simultaneously in the same tree without aggression and without the need to forage or to move long distances in search of food. Aggression over food was rarely seen in the two Kibale folivores. Only when feeding on a choice and very limited resource, such as a dead tree stump, did fights occur in a red colobus group. The red colobus, for which there was no apparent primate equivalent in the Kleins’ study, is folivorous like the bw colobus. In contrast, however, it attains a larger group size and higher biomass density than the bw colobus or any other Kibale species. This may be explained in that half the annual diet of the bw colobus consists of only one plant species, while half the diet of the red colobus consists of five plant species, with the most common food species of red colobus comprising only 15.4% of its annual diet. The density of these five red colobus food species was rather more than twice that of the one species of the bw colobus (Struhsaker, 1975). Presumably the digestive and detoxifying capabilities of red colobus allow it to exploit the vaned array of rain-forest plant species more fully

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

205

(greater dietary diversity) than the bw colobus and, therefore, it can live in larger but still cohesive groups. Group size of bw colobus is relatively stable in differing habitats and this may be related to its limited digestive and detoxification abilities. If these abilities are presumably very limited in bw colobus, then the foods available to it will also be limited regardless of habitat diversity and, correspondingly, group size may be expected to be similar in many different habitats. On the other hand, the variations in size and density of groups of red colobus may be attributed more to the density and diversity of food in different habitats. For instance, red colobus in Kibale (a relatively species-rich and aseasonal habitat) form large groups with extensive overlap in home range; in the poorer Gombe habitat (more pronounced seasonality and possibly lower plant-species diversity), red colobus form large groups, but range overlap between groups is minimal (Clutton-Brock, 1972); in the poorest and most seasonal habitats on the Tana River (C. Marsh, personal communication) and in Senegal (Gatinot, 1975), they form smaller groups with little range overlap. In summary then, the Kibale omnivores showed an inverse relationship between body and group size, and a direct relationship between body and homerange size. Similar trends are suggested by the spider, capuchin, and squirrel monkeys which were the least folivorous of the species studied by Klein and Klein ( 1975), although here we must consider foraging-group size in relation to body size rather than total social-group size. The largest omnivores relied most heavily on fruit resources which were generally of low density, had wide patterns of dispersion, and low renewal rates. Dependence on such dispersed food resources would require a large home range and relatively small foraging groups, the size of which will greatly depend on the size of the basic food units. The smallest monkeys had the largest group size and the smallest home range, probably due to their greater dietary diversity and foraging efficiency for mobile arthropods. The species intermediate to the others were the most opportunistic. Body size in the omnivores appears to be related to how the animal can exploit the environment and the amount of food required; these factors, in turn, may influence the size of the home range and the foraging group. Spacing patterns appear to reflect both the density and dispersion patterns of foods and the foraging strategies most effective in exploiting them. Folivores have the most compact group formation and closest interindividual distance because leaves occur in the greatest densities on any one resource unit. A highly varied diet of abundant foliar foods will allow a larger group size. Nonfoliar foods, such as fruits and insects, which are more widely dispersed and found in smaller densities, will necessitate wider interindividual spacing for efficient exploitation. Spacing in each species will vary according to the nature of the basic food sources themselves and the variety in the diet (Klein and Klein, 1975).

206

THOMAS T . STRUHSAKER AND LYSA LELAND

3. Fusion -Fission Societies Fluctuation in interindividual spacing and subgrouping is also a function of food density and dispersion and often related to seasonality: when food is plentiful, a group can feed together; when scarce or widely dispersed, the group will divide into foraging units, not only to find food resources more efficiently, but also to minimize direct competition when these sources are located. Homewood’s (1976) study of the Tana mangabey shows an inverse correlation between intragroup dispersion and food availability. Chimpanzees (Reynolds and Reynolds, 1965; Sugiyama, 1973; Wrangham, 1975) and hamadryas baboons (Kummer, 1968) also illustrate these subgrouping tendencies. These subgrouping tendencies take various forms. Chimpanzees and spider monkeys, for instance, are usually seen in small subgroups which will often vary in size, composition, and individual membership, but all members of a group are rarely seen together at one time. On the other hand, hamadryas baboons (Kummer, 1968, 1971) and geladas (Dunbar and Dunbar, 1975) have three levels of organization: the one-male group (harem) which is the basic social unit; the band, consisting of a stable number of harem groups; and the troop (or herd), made up of a variable number of bands. The greater majority of friendly interactions involve members of the same harem with a minority occurring between other band members. Bands either show neutral tolerance or fight one another. A single harem group of hamadryas is of the optimal size for feeding on single isolated Acacia trees; bands are able simultaneously to exploit Acacia groves consisting of ten or more trees, and the troop can drink from the same waterhole and use the same sleeping cliffs. The term “fusion-fission” is used to describe the social organization of these species where animals come together when the resource can support many of them, and disperse when the resource is dispersed. If this is the main criterion of a fusion-fission society, there are a great many more examples among primates. For instance, during the dry season, vervet groups aggregate at common waterholes (Struhsaker, 1967a), as do groups of patas monkeys (Struhsaker and Gartlan, 1970), while during wetter periods they are more widely dispersed. Groups of Tana mangabeys aggregate in times of fruit abundance and disperse widely when it is scarce (Homewood, 1976). Groups of red colobus in Kibale frequently move together and then disperse, probably in relation to food (Struhsaker, 1975). Troops of yellow baboons will share the same sleeping-tree groves at night and disperse during the day (Altmann and Altmann, 1970). Similarly, the large talapoin group disperses in small subgroups during the day and congregates at night in the sleeping lodges along the river banks (Gautier-Hion, 1970; Rowell, 1973). In other words, the concept of fusion-fission society as it now stands, with emphasis on spatial separation and reunion, could probably be applied to most primate species and is therefore of limited value. Clearly, then, a more stringent operational definition is called for if the concept is to be retained.

SOCIOECOLOGY OF FIVE SYMPATRlC MONKEY SPECIES

207

Based on empirical data, members of a fusion-fission society are ( I ) of the same social network' (Struhsaker, 1969). All members of the social network will disperse; (2) as units or individuals, and/or in variable combinations of associations of units or individuals; (3) generally for the major part of a day, but often for much longer; and (4) over distances approximately 1/4 to 1/2 the maximum linear distance of their home range. This definition would include chimpanzees, spider and talapoin monkeys in terms of individuals; and hamadryas and geladas in terms of basic social units (harems). The band of hamadryas and geladas, but not the troop or herd, would constitute a fusion-fission society in this definition. 4 . Food in Relation to Intergroup Spacing

The spacing patterns between social groups of a species are often clearly related to patterns of food density and dispersion. High food density with an even dispersion can be expected to favor the development of territories (Crook, 1970; Crook et a l . , 1976). We would add that a high renewal rate of food is also an important factor favoring territoriality. Territories must contain adequate resources to support the group during the most critical periods of resource scarcity, whether on an annual or superannual basis. Thus, in some cases, the importance of territoriality may not become apparent until food is scarce which may occur only at long and irregular intervals (e.g., Propithecus, Richard, 1974a). Crook (1972) and Goss-Custard et al. (1972) have emphasized that primate territories can occur only where all requirements exist within a defendable area. It has been suggested that territories minimize intraspecific competition (e.g., Goss-Custard ef a l . , 1972). More precisely, territories are the result and expression of intraspecific competition. The defense of an area and its resources to the exclusion of other groups of conspecifics is a form of highly successful competition. Territoriality brings order to the competition for resources in such a way as to increase the efficiency of resource exploitation, which, in turn, improves foraging efficiency. The action of territorial defense or display can be viewed among other things as a form of competition for food. The above hypotheses appear to fit the results from Kibale with but few exceptions. For example, territorial defense by the small and cohesive bw colobus groups appears to be adapted to the efficient exploitation of a monotonous diet whose chief component occurs in high densities with a uniform distribution and supplies food throughout the year (Struhsaker and Oates, 1975). However, some bw colobus groups share a swamp which constitutes a neutral ground, much as waterholes are shared by territorial groups of vervets (Struhsaker, 'Individuals of the same social network have the majority (at least 80%) of their nonaggressive social interactions within this social network. A given individual does not necessarily interact with all members of its social network, but is linked. at least indirectly, with all other members. For example, see the sociograms in Kummer (1968) and Dunbar and Dunbar (1975).

208

THOMAS T . STRUHSAKER AND LYSA LELAND

1967a). Finally, it should be emphasized that the territories of the bw colobus studied at Kibale did not contain areas that were used exclusively by any one group. Philopatry and defense of exclusive territories presumably increase the animals’ ability to predict resource location through familiarity both with the area and with recent food exploitation which, in turn, increases their foraging efficiency. This would be especially important when dealing with food items that are sparsely distributed as small single units and require a relatively great amount of search time, such as some kinds of arthropods. This situation is particularly true of the redtails which forage for phytophagous insects and fruits of optimal ripeness. By defending an exclusive territory, a group can remember which areas have been exploited for what, and when. Blues are also territorial and, like the redtails, experience periods of fruit and possibly insect shortage when territoriality may assume additional importance. Occasionally groups will trespass into one another’s territories. Presumably these incusions are to exploit prime resources that are unavailable or in low supply in their own territory. The effect will also be to conserve food supplies within their own territories. The extent and frequency of trespassing and, thus, the degree of exclusivity of these areas under a given set of visibility conditions depends on the daily or short-term ranging patterns which in turn are related to the kinds of food exploited, their distribution and renewal rates. For example, in a period of five consecutive days, a redtail group will cover about two thirds of its territory in search of food. Correspondingly, intrusions into their temtories by neighboring groups of redtails were neither frequent nor extensive. In contrast, the bw colobus have relatively short daily and 5-day ranges, probably because their food requirements are uniformly distributed in high densities and much of their time is spent resting. As a consequence, incursions into neighboring territories are both frequent and extensive (Oates, 1977c; P. Marler, personal communication). Large home ranges are incompatible with effective territorial defense (see also Goss-Custard et a l . , 1972; Crook, 1972). “Large” in this sense must be viewed in relation to the species’ daily or short-term movement patterns. Species which must rely on widely dispersed food resources to satisfy their food requirements throughout the year live in large home ranges and cannot or do not efficiently defend territories: e.g., mangabeys (Waser, 1975a, 1976), chimpanzees (Wrangham, 1975), and most savanna baboons (Hamilton et ul., 1976). In these cases, although neighboring groups may behave aggressively to one another when they do meet, the home ranges are sufficiently large that range overlap is extensive without frequent intergroup confrontation. In mangabeys, avoidance is effected through loud calls (Waser, 1975a). Shape as well as size of a range may be important in determining the defensibility of an area as illustrated by the study of two populations of chacma baboons

SOCIOECOLOGY OF FIVE SYMPATRlC MONKEY SPECIES

209

(Hamilton et a l . , 1976). Where baboon groups occupied linear ranges, overlap was common and extensive since the groups were often several kilometers away from border areas for days at a time. Baboons living in somewhat smaller and nearly rectangular ranges were usually within hearing distance of at least one boundary and generally approached all boundaries daily. Correspondingly, zones of intergroup overlap were less extensive, and, presumably, incursions less frequent than in the linear habitat. The Kibale red colobus have extensive intergroup overlap in ranging, not because the home range is too large to defend (equivalent in size to the defended territory of a blue monkey group) but rather because on a quantitative basis there is apparently enough food for several groups in the same range. Dietary complement or qualitative food requirements like trace elements probably dictate the home range size. Thus, in terms of bulk alone any one section of the home range may contain enough quantity of food to support the group, but to obtain a balanced diet the group must go to other parts of the range for other food types. Foraging predictability seems to be less critical for a folivore like the red colobus whose specialty of young foliage from a wide variety of species occurs in high densities and requires minimal search time and effort. Consequently, there is little advantage in defending territories. In more seasonal habitats and less diverse plant communities, intergroup overlap is much less pronounced and the groups rarely come close to each other (e.g., Clutton-Brock, 1972; Gatinot, 1975; C. Marsh, personal communication). In these areas the carrying capacity appears to be lower than in Kibale and can support only one group in a given area. It is still unclear why the groups of red colobus with completely overlapping home ranges in Kibale do not unite into one group. Possibly it is a matter of some subtle factor of feeding ecology or a function of social factors such as the optimal group size for maximizing the reproductive success of individual high-ranking males.

DYNAMICS

B.

GROUP

I.

Group Composition

In all five species studied at Kibale, there is an obvious discrepancy from unity in the adult sex ratio, a pattern typical of most primate species. Although data on sex ratios at birth or even for the young juvenile class are not available for these species, it is probably correct to assume the ratio is one to one. Some of the males are either forced out of a group or leave voluntarily as they approach sexual and physical maturity, particularly in harem species (e.g., Bourliere e t a f . , 1970). A solitary existence may result in higher mortality rates among these old juvenile and subadult males, but there are no data on this. Am0r.g the red colobus, and

210

THOMAS T . STRUHSAKER AND LYSA LELAND

possibly the other four species as well, the older juvenile males suffer higher mortality rates than the females either through stress or wounds when harassed and attacked by the adult males, but again supportive evidence is lacking. Differential rates of maturation in relation to longevity may account for some of the divergence from unity in the adult sex ratio, as it apparently does for baboons (e.g., Altmann et a l . , 1977) and rhesus macaques (e.g., Catchpole and van Wagenen, 1975). Captive data for mangabeys (C. albigena) suggest that females attain body weight 6-12 months earlier than males and that the discrepancy is rather greater (1-2 years) for C. nicrirans, a close relative of blue monkeys (Gautier-Hion and Gautier, 1976). Furthermore, Oates (1974) presents a hypothetical argument that the disperate adult sex ratio among bw colobus can be accounted for largely on the basis of differential rates of maturation. However, at present we are unable to specify the relative contributions of these factors to the excess of adult females over males in the study populations of our five species.

2. Social Mobility (Migration between Social Groups) What determines the age and sex class that is most socially mobile in a species? Although probably all species show both male and female mobility, many of them can be categorized as to whether the males or females are the most mobile element in the society. Outbreeding, as suggested by Clutton-Brock and Harvey (1 976), may be the ultimate factor in both categories, and intrasexual competition the proximate factor, but the dichotomy remains to be explained. In a harem system there is inevitably more mobility in males than in females, probably as a result of male-male intolerance. In the extremely small harems of hamadryas and geladas, however, both juvenile males and females frequently leave their parental harem (Kummer, 1968; Dunbar and Dunbar, 1975). In multimale groups, the predominantly mobile sex seems inversely related to which one engages in intrasexual cooperative actions and/or integrated and friendly social behavior. In the two species with multimale groups studied at Kibale, the adult males were the most mobile element in the mangabey groups, and the juvenile females in the red colobus. Adult male red colobus, the more permanent members of the group, showed the greatest degree of cooperative or integrated and coordinated behavior of benefit to themselves, their offspring, and mates, while the male mangabeys showed little cooperative action of this sort. A possible exception to this generalization may be the savanna baboons where in some areas the males appear to “cooperate” in group defense against predators, but are the mobile element (Hall and DeVore, 1965; Altmann and Altmann, 1970; Hausfater, 1975). In some other areas, however, they appear not to defend the group and are still the mobile element (Rowell, 1972b). Male movement out of the group would be adaptive in that the emigrant may achieve greater reproductive success in another group where competition is less intense (Clutton-Brock and Harvey, 1976) or there may be more females in estrus

’

SOCIOECOLOGY OF FIVE SYMPATNC MONKEY SPECIES

211

(see also Goss-Custard et a l . , 1972). This may prove to be especially true of young adult andor low-ranking males. Hausfater’s (1975) study of yellow baboons suggests that adult males of any dominance status may emigrate from their multimale groups, but that the propensity to do so is greater among low-ranking individuals. The case of females leaving their parental group to join another group is less clear. Few primate species other than the red colobus show this pattern: e.g., mountain gorillas (Harcourt et al., I976), chimpanzees (Nishida and Kawanaka, 1972; Wrangham, 1975), hamadryas (Kummer, 1968), and possibly geladas (Dunbar and Dunbar, 1975). In the case of hamadryas, and perhaps geladas, it appears that the young female is taken away from her parental group by an extragroup male rather than her leaving “voluntarily.” In the multimale groups of red colobus and chimpanzees, the young females seem to leave of their own accord. Among the gorillas, which form small, predominantly one-male groups, both immature males and females leave their natal groups, with females tending to join solitary males or “new groups’’ (Harcourt et af., 1976; Harcourt, personal communication). The suggestion by Clutton-Brock and Harvey (1976) that female mobility is most likely to occur in species in which genetically related males form “breeding cooperatives” seems applicable to red colobus and chimpanzees but not to hamadryas, geladas, and gorillas. In the main red colobus study group, which was smaller than the average size, female emigration was an uncommon event although immigration of young females was relatively frequent. Why young female red colobus leave their parental group is uncertain. Proximate factors may conceivably involve intrasexual competition. However, many of these young immigrant females were not sexually mature; intragroup estrous synchrony is not pronounced in red colobus, and the dominant male was seen on some occasions to copulate with as many as three different females in a period of two consecutive days. Therefore, competition for mating opportunities with the dominant male seems an unlikely determinant of female mobility. Selection for outbreeding combined with the absence of any pronounced cooperative activity on the part of female members of red colobus groups may explain much of their propensity to emigrate and immigrate. In all of the other four species studied at Kibale there is a greater cohesion among the females of a group, such as in unified defense, aunt behavior, or grooming relations. Red colobus females are notably lacking in these kinds of cohesive behaviors.

SUCCESS C. MALERELATIONSA N D REPRODUCTIVE

In harem species, Crook and Gartlan (1966) have suggested that exclusion of all males but one from the heterosexual group is adaptive in that it reduces intersexual competition for food, thereby allowing more for adult females re-

212

THOMAS T . STRUHSAKER AND LYSA LELAND

sponsible for rearing young. In addition, there would be more food available for the harem male and his offspring. For this strategy to be effective, however, both direct and indirect competition between extragroup males and the harem must be avoided, which under most conditions would necessitate geographical as well as extragroup separation (Crook, 1972; Goss-Custard et al., 1972; Dunbar and Dunbar, 1975). Although intuitively appealing, this hypothesis has very little supporting evidence. In all rain-forest species so far studied, extragroup males are not geographically segregated from reproductive groups, nor is there any evidence that they use different food resources. It appears that extragroup males use a larger range than harem groups, possibly to monitor other groups. Likewise, the studies of open-country species fail to support Crook and Gartlan’s hypothesis. Kummer’s (1968) study of hamadryas baboons clearly implies that nonbreeding, extragroup males, especially the so-called follower males, use the same areas and resources as do the harems. Crook’s (1966) observations of gelada suggested that all-male groups were grazing in a different part of the range from the harems. This was true, however, only on a statistical basis because of intermingling and range overlap with these two types of groups. In another more detailed and longer-term study of geladas, all-male groups apparently fed in the same areas as the harems even in periods of food scarcity, and intraspecific competition for food was not obviously reduced with increased dispersion of the harems (Goss-Custard et al., 1972; Dunbar and Dunbar, 1975). Solitary males, all-male groups, and harems of patas were all seen using the same waterholes and ranges, sometimes simultaneously, in the Waza National Park of Cameroun (Struhsaker and Gartlan, 1970). Hall ( 1 965) also found solitary males using the ranges of harems in Uganda. In a more recent study of the Waza patas, part of which took place during the severe sahel drought of 1974, Gartlan (1975) suggested that harems had priority of access to waterholes over solitary males and all-male groups, but this did not eliminate indirect competition for this very limited resource since they still used some of the same waterholes. Gartlan (1973, however, did find all-male groups in which the individuals were obviously dying from thirst, while at the same time harem members some 8 km away all appeared in relatively good condition. These latter conditions lend support to Crook and Gartlan’s hypothesis in that during periods of extreme water shortage, competition between harems and extragroup males may be very intense to a point where the harem benefits at the expense of the extragroup males. As Crook (1972) points out, “although the ecological value of other-male exclusion is only operative when food shortage is actually present, exclusion may have predictive value for survival when shortage occurs.” Detailed studies on extragroup males must be made to clarify their ecological relationships with the harems.

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

213

Exclusion of “surplus” males from harems certainly involves factors in addition to intraspecific competition for food. An obvious factor is intrasexual competition for mates (Crook, 1972). In other words, all males but one are excluded from the group so that the harem male has exclusive access to the females, thereby improving his reproductive success. Retention of more than one fully adult male in a heterosexual group is dependent on the codbenefit ratio to the males concerned, their mates, offspring, and close relatives. The cost of retaining several males in the group would be the loss of exclusive access to estrous females by the harem male. What are the benefits to the dominant male of allowing more than one male in the group? In some species, males, generally having a larger body size and more aggressive nature than females, cooperate in predator deterrence, detection or defense, and defense against other conspecific groups for access to food and other important resources (Crook, 1972; Goss-Custard et al., 1972). Males also contribute their knowledge of the group’s range, and due to the more peripheral nature of some males (e.g., mangabeys, Waser, 1974), may aid in finding superabundant food resources. The males will be improving their own prospects of survival as well as that of their mates and close relatives. How, then, have multimale groups evolved where potential competition for estrous females is omnipresent? Certainly the emergence of a dominance hierarchy among the males of a group is one factor. We would suggest that the ability to monitor the sexual state of females easily is another. This depends on visibility: the type of habitat, the degree of group spread and interindividual distance, and whether the female has some external sign of esfrus. The degree of estrous synchrony among females of a group will also directly affect a male’s ability to monitor them. With few females in estrus simultaneously, the task of monitoring will be easier. Among cercopithecids, females lack any external sign correlating with estrus in all Cercopithecus species, patas, black and white colobus, and all Asiatic Colobinae that have been studied. All of the above except vervets, the proboscis monkey, and some populations of grey langurs live in harem groups. In contrast, species with females having external signs of estrus (swelling or reddening of sexual skin, vulvar protrusion, bead formation, and coloring of the chest) include all the African Colobinae except the black and white colobus [red colobus, Struhsaker, 1975; black colobus (Cofobus satanas), Sabater Pi, 1973; D. McKey, personal communication; olive colobus, Napier and Napier, 19671, all mangabey species (Chalmers, 1968; Homewood, 1976), all baboons, drills, and mandrills, the gelada, the talapoin (Hill, 1966), and most macaques (Napier and Napier, 1967; Rowell, 1972b). All of these species live in either multimale groups or bands (see also Clutton-Brock and Harvey, 1976). Although some of these species also show sexual swellings or other signs of estrus at nonfertile

214

THOMAS T . STRUHSAKER AND LYSA LELAND

periods, they all show estrous signs during ovulation. In the following discussion, the term estrus refers to periods of sexual receptivity occumng during fertile periods. It might be argued that hamadryas baboons and geladas are exceptional because the females have conspicuous signs of estrus, yet they live in one-male units. Both species, however, commonly aggregate in close proximity with 100 or more conspecifics (in bands and troopdherds), including males without harems who could potentially copulate with harem females. In hamadryas, the combination of an abundance of extraharem males, particularly the “followers,” the females’ propensity to copulate with males other than their harem male, the tendency for synchronized estrus among females of a harem, and the limited visibility provided by areas of dense scrub brush make it difficult for the harem male to monitor the estrous females (Kummer, 1968). The situation is much more like a multimale group than the harems of, for instance, forest species; and the important role of the perineal swelling as an aid in monitoring the estrous females is equally apparent. The geladas also have a more typical multimale, rather than harem, organization although it is less obvious than with the hamadryas. Conclusions on sexual behavior, however, seem based on only nine copulations during a small part of one estrous period for each of two subadult females (Dunbar and Dunbar, 1974, 1975). Although gelada females seem less ready to copulate with males other than the harem male, they interact in nonagonistic ways with extraharem males. Since adult females become separated from the harem male by as much as 450 m, and vegetation is sufficiently dense in many areas as to place the harem male and his females out of view of one another, these interactions could lead to potential matings. Juvenile female geladas, in their first estrous cycles, copulate with extraharem males, and on occasion the harem male will intercede aggressively. Several other apparent exceptions require further explanation. Most vervets (Cercopithecus pethiops, Struhsaker, I967a), some populations of grey langurs (Presbytis entellus, Yoshiba, 1968), and the proboscis monkey (Nasalis larvatus, Kawabe and Mano, 1972) live in multimale groups but do not have signs of estrus. In the case of vervets, the open conditions of most of their habitats permit greater ease and efficiency of monitoring the behavior of other group members than if they lived in dense vegegation as all other Cercopithecus species do. Group spread is less than that of baboons or patas. The mere proximity and visibility of the dominant male in these conditions is apparently enough to inhibit copulation by lower-ranking males and to allow monitoring of females. “Open” habitats do not always lead to multimale groups. Some populations of patas, however, live in very open habitats but in one-male groups. Most patas, however, live in areas of poor visibility where grass is tall (at least 1-2 m) for part, if not most, of the year. Furthermore, the extremely wide intragroup dispersion pattern of this species would also select against tolerance of more than

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

215

one adult male in the group, as well as the fact that females have no external estrous signs. The proboscis monkey and those populations of grey langurs living in multimale groups remain enigmas. Three macaque species, all of whom live in multimale groups, either lack pronounced visual signs of estrus or have signs that are equivocal. Both the toque (Macaca sinica, Napier and Napier, 1967; W . P. Dittus, personal communication) and bonnet macaque (M.radiata, Napier and Napier, 1967; Rahaman and Parthasarathy, 197 1) secrete copious quantities of highly odiforous mucus from the vagina at the time of estrus. Rahaman and Parthasarathy concluded that bonnet males select mates on the basis of olfactory and gustatory cues. The perivaginal area of estrous toques is only very slightly swollen and brighter red in color (W. P. Dittus, personal communication). Toque males copulate most frequently with females when the flow of their vaginal fluid is strongest. Young female rhesus (M.mufatra) show swellings and increased reddening of sexual skin during their early estrous periods; but as they reach full maturity, these estrous signs become less prominent (Carpenter, 1942; Napier and Napier, 1967; Rowell, 1967, 1972a,b). Olfactory cues from the vagina are apparently more reliable indicators of estrous conditions in adult rhesus females than are visible changes (Michael and Kerverne, 1970), but recent studies challenge this conclusion (Goldfoot et a f . , 1976 a,b; Kerverne, 1976; Michael et al., 1976). Thus, in these three species, monitoring of the females’ estrous state is more difficult than in species having conspicuous visual correlates of estrus, but not so difficult as in those lacking either pronounced visual or olfactory cues. Olfactory cues also appear to be the major sensory aids in monitoring female estrous states among the New World primates (e.g., Rowell, 1972b; Eisenberg, 1976) and the prosimians (A. Jolly, 1966; Richard, 1974b). Examples of pronounced morphological changes associated with estrus also exist in both of these major taxa; e.g., increase in size and reddening of genitalia in female Lemur catta (A. Jolly, 1976) and genitayperineal swellings in some populations of Alouarta palliara (Glander, 1975), both of whom live in multimale groups. Among the apes, species lacking estrous swellings tend to live in pair bonds (gibbons and siamangs) or form temporary male-female sexual consortships in an otherwise relatively solitary existence where male-male intolerance is very pronounced (orang-utans, MacKinnon, 1974). Both chimpanzees and gorillas (Nadler, 1975) have estrous swellings; the former live in multimale fusionfission societies and the latter in small bisexual groups with more than one sexually mature male (Schaller, 1965). The evolution of swellings and other external signs of estrus must have relied on reproductive advantages to the females in terms of their genetic fitness. Female fitness is improved through impregnation by dominant males who presumably have genotypes for superior physical, physiological, and behavioral

216

THOMAS T. STRUHSAKER AND LYSA LELAND

attributes(also see Clutton-Brock and Harvey, 1976). Selection would favor the genotypes of females fertilized by dominant males. External signs of estrus, such as swellings, allow closer and more precise monitoring by the males in a group of both a female’s reproductive state (including probable time of ovulation) and her sexual behavior. High-ranking males presumably have priority of access to estrous females, thereby improving their genetic fitness (e.g., Hausfater, 1975). Although an estrous female often displays choice in sexual partners and is capable of rejecting particular males, the positive response of a dominant male toward a receptive female, and his inhibitory influence over lower-ranking males attempting to mate with her, greatly affect with whom she copulates (e.g., Gautier-Hion and Gautier, 1976). Under some circumstances she may accept any male regardless of his dominance status (e.g., Loy, 1971; Hausfater, 1975) and may copulate with many males in any one estrous period (e.g., rhesus, Kaufmann, 1965; Loy, 1971; baboons, Hausfater, 1975; mangabeys, Homewood, 1976). The important issue, however, concerns fertilization. Available data suggest that in many multimale groups the high-ranking males do the great majority of fertilization (e.g., Carpenter, 1942; Altmann, 1962; Kaufmann, 1965; Hausfater, 1975; Struhsaker, 1967b, 1975). External signs of estrus may also stimulate ’aggression among the males of the group whereby the dominance hierarchy is regularly challenged to establish the “fittest” male by competition and are therefore of apparent advantage to the female’s reproductive fitness. What, then, are the reproductive advantages to subordinate males in belonging to a group? They may gain direct reproductive advantage either through infrequent copulation (e.g., Goss-Custard et u f . ,1972; Saayman, 1975; Hausfater, 1975) or by rising in rank to assume the position of chief copulator (e.g., Struhsaker, 1975; Homewood, 1976). Furthermore, it is likely that these males may have sired some of the other members of the group and by remaining in the group can contribute to their inclusive fitness, as described above. Phylogeny among the Cercopithecidae correlates strongly with whether a species has more than one adult male in the heterosexual group and the presence or absence of an external sign of estrus. C. J. Jolly (1966) has proposed a division of the Cercopithecinae into three tribes. All of the Cercopithecini (Cercopithecus spp. and patas) lack any signs of estrus and, with the exception of vervets, live in harems. The tribal affinity of talapoin monkeys is in doubt, but they have frequently been aligned with the Cercopithecini (e.g., Simpson, 1945; Hill, 1966). If this alignment is correct, then the talapoin is exceptional to this tribe in having large multimale groups and females with large estrous swellings. Affenopithecus may also be related to this tribe; they have swellings (Rowell, 1972a) but nothing is known of their sociology. The Cercocebini (Pupio, Mucucu, Cercocebus, Mandrillus) live either in multimale social groups or in harems which usually form large aggregations with other harems and extragroup males; females have either a prominent external

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

217

visible sign of estrus or conspicuous olfactory cues in the form of vaginal secretions. The geladas belong to the tribe Theropithecini along with several fossil genera but are like the Cercocebini in having external signs of estrus and living in harem clusters. No tribal division of the Colobinae has been proposed, but most Asiatic species live in harems (Bernstein, 1968) and lack any sign of estrus. All the African colobus, except the black and white colobus, appear to have estrous swellings. The red colobus7and black colobus usually live in multimale groups. Female olive colobus also have swellings but there is essentially no information about their sociology. The external signs of estrus among these different species are variable in form and in the tissues involved. In several cases, they probably represent examples of convergent evolution suggesting that they are not derived from one primitive character, but have evolved independently in several different lines (Wickler, 1967; Rowell, 1972a). When environmental conditions make monitoring of a female’s estrous state difficult and the retention of more than one adult male in the group advantageous and/or the expulsion of these “extra” males too costly, selection would favor the evolution of external signs of estrus. In other words, estrous signs and multimale groups would co-evolve. The hypothesis is, then, that intrasexual selection will favor males who exclude other males from the heterosexual groups when it is difficult to monitor the females’ estrous condition and, more importantly, their periods of fertility, due to the absence of conspicuous external signs of estrus and/or poor visibility due to dense vegetation andor a widely dispersed spacing pattern of group members. The latter occurs when exploiting food items of low density and wide dispersion, such as some types of phytophagous insect prey. The presence of external signs of estrus, on the other hand, would increase the efficiency of monitoring females and therefore reduce the value of excluding other males, a process which may be costly and harmful to all concerned (e.g., Goss-Custard et al., 1972; Gautier-Hion and Gautier, 1976; Struhsaker, 1977). This assumes that with increased efficiency in monitoring, high-ranking males are better able to improve their reproductive success either through direct intervention in preventing the females from mating with lower ranking males (e.g., Altmann, 1962) or by copulating with these females at a period when ovulation is most likely (e.g., Hausfater, 1975). In our studies in the Kibale Forest, the red colobus provide an example of a unique social structure among primates where all the adult males are apparently closely related to one another. Therefore, they benefit in terms of kin selection ‘C. Marsh (personal communication) reports that many red colobus groups along the Tana River have only one adult male and are about half the size of those living in rain forests. These two differences are most likely related to the impoverished and highly seasonal habitat which has in many places been recently and drastically diminished in area by man.

218

THOMAS T . STRUHSAKER A N D LYSA LELAND

and inclusive fitness through their unified efforts in supplanting and fighting other red colobus groups over choice food resources. The males in the mangabey groups are probably not particularly closely related genetically judging by their high rates of intergroup migration. Estrous synchrony was not apparent in either the red colobus or mangabey groups studied which meant that there were never more than two or three females simultaneously in estrus. This factor combined with the presence of estrous swellings simplified monitoring of females. In the redtails and blues, a number of factors were obviously against tolerance of more than one male in the group, all related to reproductive success and intrasexual competition. Females lacked external signs of estrus and were relatively seasonal and synchronous in estrus; and members of the group were widely dispersed. Bw colobus females lack external signs of estrus. The close spacing of group members in this species does not nullify the importance of visibility but simply implies that the harem male has even tighter control over the females. In all five species studied in Kibale, it appears that predation pressure is low and confined to the crowned eagle (Stephanoaetus coronatus). Due to the arboreal environment where escape and concealment are the primary tactics for avoiding predation, there would be little value in retaining several adult males in the group for defense against predators. Even their larger size does not seem to be a deterrent to attack as evidenced by a case of predation by a pair of crowned eagles on a fully adult 10-kg male bw colobus (T. T. Struhsaker, unpublished observations).'

VII. A.

GENERAL SUMMARY

SUMMARY OF RESULTS

This report is a synopsis and collation of socioecological data from studies of five sympatric monkey species in the Kibale Forest of West Uganda. Some of the major behavioral and sociological findings are as follows: Time budget: The proportion of time spent foraging and scanning could be related to gross food habits. Time spent resting could in some cases also be related to feeding ecology. Omnivores locomoted more than folivores. The amount of time infants and young juveniles clung to their mothers and played 'In this case an adult crowned eagle was found on the fresh carcass of an adult male bw colobus. The eagle flew away o n our approach and landed near another crowned eagle about 20 meters from us. A postmortem examination o f the male colobus revealed that his body was still warm and not in rigor m o n k , none of his bones w a s broken, and there were a series of puncture wounds about his head and thorax which were not bleeding o n the external surface but led to massive hemorrhaging in the pericardial cavity. The two eagles flew onto the colobus carcass as w e moved away.

SOCIOECOLOGY OF FIVE SYMPATRlC MONKEY SPECIES

219

was related to the amount of time the mothers spent resting, which in turn could be related to their feeding ecology. Allogrooming was similar in all five species and this was probably due to its important role in hygiene and social cohesion. Group size and composition: Among the five species, gross food habits did not correlate with either group size or composition. Adult male red colobus were the most stable members of the group in contrast to the other four species where males shifted between groups relatively frequently. Juvenile and subadult females were the mobile elements in red colobus social groups, but apparently did not migrate between groups in the other species. Solitary adult and subadult males were seen in all five species. All-male groups were not formed, with rare and infrequent exceptions occurring only in bw colobus. Spacing: Spatial dispersion of group members was greater, and the number of neighbors within 2.5m was less, among omnivores than folivores. Of the three omnivores, mangabeys had the greatest group spread and this was probably related to their heavy reliance on widely dispersed and low-density fruit and arthropod resources. Directly related to interspecific differences in group spread were the frequency of occurrence and loudness of cohesion vocalizations. Adult males: Relations among adult males and their social roles in the group vaned dramatically between the five species. For example, in the three harem species, males were generally intolerant of one another in contrast to the moderate male-male tolerance among mangabeys and the extreme male-male tolerance and cohesiveness of red colobus. Only among red colobus did the males groom one another more than expected, remain spatially close to one another, form a cohesive and coordinated subgroup when fighting other groups, and give a stylized forni of presentation among themselves which never involved other age-sex classes. In contrast, adult male mangabeys even of the same group tended to avoid one another. Agonistic behavior: Agonistic encounters appeared to be more frequent in species having multimale heterosexual groups than in harem species. Aggression among adult males was common to all five species. Female-female aggression was uncommon and only in redtails and mangabeys did they aggress against one another more than expected by chance. Grooming: In all five species adult males were groomees more than or as much as expected by chance and groomers less than expected. It appears that in species where the males are transient they groom females more than in species with nontransient males. The extent of grooming among adult females tends to be related to interspecific differences in the frequency and extent to which they joined together to defend the group’s territory or social space and the duration of their tenure in the group. Adult females of all species were groomers more than expected, and all except red colobus were groomees more than or as much as expected.

220

THOMAS T . STRUHSAKER AND LYSA LELAND

Sexual behavior: Female perineal sexual swellings were present only in the two species that lived in multimale groups and were absent in the three haremliving species. In the multimale groups, the copulation frequency of the adult males was directly related to their dominance status, with exceptions in some mangabey groups. Neonates: The five species could be ranked according to the degree of aunt behavior shown toward neonates by other group members as follows, from greatest to least: bw colobus, mangabey, redtail, blue, and red colobus. Intergroup relations: Red colobus social groups had extensive and nearly complete range overlap with neighboring groups. Relations between these groups varied from extreme tolerance at close quarters to intense aggression. Mangabey groups also had extensive range overlap with adjacent groups, but these groups tended to avoid one another and they rarely met. The other three species were territorial but the bw colobus had more intergroup range overlap than did the redtails and blues.

B. SUMMARY OF CONCLUSIONS AND HYPOTHESES, SUGGESTIONS FOR FUTURERESEARCH

AND

(1) Within a species, group size is primarily related to food density and a~ailability.~ This usually seems to be a function of mortality rates in young age classes rather than through changes in fecundity. Eventually the effect of this low recruitment will spread to the older classes. (2) When food is of chronically low density, we would expect smaller group sizes. It is important to know if such situations lead to increased differential mortality between the sexes which may account for interpopulation differences in the numbers of males in heterosexual groups in some species. (3) Interspecific differences in group size can often be related to food density and patterns of dispersion. Among the three omnivorous monkey species studied at Kibale there was an inverse relationship between body and group size and a direct relationship between body and home range size. Similar trends seem to prevail with some sympatric New World omnivorous monkeys. These relationships are in turn related to the kinds and densities of food exploited by species of different body sizes. For example, one might expect comparatively large omnivores to rely more heavily on fruit and forage in small groups, the size of which depends on the size and dispersion of the basic food unit. (4) In terms of interindividual spacing and group spread, it is predicted that: (a) species feeding on high density and uniformly distributed foods such as some foliar foods will probably live in cohesive groups and have short interindividual 'This refers to situations in which other variables such as predation and availability of sleeping sites or water holes are constant or have minimal influence.

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

22 1

distances; (b) species which hunt insects, especially mobile forms, will have wider interindividual distances as a means of increasing foraging efficiency; (c) species relying on foods with low overall density and occurring in widely separated clumps will have widely spread groups. Intragroup spacing may also be affected by competition and aggression over food. ( 5 ) The existing hypotheses relating intergroup spacing and food density and dispersion generally apply to the Kibale data. It is emphasized that philopatry and defense of exclusive territories should increase the predictability of resource location and thereby increase foraging efficiency. It is predicted that the extent and frequency of territorial violation (trespassing) depends on the daily ranging patterns in relation to territory size, which in turn are related to food density and dispersion. The hypothesis that high food density with an even distribution leads to territoriality should be examined more closely. (6) The sex that is the most socially mobile in a species seems correlated with the mating system, as it relates to the habitat and feeding ecology, and intrasexual selection, and in the degree to which members of the same sex join in cooperative efforts to the benefit of themselves, their offspring and close relatives. Outbreeding is probably the ultimate factor in migration between social groups. The situation seems particularly complex with regard to cases where females voluntarily leave their parental group. (7) Because extragroup males are not excluded from resources used by reproductive groups, their exclusion from the group must be related to factors in addition to food, such as intrasexual competition for mates. The socioecology of solitaries and all-male groups should be studied in detail to determine the extent of indirect competition for food with heterosexual groups, as well as the nature and frequency of their interactions with heterosexual groups and possible differential mortality. (8) It is predicted that one-male groups will exist where females lack external signs of estrus at the time of ovulation. This will be especially pronounced where visibility is poor due to dense vegetation andor a widely dispersed pattern of group members and, as a consequence, monitoring of the females’ sexual behavior is difficult. Further attention should be given to the apparent exceptions to this generalization such as the proboscis monkey and those populations of grey langurs with multimale groups. Studies of species like the olive colobus and of vervet populations living in rain forest (e.g., possibly Sese Is., Uganda) would further test the general validity of this hypothesis. (9) When environmental conditions make monitoring of a female’s estrous state difficult and the retention of more than one adult male in the group advantageous and/or the expulsion of these extra males too costly, selection would favor the co-evolution of external signs of estrus and multimale groups. Among Old World monkeys these two characteristics are often closely correlated with phylogenetic affinities. The codbenefit ratio of retaining or allowing more than

222

THOMAS T. STRUHSAKER AND LYSA LELAND

one adult male in heterosexual groups is not always apparent and needs further study. (10) Many of the above problems are best evaluated through the comparative approach within and between habitats, particularly in the study of sympatric species. ( I I ) Long-term primate studies are essential because we are usually dealing with long-lived, slowly reproducing mammals. Meaningful data on group dynamics and the probable degree of genetic relatedness among the group members can be collected only by observing groups for at least half the adult life span, which for most Old World monkeys means a period of five to six years. Longterm studies will also provide critical data on mating patterns and the relations be!ween social roles, dominance, and probable reproductive success during a large proportion of the individuals' lives rather than the usual one or two seasons of most studies. Short-term studies can be extremely deceptive in these respects as our work on red colobus is showing. When feasible, these observational studies should be accompanied by genetic studies such as with serological analyses. (12) Of vital importance to many of the preceding hypotheses and research topics is the problem of food density and distribution. We are sorely lacking adequate studies on food abundance, its distribution in time and space, temporal changes in quality,and renewal rates.Quantitative data on these subjects over a period of at least two years and preferably longer in each study area are critical to the development and testing of many of our socioecological hypotheses. ( 13) The complexity of primate socioecology, involving such a great number of interacting variables, logically leads to the suggestion of systems analysis (Crook et a / ., 1976) and the development of evolutionary hypotheses based on models of population biology (Wilson, 1975). The value of these analyses and their conclusions hinge on having representative data. Finally, because most primates live in rain forests, more attention should be given to the species of this biome.

Acknowledgments This study would not have been possible without the cooperation of Drs.J . F. O a k s . R. Rudran. and P. Waser, who. through their conscientious field studies, have provided so much of the basic data ofthis paper. All three have also generously supplied us with additional unpublished data. which they have perniitted us to include here. Mr. Simon Wallis has also kindly provided us with some of his unpublished results. Although we assunie full responsibility for the ideas presented i n this paper, many of them have been developed through, and benefited from, discussions with these four colleagues. Valuable comments on the manuscript were provided by the following individuals: Colin Beer. Steven Green. Robert Hinde, Peter Marler, Clive Marsh, John O a k s , Jay Rosenhlatt. R. Rudran, Simon Wallis, and Peter Waser. Financial support was from the New Y o r k Zoological Society and the United States National Institutes of Mental Health (grant no. ROI-MH23008- I EPR).

SOCIOECOLOGY OF FIVE SYMPATRlC MONKEY SPECIES

223

Permission to study in Uganda and the Kibale Forest was kindly granted by President’s Office of Uganda, the Uganda National Research Council, and the Uganda Forest Department. The Department of Zoology, Makerere University, Kampala acted as our local sponsor. To all of these individuals and agencies we extend our thanks.

References Altmann, J., Altmann, S. A,, Hausfater, G., and McCuskey, S. A. 1977. Life history of yellow baboons: Physical development, reproductive parameters and infant mortality. Primates 18, 3 15-330. Altmann, S . A. 1962. A field study of the sociobiology of rhesus monkeys, Macaca mularra. Ann. N Y . Acud. Sci. 102, 338435. Altmann, S . A,, and Altmann, I . 1970. “Baboon Ecology” Univ. of Chicago Press, Chicago, Illinois. Bernstein, 1. S. 1968. The lutong of Kuala Selangor. Behaviour 32, 1-16. Bernstein, I. S. 1972. Activity profiles of primate groups. In (A. M. Schrier and F. Stollnitz, eds.), “Behavior of Non-Human Primates” Vol. 3, p. 69-106. Academic Press, New York. Bourliere, F., Hunkeler. C.. and Bertrand, M. 1970. Ecology and behavior of Lowe’s guenon (Ccvc.opithecuscwnphelli h v i ) in the Ivory Coast. In “Old World Monkeys, Evolution, Systematics, and Behavior” ( J . R . Napier and P. H. Napier. eds.), pp. 297-350. Academic Press. New York. Carpenter, C. R. 1942. Sexual behavior of free ranging rhesus monkeys (Macaca mulaffa).J . Conrp. Psychol. 33, 113-162. Catchpole. H. R., and van Wagenen, G. 1975. Reproduction in the rhesus monkey, Mtrccrcu mulatfu.In “The Rhesus Monkey” (G. H. Bourne, ed.), Vol. 2, pp. 117-140. Academic Press, New York. Chalmers, N. R. (1968). The social behaviour of free living mangabeys in Uganda. Folia Primafol. 8, 263-281. Chalmers, N. R. 1973. Differences in behaviour between some arboreal and terrestrial species of African monkeys. In “Comparative Ecology and Behaviour of Primates” (R. Michael and J . Crook, eds.), pp, 59-100. Academic Press, New York. Charles-Doniinique, P. 1977. “Ecology and Behaviour of Nocturnal Primates.” Duckworth, London. Clutton-Brock. T. H. 1972. Feeding and Ranging Behaviour in the Red Colobus Monkey. Ph.D. Thesis, Cambridge Univ., Cambridge, England. Clutton-Brock, T. H. 1974. Primate social organisation and ecology. Nature (London) 250, 539542. Clutton-Brock, T. H., and Harvey, P. H. 1976. Evolutionary rules and primate societies. In “Growing Points in Ethology” (P. P. G. Bateson and R . A. Hinde, eds.), pp. 195-238. Cambridge Univ. Press, London and New York. Crook, 1 . H. 1966. Gelada baboon herd structure and movement, a comparative report. Symp. Zool. SOC.London 18, 237-258. Crook, J. H. 1070. The socio-ecology of primates. In “Social Behaviour in Birds and Mammals” (J. H. Crook, ed.). pp. 103-166. Academic Press, New York. Crook, J . H. 1972. Sexual selection, dimorphism. and social organization in the primates. In “Sexual Selection and the Descent of Man 1871-1971” (B. Campbell, ed.), pp. 231-281. Aldine, Chicago. Illinois. Crook, J. H . , and Aldrich-Blake, F. P. G. 1968. Ecological and behavioural contrasts between sympatric ground-dwelling primates in Ethopia. Folia Primafol. 8, 180-191,

224

THOMAS T. STRUHSAKER AND LYSA LELAND

Crook, J. H., and Gartlan, 1. S . 1966. Evolution of primate societies. Nature (London) 210, 1200-1203. Crook, J. H . , Ellis, J . E., and Goss-Custard, J. D. 1976. Mammalian social systems: Structure and function. Anim. Behav. 24, 261-274. Dunbar, R. I. M., and Dunbar, P. 1974. The reproductive cycle of the gelada baboon. Anim. Behav. 22, 203-210. Dunbar, R. 1. M., and Dunbar, P. 1975. Social dynamics of gelada baboons. Conrrib. Primatol. 6, 1-157. Dunbar, R. I. M., and Dunbar, P. 1976. Contrasts in social structure among black-and-white colobus monkey groups. Anim. Behav. 24, 84-92. Eisenberg, J. F. 1976. Communication mechanisms and social integration in the black spider monkey Arelesfusciceps robustus and related species. Smirhson. Conrrib. Zool. 213, 1-108. Eisenberg, J. F., Muckenhim, N. A., and Rudran. R. 1972. The relation between ecology and social. structure in primates. Science 176, 863-874. Gartlan, J. S. 1975. Adaptive aspects of social stmcture in Eryrhrocebus paras. Symp. Congr. In!. Primarol. SOC., 51h, 1974, pp. 161-171. Gatinot, B. K. 1975. kcologie d’un Colobe Bai (Colobus badius remmincki, Kuhl 1820) dans un Milieu Marginal au Senegal. Ph.D. Thesis, Univ. de Paris, Paris. Gautier-Hion, A. 1970. L’organisation sociale d’une bande de talapoins (Miopirhecus rulapoin) dans le Nord-est du Gabon. Folia Primatol. 12, 116-141. Gautier-Hion, A., and Gautier, J. P. 1976. Croissance, maturite sexuelle et sociale, reproduction chez les cercopithecines forestiers africains. F o h frimatol. 26, 165-184. Glander, K. E. 1975. Habitat and Resource Utilization: An Ecological View of Social Organization in Mantled Howling Monkeys. Ph.D. Thesis, Univ. of Chicago, Chicago, Illinois. Goldfoot, D. A,, Goy, R. W . , and Freeman, S . K. 1976a. Lack of effect of vaginal lavages and aliphatic acids on ejaculatory responses in rhesus monkeys: Behavioral and chemical analyses. Horm. Behav. 7, 1-27. Goldfoot, D. A., Goy, R. W., Kravetz, M. A., and Freeman, S. K. 1976b. Reply to Michael. Bonsail, and Zumpe. Horm. Behuv. 7 , 373-378. Goodall, J. 1965. Chimpanzees of the Gombe Stream Reserve. In “Primate Behavior” (I. DeVore, ed.), pp. 425473. Holt. New York. Goss-Custard, J . D., Dunbar, R. I. M., and Aldrich-Blake, F. P. G. 1972. Survival, mating and rearing strategies in the evolution of primate social StNCtUre. Folia frimurol. 17, 1-19. Hall, K. R. L. 1965. Behaviour and ecology of the wild patas monkey, Eryrhrocebus paras. in Uganda. J . Zool. 148, 15-87. Hall, K. R. L., and DeVore. I. 1965. Baboon social behavior. In “Primate Behavior” (I. DeVore, ed.), pp. 53-1 10. Holt, New York. Hamilton, W. J., 111, Buskirk, R. E., and Buskirk, W. H. 1976. Defense of space and resources by chacma (Papio ursinus) baboon troops in an African desert and swamp. Ecology 57, 12641272. Harcourt, A. H.,Stewart. K. J., and Fossey. D. 1976. Male emigration and female transfer in wild mountain gorilla. Nature (London) 263, 226-227. Hausfater, G. 1975. Dominance and reproduction in baboons (Papio cynocephalus), a quantitative analysis. Conrrib. Primafol. 7, I - 150. Hill, W. C. 0. 1966. “Primates, Comparative Anatomy, and Taxonomy. VI. Cercopithecinae” Edinburgh Univ. Press, Edinburgh. Hladik, C. M. 1975. Ecology, diet, and social patterning in Old and New World primates. In “Socioecology and Psychology of Primates” (R. H. Tuttle, ed.), pp. 3-36. Mouton, The Hague. Homewood, K. M. 1976. Ecology and Behaviour of the Tana Mangabey. Cercocebus galerirus galerirus. Ph.D. Thesis, Univ. College, London.

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

225

Itani, J. 1958. On the acquisition and propagation of new habit in the natural group of the Japanese monkeys at Takasakiyama. Primates 1, 84-98. Itani, J., Tokuda, K.. Furuya, Y., Kane. K., and Shin, Y. 1963. The social construction of natural troops of Japanese monkeys in Takasakiyama. Primares 4, 1 4 2 . Jolly, A. 1966. “Lemur Behavior, a Madagascar Field Study.’’ Univ. of Chicago Press, Chicago, Illinois. Jolly. C. J . 1966. Introduction to the Cercopithecoidea with notes on their use as laboratory animals. Symp. 2001. Soc. London 17, 4 2 7 4 5 7 . Kaufmann, J . H. 1965. A three-year study of mating behavior in a free-ranging band of rhesus monkeys. Ecology 46, 500-5 12. Kawabe, M., and Mano, T. 1972. Ecology and behavior of the wild proboscis monkey, Nasalis larvarus (Wurmb), in Sabah, Malaysia. Primates 13(2), 213-228. Keverne, E. B. 1976. Sexual receptivity and attractiveness in the female rhesus monkey. Adv. Study Behav. 7 , 155-200. Klein, L. L. 1974. Agonistic behavior in neotropical primates. In “Primate Aggression, Territoriality and Xenophobia. A Comparative Perspective” (R. Holloway. ed.), pp. 77-122. Academic Press, New York. Klein, L. L., and Klein, D. 1. 1975. Social and ecological contrasts between four taxa of neotropical primates. In “Socioecology and Psychology of Primates” (R.H. Tuttle, ed.), pp. 59-86. Mouton, The Hague. Koford, C. B. 1956. Population dynamics of rhesus monkeys on Cay0 Santiago. In “Primate Behavior” (1. DeVore, ed.), pp. 160-174. Holt, New York. Kummer, H. 1968. “Social Organization of Hamadryas Baboons.” Univ. of Chicago Press, Chicago, Illinois. Kummer, H. I97 I . “Primate Societies: Group Techniques of Ecological Adaptation.” Aldine, Athenon, Chicago, Illinois. Leskes, A,, and Acheson, N. H. 1971. Social organization of a free-ranging troop of black and white colobus monkeys (Colobus abyssinicus). Proc. Inr. Congr. Primarol., 3rd, 1970, Zurich, pp. 22-31. b y . J. D. 197 I . Estrous behavior of free-ranging rhesus monkeys (Maraca mularra). Primates 12, 1-31. MacKinnon, J . 1974. The behaviour and ecology of wild orang-utans. h i m . Behav. 22, 3-74. Marler, P. 1969. Colobus guereza: Territoriality and group composition. Science 163, 93-95. Marler, P. 1972. Vocalizations of East African monkeys 11: Black and white colobus. Behaviour 42, 175-197. Marler, P. 1973. A comparison of vocalizations of red-tailed monkeys and blue monkeys (Cercopithecus ascanius and C . mitis) in Uganda. 2. Tierpsychol. 33, 223-247. Michael, R. P., and Kerverne, E. B. 1970. Primate sex pheromones of vaginal origin. Narure (London) 225, 84-85. Michael, R. P., Bonsall, R. W., and Zumpe, D. 1976. “Lack of effects of vaginal fatty acids, etc.”: A reply to Goldfoot et al. Horm. Behav. 7 , 365-367. Nadler. R. D. 1975. Sexual cyclicity in captive lowland gorillas. Science 189, 813-814. Napier, J . R., and Napier. P. H. 1967. “A Handbook of Living Primates.” Academic Press, New York. Nishida, T . , and Kawanaka, K . 1972. Inter-unit group relationships among wild chimpanzees of the Mahali Mountains. Kyoro Univ. Afr. Stud. 7 , 131-169. Oates, J . F. 1974. The Ecology and Behaviour of the Black-and-white Colobus Monkey (Colobus guereza Riippell) in East Africa. Ph.D. Thesis, Univ. of London, London. Oates, 1. F. 1977a. The guereza and its food. In “Primate Ecology: Studies of Feeding and Ranging Behaviour in Lemurs, Monkeys and Apes” (T. H. Clutton-Brock, ed.), pp. 275-321. Academic Press, New York.

226

THOMAS T. STRUHSAKER AND LYSA LELAND

Oates, J. F. 197%. The guereza and man: How man has affected the distribution and abundance of Colobus guereza and other black colobus monkeys. In “Primate Conservation” (Prince Rainier of Monaco and G . H. Bourne, eds.), pp. 419467. Academic Press, New York. Oates, J . F. 1977~.The social life of a black-and-white colobus monkey, Colobus guereza. Z. Tierpsychol. 45, 1-60, Oates, J. F. 1978. Water-plant and soil consumption by guereza monkeys (Colobus guereza): A relationship with minerals and toxins in the diet? Biorropica (in press). Oates, J. F., Swain, T., and Zantovska. J. 1978. Secondary compounds and food selection by colobus monkeys. Biochem. Sysr. Ecol. (in press). Rahaman, H., and Parthasarathy, M. D. 1971. The role of the olfactory signals in the mating behavior of bonnet monkeys (Mucaca radiara). Commun. Behav. Biol. 6 , 97-104. Reynolds, V., and Reynolds, F. 1965. Chimpanzees of the Budongo Forest. In “Primate Behavior” (I. DeVore, ed.). pp. 368424. Holt, New York. Richard, A. 1974a. Intra-specific variation in the social organization and ecology of Propirhecus verreauxi. Folia Primarol. 22, 178-207. Richard, A. 1974b. Patterns of mating in Propirhecus verreuuxi verreauxi. In “Prosirnian Biology” (R. D. Martin, G. A. Doyle, and A. C. Walker, eds.), pp. 49-74. Duckworth, London. Rodman, P. S. 1973. Population composition and adaptive organization among orangutans of the Kutai Reserve. I n “Comparative Ecology and Behaviour of Primates” (R. P. Michael and J. H. Crook, eds.), pp. 171-209. Academic Press, New York. Rowell, T. E. 1967. Female reproductive cycles and the behaviour of baboons and rhesus macaques. In “Social Communication in Primates” (S. A. Altmann, ed.), pp. 15-32. Univ. of Chicago Press, Chicago, Illinois. Rowell, T. E. 1972a. Female reproduction cycles and social behavior in primates. Adv. Study Behav. 4, 69-105. Rowell. T. E. 1972b. “The Social Behaviour of Monkeys.” Penguin Books, London. Rowell, T. E. 1973. Social organization of wild talapoin monkeys. J . Phys. Anrhropol. 38, 593598.

Rudran, R. 1976. Socio-Ecology of the Blue Monkeys (Cercopirhecus miris sruhlmanni) of the Kibale Forest, Uganda. Ph.D. Thesis, Univ. of Maryland, College Park. Rudran, R. 1978. Socio-ecology of the blue monkeys (Cercopirhecus miris stuhlmanni) of the Kibale Forest, Uganda. Smithson. Conrrih. Zoo/. No. 249, 1-88. Saayman, G. S. 1975. The influence of hormonal and ecological factors upon sexual behavior and social organization in Old World primates. In “Socioecology and Psychology of Primates” (R. H. Tuttle, ed.), pp. 181-204. Mouton, The Hague. Sabater, Pi, J . 1973. Contribution to the ecology of Colobus polykomos satanas (Waterhouse 1838) of Rio Muni, Republic of Equatorial Guinea. Folia Primatol. 19, 193-207. Schaller, G. B. 1965. The behavior of the mountain gorilla. In “Primate Behavior” (I. DeVore, ed.), pp. 324-367. Holt, New York. Schenkel, R., and Schenkel-Hulliger, L. 1967. On the sociology of free-ranging Colobus (Colobus guereza caudurus Thomas 1855). In “Progress in Primatology” (D. Starck, R. Schneider, and H. J . Kuhn, eds.), pp. 185-194. Fischer, Stuttgart. Simpson, G. G. 1945. The principles of classification and a classification of mammals. Bull. Am. hfus. Nar. Hisr. 85, 1-350. Struhsaker, T. T. 1967a. Social structure among vervet monkeys (Cercopithecus aerhiops). Behaviour 29, 83-121. Struhsaker, T. T. 1967b. Behavior of vervet monkeys (Cercopithecus uerhiops). Llniv. Calif., Berkeley, Publ. Zool. 82, 1-64. Struhsaker, T. T. 1969. Correlates of ecology and social organization among African cercopithecines. Folia Primarol. 11, 80-1 18. Struhsaker, T. T. 1973. A recensus of vervet monkeys in the Masai-Amboseli Game Reserve, Kenya. Ecology 54, 930-932.

SOCIOECOLOGY OF FIVE SYMPATRIC MONKEY SPECIES

227

Struhsaker, T. T. 1974. Correlates of ranging behavior in a group of red colobus monkeys (Colobus badius rephrosceles). Am. Zool. 14, 177-184. Struhsaker, T. T. 1975. “The Red Colobus Monkey.” Univ. of Chicago Press, Chicago, Illinois. Struhsaker, T. T. 1976. A further decline in numbers of Amboseli vervet monkeys. Biorropica 8, 2 I 1 -2 14. Struhsaker. T. T. 1977. Infanticide and social organization in the redtail monkey (Cercopirhecus ascanius schmidti) in the Kibale Forest, Uganda. 2. Tietpsychol. 45, 75-84. Struhsaker, T. T. 1978a. Interrelations of red colobus monkeys and rain-forest trees in the Kibale Forest, Uganda. Smithson. Conrrib. 2001.(in press). Struhsaker, T. T. 1978b. Comparison of the behavior and ecology of red colobus and redtail monkeys in the Kibale Forest, Uganda. Proc. Wildl. Symp. E . Afr., 3rd (in press). Struhsaker, T. T. 1 9 7 8 ~Food . habits of five monkey species in the Kibale Forest, Uganda. In “Recent Advances in Primatology, Vol. 1, Behaviour” (D. J . Chivers and J. Herbert, eds.), pp. 225-248. Academic Press, New York. Struhsaker, T. T . , and Gartlan, J . S . 1970. Observations on the behaviour and ecology of the patas monkey (Erythrocebus paras) in the Waza Reserve, Cameroun. J. Zool. 161, 49-63. Struhsaker, T. T., and Leland, L. 1977. Palm-nut smashing by Cebus a. apella in Colombia. Biotropica 9(2), 124-126. Struhsaker, T. T . , and Oates, 1. F. 1975. Comparison of the behavior and ecology of red colobus and black and white colobus monkeys in Uganda: A summary. I n “Socioecology and Psychology of Primates” (R. H. Tuttle, ed.), pp. 103-124. Mouton, The Hague. Sugiyama, Y. 1973. The social structure of wild chimpanzees: A review of field studies. I n “Comparative Ecology and Behaviour of Primates” (R. P. Michael and J. H. Crook, eds.), pp. 376410. Academic Press, New York. Sussman, R. W. 1974. Ecological distinctions in sympatric species of Lemur. In “Prosimian Biology” (R. D. Martin, G. A. Doyle, and A. C. Walker, eds.), pp. 75-108. Duckworth, London. Sussman, R. W., and Richard, A. 1974. The role of aggression among diurnal prosimians. I n “Primate Aggression, Territoriality and Xenophobia. A Comparative Perspective” (R. Holloway, ed.), pp. 49-76. Academic Press, New York. Waser, P. M. 1974. Intergroup Interaction in a Forest Monkey: The Mangabey Cercocebus albigena. Ph.D. Thesis, Rockefeller Univ., New York. Waser, P. M. 1975a. Experimental playbacks show vocal mediation of avoidance in a forest monkey. Nature (London) 255, 56-58. Waser, P. M. 1975b. Monthly variations in feeding and activity patterns of the mangabey, Cercocebus albigena (Lyddeker). E . Afr. Wildl. J . 13, 249-263. Waser, P. M. 1976. Cercocebus albigena: Site attachment, avoidance, and intergroup spacing. Am. Nut. Vol. 110. NO. 976, 91 1-935. Waser, P. M. 1977a. Individual recognition, intragroup and intergroup spacing: Evidence from sound playback to forest monkeys. Behaviour 60, 28-74. Waser, P. M. 1977b. Mangabey feeding, movements, and group size. In “Primate Ecology: Feeding and Ranging Behaviour of Lemurs, Monkeys and Apes” (T. H. Clutton-Brock, ed.), pp. 183222. Academic Press, New York. Waser, P. M. 1978. Postreproductive survival and behavior in a freeranging female mangabey. Folia Primarol. (submitted). Waser, P. M.. and Floody. 0. 1974. Ranging patterns of the mangabey, Cercocebusalbigena, in the Kibale Forest, Uganda. Z. Tierpsychol. 35, 85-101. Waser, P. M., and Waser, M. S. 1977. Experimental studies of primate vocalizations: specializations for long distance propagation. Z . Tierpsychol. 43, 239-263. Wickler, W. 1967. Socio-sexual signals and their intra-specific imitation among primates. I n “Primate Ethology” (D.Moms, ed.). pp. 69-147. Weidenfeld & Nicolson, London. Wilson. E. 0. 1975. “Sociobiology, the New Synthesis.” Belknap Press, Cambridge, Massachu setts.

228

THOMAS T. STRUHSAKER AND LYSA LELAND

Wrangham. R . W . 1975. The Behavioural Ecology of Chimpanzees in Gornbe National Park, Tanzania. Ph.D. Thesis, Cambridge Univ., Cambridge, England. Yoshiba, K . 1968. Social and intertroop variability in ecology and social behavior of common Indian langurs. In “Primates: Studies in Adaptation and Variability” (P. C. Jay, ed.), pp. 217-242. Holt, New York.

ADVANCES IN THE STUDY OF BEHAVIOR. VOL. 5,

Ontogenesis and Phylogenesis: Mutual Constraints* GASTONRICHARD FORMERLY, LABORATOIRE D’ETHOLOGIE

UNlVERSIT6 DE RENNES RENNES-CEDEX. FRANCE

I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Toward a Model of Ontogenesis ........................ A. In the Nest Site of Gallinaceae ..................................

B. Toward Adult Behaviors ............................. C. Nature and Construction of Complex Patterns of Behavior which Assimilate Time . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Toward a Model of Phylogenesis ................................... A. Convergences and Divergences of Ontogenesis of Present Species. . . . . . B. From the Ontogenesis Model to the Phylogenesis IV. Mutual Constraints between Ontogeny and Phylogeny V. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

229 234 234 240 245 249 249 260 264 267 269

1. INTRODUCTION

Nothing begins at birth, nor even in the egg. But there is more, and the present paper will try to show that if an egg receives from two parent cells hereditary information characterizing a moment in evolution, then ontogenetic development, during which this egg changes progressively into an adult genitor, influences in its own way the future trend of that evolution. “To describe behaviour is much more difficult than appears at first sight” (Hinde, 1974). In particular, such description is insufficient if it is limited to considering each animal as reacting to its environment regarded only as a stimulating agent. Such an asymmetrical approach, although frequently adopted in ethology, is a consequence of the historical weight of the reflex concept. *This review is dedicated to T. C. Schneirla’s memory on the tenth anniversary of his death. As early as 1935 in “F’nnciples of Animal Psychology” (Maier and Schneirla, 1935). he insisted on the necessity of taking into consideration phylogenetic relationships us well as the degree of ontogenetic development of the animal being studied at the time it is observed. His conceptual efforts, like those of Hebb, have progressively enlightened this procedure.. which has been adopted more. and more widely by many research teams since 1960. 229

Copyright i$J IY7Y by Academic Preaa. Inc. All rights of reproduction in my form reserved. ISBN 012-CQ4509-5

230

GASTON RICHARD

Rather, I shall try to apprehend simultaneously the organism and the part of environment with which it exchanges information and I shall describe the System thus constituted by referring to the two subsystems [organism, environment] that make it up, as well as to the interrelationships which these subsystems involve. Thus, in a System, I shall confront the egg as well as the broody hen in the nest site, or the egg as well as the mother’s uterus; later, I shall study in the same way the young as well as the social environment (parents, siblings, etc.) within which it lives; but I could deal globally on the phylogenetic level of species, with Insects and Angiosperms, or with Primates and their sociobiological niches. This procedure is not original: It is the same one that Crook’s work revealed progressively (Crook et a l . , 1976); but it is also the same one that Apostel (1967), Meyer (1967), Nowinski (1967), Papert (1967), Piaget (1967b), have defended for a long time. This approach has given rise to many theoretical publications in recent years (Delattre, 1971; Weiss, 1974; Morin, 1977) and it appears as one of the forceful ideas in “Growing Points in Ethology” (Bateson and Hinde, 1976) or in “Perspectives in Ethology” (Bateson and Klopfer; 1973, 1976). Nevertheless it is necessary to be precise about several characteristics of the cybernetic model considered here, which will give this model a structure easier to generalize than Crook’s sociobiological model. In a System [organism, environment], the two components (subsystems) exert permanent mutual constraints, but the entirety is characterized by a homeostatic state which we shall call state of adaptation. Three remarks must now be made: The first one concerns reciprocity of constraints between subsystems. Giving equal importance, value, and dynamics to the traditional field of ethology (constraints exerted by an organism on its environment) and to the traditional field of ecology (constraints exerted by the environment on organisms) gives a symmetrical character to functional analyses. The second one concerns the fundamental value of the exchanges. Behavior, besides its “output” function in the organism subsystem, projects itself onto the environment it modifies; impelling acts of the environment on the organism form, in turn, a permanent “output” of the enyironment Subsystem (Fig. 1). Thus, each subsystem exerts a feedback-type control on the other, and outputs from the System convey its state of adaptation as well as representing the results of the internal working of the whole system. The third one concerns the reference point for homeostasis. The time unit used to study it can give it an evident fixity (the time for an immediate observation) or make homeostatic recalibrations (McFarland, 1971) without destroying the homeostatic state of Systems considered (the duration of individual ontogenesis, or the time for orthogenesis). In colloquial language, this means that an organism

23 1

ONTOGENESIS AND PHYLOGENESIS

S

Y

S

T

E

M

ind ividuaI sub system

4$-

Ai

transformat i a n

J

I..................

e...................

0 .

e x t e r n a I

FEEDBACK

M ECHANI SM

7l As

U e x t e r n a l

FEEDBACK MECHANISM

....,.............

m.

e...................

I

B L A C K

-

BOX

internal FEEDBACK MECHANISM

sub system ~~

FEEDBACK -controlling

MECHANISM functions

of

S Y S T E M

FIG. 1 . Diagram of the structure of a system within which two equal subsystems exchange feedbacks. Letter “A” indicates points of loops where feedback mechanisms are sensitive to the working variations of the transformation blackboxes. Letter “I” indicates points where the eventual introduction, by feedback mechanisms, of the necessary correction occurs (symbols “e” and “i” correspond, respectively, to points A and I, to environment and individual subsystems). Terms “internal” and “external” applied to feedback mechanisms refer to each subsystem. Dotted lines between blackboxes and feedback mechanisms belonging to the same subsystem represent functional or structural links possible between the two elements considered (in Gautier er al., 1978).

232

GASTON RICHARD

and the environment within which it develops maintain between them a state of adaptation, but that the descriptive characteristics of subsysfems are continuously modified with time. Such problems have been widely studied both theoretically and experimentally by the epistemological group in Geneva led by Piaget, and we think that we can name this state (permanent when considered as a whole, but with continuously transforming elements) “invariant-variable , a term already used by Piagetians. From the evolutionary dynamic point of view which concerns us here, it is important to consider possible generalization of this type of homeostasic system. This generalization concerns the functional structure of each constituent subsystem as well as the functional structure of greater taxonomic entities covering simpler systems. Thus, for each subsystem, we could describe homeostases, opposing an endocrine gland to the organism as a whole (physiological type of homeostasis), or a gene to the genome considered as a whole (biochemical type of homeostasis). But, to continue with our representatives of Nature from a System [organism, environment] we could describe homeostases oppsing a species with its ecoethological niche or the biosphere to the geosphere (geobiological-type homeostasis) (Fig. 2). Each one of these homeostases represents the state of adaptation of a particular structure of living matter and the environment with which it finds itself interacting. The interlocking rules of these numerous homeostases thus constructed are none other than the grammatical ones (Vowles, 1970) or those of communication economy which arise from the principle of hierarchy such as it is presented by Dawkins (1976). However, every human taxonomic hierarchy fits in fact into a network of the type Dawkins presents (Fig. 3 ) and description of the insertion necessitates a clear representation of the ways in which the rate of adaptation of a System can interact with the states of adaptation of all the others. A schematic example will ”

environment

ENVIRONMENT

FIG. 2. Diagram of nesting within classes. Note that the one term “environment” covers degrees of progressive complexity exactly parallel to those expressed by the different words: individual, population, species, biocenosis; the increasing complexity of the environment refers not only to the inorganic part but also to the organic part of the environments where the biological system considered occurs (in Gautier et al., 1978).

ONTOGENESIS AND PHYLOGENESIS

233

FIG. 3. (a) Linear hierarchy (“peck order”). (b) Non-overlapping branching hierarchy. (c) Overlapping hierarchy. (d) Not a hierarchy. (e) Shallow hierarchy. (f) Hierarchy of loops. (9) Network. (From Dawkins, 1976.) enable us to better understand this problem. At nesting time, a bird can be described as a subsystem in a System made up of this bird and a clump of trees (the concept “trees” taken as “environment” includes, of course, all dependent links that primary producers maintain with their geophysical world, but also all potential food for the bird, insects, seeds, etc., which these trees conceal). But this same organism “bird” maintains other relationships with other plant forms, with conspecifics, with individuals of other species, etc., relationships which, during the time of an ecoethological analysis, can all be considered as parts of a stable System in evolution. Each individual studied then becomes the common denominator (we shall say the nodus ofrelationship making) of all the Systems that can be built when considering it either as a subsystem or as an element in a subsystem. Any tree in a clump where a bird nests could equally well be used as a center for starting relationships for many homeostasic Systems, including the bird or not. Step by step, and using diverse channels in the network of relationship making, we can describe, with different words, complex natural entities such as the

234

GASTON RICHARD

ecosystem or the enveloping System [biosphere, geosphere]; their homeostatic recalibrations constitute the Coevolution of Organisms and Environments. All that has been written above is aimed at emphasizing two facts: ( 1 ) Description of ethological dynamics of development cannot be conceived without describing simultaneously the environmental dynamics within which this development takes place, nor without taking into consideration permanent exchanges of information between the organism and environment concerned. (2) Words or classification systems used for a description of a phenomenon represent an organized collection of discontinuities projected onto the continuum of Nature in evolution. Only a good knowledge of ways and modalities of relationship-makingwithin and between systems may bring discontinuities closer to continuity.

11.

TOWARD A MODEL OF ONTOGENESIS

In order to draw up a model for ontogenesis, we have chosen first to refer to the class of Aves for several reasons. The main ones are as follows: This zoological group is relatively homogeneous from a morphological, physiological, and ethological point of view. However, it presents possibilities for interesting comparisons between precocial and altricial species. Published research is sufficiently extensive and sufficiently advanced to allow a near complete longitudinal study from egg to adult. Lastly, birds occupy, from an evolutionary point of view, a position which allows us to make inferences about more ancient, diversified classes such as fishes, even insects, as well as about “young”c1asses such as mammals. A.

IN THE NEST SITEOF GALLINACEAE

Leaving aside for the moment discussion of phylogenetic problems, we must state straight away the fact that the egg and the environment within which it will develop have a very recent history, which must necessarily take into account: the physical structure and biochemical composition of the egg, the position of the germinative disc on the yolk sac, and even the plane of symmetry of the embryo, all of which are perfectly definable in specific terms. But the brooding environment is just as susceptible to definition, whether altricial birds, such as Passerines (see Hinde, 1966), or precocial birds, such as gulls (Baerends, 1976), are considered. These facts are too well known for further emphasizing. I shall not mention all of the exchanges of information occurring on a biochemical level and ensuring embryonic growth and maturation, and I shall consider here only co-retroactive information connecting the developing embryo and the brooding environment

ONTOGENESIS AND PHYLOGENESIS

235

that gives heat and mechanical stimuli (turning of the eggs) essential for development. We must emphasize that the heat supply as well as the mechanical stimuli from egg turning are organized into quantitatively alternating cycles through the behavior of the brooder, which interrupts its task at regular intervals either because it leaves the nest for a moment and then comes back like a hen, or because it is relieved by its partner, as in gulls. This characteristic is fundamental, and represents the first synthetic information to be received by the embryo. It will be found again in practically all events in the incubation environment to which the embryo has access in relation to the progress of sensory maturation. Following Bateson (1976), I do not like the distinction between “general and specific effects,” but it must be stressed that cyclic supplying of heat, mechanical stimuli, and later vocalization conveys to the embryo at the same time the information ‘‘heat, ’’ ‘‘turning’’ or ‘‘sound ’ ’ and ‘‘temporal organization. ’ ’ This may be an ecoethological form of the parsimony principle (Schneirla, 1952; Baerends and Kruijt, 1973). Moreover, all present-day authors who have developed Preyer’s pioneering work generally describe motility of the embryo as rhythmic, even before it has come under the control of exteroceptive stimuli from the incubation environment (Hamburger, 1973; Oppenheim, 1973, 1974). Lashley expressed the belief that rhythmic motor activities “form a sort of substratum upon which other activity is built. They contribute to every perception and to every integrated movement” (cited in Oppenheim, 1974). Thus, the embryo has (no question of “consciousness,” of course) information about itself that has the same dual characteristics as those mentioned above: “movement” and “temporal organization of movement.” Some noteworthy events in the cycles during incubation (return of heat supply after turning over the eggs, for example) coincide, through the heat-metabolic activity link, with some equally noteworthy events in the embryo’s own motility cycles (intensification of movements when temperature rises). But, little by little, other types of coincidences are expressed, implying more particular phenomena. Impekoven (1976) suggests an arousal value for embryos in the turning over of the eggs; the next immediate maternal utterance would then be more effective. Gottlieb (197 1) showed that when the auditory system of a duck embryo becomes able to receive sound information coming from the environment external to the egg, the first motor manifestation of working of the auditory apparatus is an interruption of bill clapping by that embryo if maternal clucking occurs during a phase of mandibular activity. But, after a few hours (during the 22nd to 24th days of incubation for ducks), the embryo comes to place its periods of maximum buccal activity within periods when maternal cluckings can be heard. There is a real strategy of coincidence-making in which previously matured movements are organized in temporal patterns on the basis of both anticipation of activation of

236

GASTON RICHARD

motor activity and anticipation of presentation of sensory stimulation. I consider that this type of strategy has its roots in the long experience acquired by the embryo of reoccurrences, undergone passively at first, then awaited actively. In any case, this is a new fact in embryonic development, that represents a real incorporation (“assimilation,” Piaget, 1967a) of Time into the System [embryo, incubation, environment]. It allows more complex experience on exchange relationships within the System. We shall find some additional examples of this in ontogenetic development when, after the postural changes of tucking and draping, the embryo protrudes its bill into the egg air-space. It becomes capable of uttering vocalizations which are added gradually to auditory information from the environment. Moreover, these vocalizations contribute information to the other eggs of the brood and the incubating hen. Although it is not the most frequent utterance of Gallinaceae, the “cri d’equilibre psychophysiologique” (Guyomarc’h, 1972) (pleasure note, Colhas, 1952; twitter, Andrew, 1964) seems to play a special role at this time because maternal clucking represents the end result of its ontogenetic development and because the young utter it in phases corresponding to lesser constraints from the environment (relaxation phases after a thrust that has broken the shell). All happens in fact as if the link “twitter-clucking” established by self- and hetero-audition gave a special status of familiarization to this utterance and as if the correspondence between utterance and decrease of environmental constraints gave it anticipatory stress-reducing properties. Perhaps it should be emphasized here that twitters, first uttered separately, sometimes present a rhythmic form even before hatching: just under three cries per second. This shows that the rhythm of a motor act is part of the maturation of that act. Experience thus gathered allows new behaviors to be realized and expressed after hatching by the,intermediary of locomotor motility. The mother continues to utter long series of clucks, she remains the origin of heat and, under natural conditions, she leaves the nest only, on the average, 36 hours after hatching. The young continue uttering twitters and if they find themselves temporarily apart from the hen, they run to rejoin her. However these must not be viewed as new forms of strategy but only as the gradual substitution of sensorimotor channels through which the same types of stress reduction are expressed. Just on the basis of previous experience of familiar and unfamiliar, chicks can find the optimal environment to which hatching gave them access. Several researchers can be mentioned to support this opinion: When Gottlieb (1974, 1975a,b,c) devocalized ducklings before they could hear themselves in the egg, he depressed considerably their following reactions towards their mother or the choice of her utterances for 2 or 3 days following hatching; when young Lams atricilla were hatched in an incubator in the absence of parental incubating sounds (crooning) (Impekoven, 1976), these chicks did not show the strong approach response that such sounds elicit in young chicks reared by their parents.

ONTOGENESIS AND PHYLOGENESIS

237

There is no need then to postulate a discrete genetic basis for the behavior by a newly hatched altricial chick of following its mother. The visual system, which has become functional (Comer et a f . , 1973) while locomotor activity was completing its maturation (phylogenetic hereditary characteristics), is added gradually to the auditory system and to the systems of labyrinthine, cutaneous, and thermal sensitivities, as an analyzer of environmental events; but familiarity already established remains the basis of anticipatory strategies. Up to now, we have considered the role of the vocalization “twitter4ucking” of Callus gallus in establishing a familiarization. The other vocalizations, either because of their physical parameters or because of their time of utterance are also susceptible of acquiring either a status of familiarity or of strangeness that can confer onto them nun-value properties or redundance properties described by Mackintosh (1973). This was shown by Impekoven (1976) when she compared, through their effects on behavior of Larus atricifla chicks, several parental cries heard during incubation: “uhr” accompanying raising and readjusting on the brood and exchanges between parents, “crooning” accompanying reliefs between brooders during incubation, and later associated with feeding the young, and “uk-uk” and “kow” calls that are heard during alarms when the colony is disturbed by a potential predator or (kow) when conspecifics disturb a brooder. However, for one-day chicks reared by their parents, crooning elicits a strong approach; uk-uk suppresses activity and vocalizing leads to crouching; kow elicits similar reactions (suppression of activity) but with less intensity. For chicks hatched in an incubator and without prenatal sound experience, presentation of crooning does not activate them and when they are older it can have the same effects as alarm cries: suppression of activity and crouching. For chicks hatched in an incubator but having had the opportunity before hatching to hear several types of vocalizations, crooning and uhr have the effect of increasing postnatal responses to presentations of crooning, whereas kows have no quantitative effects on responses to those presentations; kow calling heard prenatally however seems to reduce its effect as an activity suppressor that normally possessed after hatching. Evans ( 1975a,b) adds to all this that vocalizations have species-specific effects (comparison between ring-billed gulls and hemng gulls chicks) and that the simultaneous presence of visual stimuli increases the effects of postnatal auditory stimulation (see also Tschanz and Hirsbrunner-Scharf, 1976). There must be seen in all this the problem of the gradual acquisition of a semantics as Guyomarc’h (1974a) has shown concerning the special status linking the chicks’ twitter and the hen’s clucking. The acquisition depends in great part on the form of frequency modulation of the vocalization. Gottlieb (1974) states a hypothesis that points in the same direction for wood ducks. It must however be specified that the amplitude of the sound stimulus acts in a cumplementury way to frequency modulation (law of heterogeneous summation, Tinbergen, 1951) with respect to the attractive value of this stimulus [Collias

238

GASTON IUCHARD

(1952) earlier insisted on the highly attractive value of low sounds]; this quality explains why neonates prefer the maternal cry to the juvenile one (Gottlieb, 1966). All this can form the basis, even before hatching, for chicks to rapidly develop an auditory recognition of their own mother, as each hen possesses an individualized clucking theme. As a complement to the above case, we can try to discover the roles played, for Gallinaceae, by other vocalizations emitted sooner and more frequently than the twitter, but with different physical characteristics (descending frequency modulation). Some maternal vocalizations with similar characteristics appear, in fact, nonattractive or only slightly attractive to newly hatched chicks, even chicks possessing prenatal maternal experience: this is the case particularly for the tidbit when it is not accompanied by the gestural components of the signal; it only becomes attractive after at least 24 hours experience of associating it with alimentary reinforcement. Thus, we can say that the quantitative aspect of the frequency of an event (vocalization, for example) is in itself insufficient to account for the phenomenon of familiarization implied as support for establishing strategies of young precocia1 birds. Therefore, familiarization does not imply only habituation; some hereditary qualitative aspects must be invoked: similarity between twitter and clucking, interdependence between vocal and locomotor systems, for example. Contrary to Andrew’s (1964) suggestion, Guyomarc ’h ( 1974a) considers in fact that integration of the hereditary form of some vocalizations (twitters especially) and successive movements which accompany them during maturation (coiling up of the embryo, which increases shell pressures; race towards the mother, ending in warming up by contact) are such that it is not possible later for chicks to condition their locomotor response without influencing correlatively the level of vocal response. Experimental proof of such links between motor mechanisms, besides, was demonstrated a long time ago by using conditioning procedures (Lane, 1961). Gottlieb ( 1 9 7 5 ~1976) proposes that the effects of vocalization on chicks are not only channelling, facilitating, and maintaining of the development of receptor functions but also the establishment of motivational state. The peculiar quality associated with twitters is social cohesion, interindividual attraction appearing permanently during phases of collective active assertion of control of the environment by chicks. But, and this brings us back to the symmetry in our System [organism, environment], for the hen leading her brood, clucking calls are, in the same way, characteristic of collective exploratory activity phases in the environment: they coincide more particularly with displacements and displacement intentions of the brooder; they play a part in decreasing the slight social tension which is created by variation of interindividual distances. The mother has been changed at the same time as the brood was changed: as Guyomar’h (1973) has shown, repeating Lorenz (1937) and Schleidt et a l . ’s (1960) observations, the hen kills a chirping chick placed in front of her

ONTOGENESIS A N D PHYLOGENESIS

239

on the edge of the nest, if this experiment is carried out before the period when vocalizations of chicks begin to become audible. But, letting a hen hear, for several hours, chirping emitted by a loudspeaker hidden among the eggs, allows familiarization and sound "exchanges" which later facilitate adoption. After hatching and drying of chicks, the hen does not go far from the nest site at first: she sits down frequently, fluffing up her feathers and clucking actively; this encourages regrouping of the chicks, and it is only gradually that the space between individuals increases and that, thanks to the use of all their analyzers, the young of a brood will learn, on the one hand, as Bateson (1973) said, to recognize characteristics of its mother seen from different angles and different distances, and to build up a composite picture of its parent's characteristics, and on the other hand, to differentiate on the basis familiarhonfamiliar or significanthedundant, motor tactics like "clucking-following the mother" and ''alarm callquick withdrawal under cover" (these progressive changes of maternal behavior simultaneously with changes of chick behavior are described for other birds by Beer, 1961, 1963a,b; Tinbergen, 1965; Tschanz, 1968; Tschanz and Hirsbrunner-Scharf, 1976; Norton Griffiths, 1967; Baerends, 1970; Evans, 1973; Impekoven, 1976; Impekoven and Gold, 1973) (Fig. 4).

FIG.4. Diagram representing the setting up of strategies in ontogenesis. The phylogenetic past enters into the egg and its environment, but the embryo's growth and maturation and changes in the brooding adult and the environment result in the emergence of successively more complex strategies.

240

GASTON RICHARD

In all this, and according to Bateson’s (1976) picturesque image, “the actions of adding ingredients, preparing the mixture and baking the cake, all contribute to the final effect. But this final effect is only a momentary stage in a continuous process of development, and the picture must be pursued by describing how mother and young (Gallinaceae, Anatidae, etc.) will leave the nest site, reinforce their own brood ties, then reintegrate the social group, separate at last (weaning) before experience of juvenile interindividual relationships will allow the young to express their adult behavior. ”

B. TOWARD ADULTBEHAVIORS The aim of this article is to show how interaction between mother and young gradually widens the experience of the letter and prepares for the establishment of their adult behaviors. The postnatal phase, lasting about 36 hours, spent on the nest site ensures in fact the formation of coordination mechanisms indispensable for resolving problems of group cohesion which will arise after leaving the nest, namely in feeding activity and in supplying maternal heat to compensate for the imperfect thermoregulation of chicks. In the System [hen, chicks], reliable interactions will be observed then, conferring particular dynamics to the System [brood, environment] (polyphasic modulation of activities, Guyomarc’h et a l . , 1973; Guyomarc’h, 1974b; Saucier and Astic, 1975). But these interactions have value according to our synthetic model of ontogenesis, only so far as we take into account as well psychophysiological modifications which occur within each partner (subsystem), modifications which can go as far as completely changing the significance of an apparently unique stimulus (the brooding hen from the experimenter’s point of view). That is the case, when, for the chick, oscillating between its tendency to feed and its tendency to acquire heat, the hen changes from being a signal for calm exploration of the environment to a consummatory object to reach quickly. Beyond Schneirla’s epigenetic proposal, we find here ideas previously expressed by Fentress (1976) on the role of interactions and self-organizationphenomena in modelling the dynamic limits of behavior systems. We shall not return in detail to the point concerning psychophysiological modifications that accompany the acquisition of semantics by vocalizations (Fig. 5 ) although, several paragraphs following, we shall meet a reminder of the fundamental characteristics of bond-forming behavior. This is one of the most widely studied behaviors over the last 40 years (cf. Hinde, 1966, 1974; Sluckin, 1972; Hess, 1973; Vidal, 1976) and even if most of the work has been done under artificial experimental conditions, we can gather from this work some important facts with which to build our model. During a special period after hatching, the young chick attaches itself to an object in its environment (the mother in a natural brood), but becomes slightly

ONTOGENESIS AND PHYLOGENESIS

24 1

Ib

/--\

FIG. 5. Acquisition of semantics by tidbit vocalizations and gestures (Gallus gallus). For adult (top), the vocal introduction, often a trill ( a ) is emitted with low posture. The rhythmic emission continues with erect posture (6). It is accompanied by particular gestural signals: vertical and lateral head tossings, jerks of the straightened and spread tail, simultaneous with successive elements of the cry. For chicks (bottom), no tail and no erect posture, at least during the first two weeks; thus, it is never a real presentation of a seed with the bill. When, between two series of juvenile tidbits ( c ) the chick stops, it briefly raises its head (or, if it is isolated, its entire body) and utters calls (a‘), but never tidbits, as the adult. (From J . C. Guyomarc’h, 1974a.) detached about a fortnight later. There are, however, no strict limits to this special period, and, in its permanent quest for relative stability of communication with the environment (adaptation state of the system [organism, environment]), the chick can show behavioral regression. This is more important the younger the individual and the richer the situations it has previously experienced (the natural situation compared to isolation, for example), but previously established bonds always represent a constraint which makes a regressing cockerel never exactly similar in capacities to a progressing chick in front of a “same” experimental

242

GASTON RICHARD

situation. Vidal(l976) shows this particularly well for gestural and vocal crouching behavior. Several authors have already described the capacity of young birds to show approach and following reactions towards different objects presented successively (Jaynes, 1956, 1957; Hinde e f a l . , 1956; Hoffman et al., 1972). Salzen and Meyer (1967, 1968) and Zajonc e f al. (1973) have even proved that in some cases this capacity leads to reversibility of the first imprinting in favor of the second training object. Jaynes (1956) notes, however, that this process is accompanied by a decrease in intensity of following reactions (decrement of generalization) and several authors consider that late imprinting is obtained more exclusively or more easily in subjects previously reared without social contacts or without precocious imprinting (Guiton, 1958, 1959; Salzen, 1962; Asdourian, 1967; Sluckin, 1972). Others consider that, of two simultaneously or alternately presented objects to young nidifugous birds, the one presenting species-specific characteristics will be preferred as the imprinting model (Guiton, 1961; Waller and Waller, 1963; Kovach et a l . , 1968). However, it seems necessary to qualify all these conclusions, as diversity in experimental procedures must make us cautious about making any generalizations. More particularly, time of exposure to a model is a very important parameter, as Hinde et a l . (1956) have shown; but also the age at which each individual is confronted with a particular situation influences the bond it establishes then. Vidal (1976) studied, comparatively. in an imprinting experimental situation, newborn chicks and 30-day old chickens, some of them previously reared in isolation and others reared with a similar-aged female, and showed that, in the oldest subjects, the emergence oT an intense bond towards a novel object seems to be obtained more easily by transfer of a pre-established bond with another object than by generalization of familiarization with a static environment. An objection could be raised, with justification, that these experimental situations are artificial and that it is very improbable that a chicken that has lived for 30 days in a natural maternal social group which has aged at the same time as it has, would suddenly be cast into a situation which is the same as during the first few hours of a brood. However, in certain contexts where interindividual stimulation and particular physiological states are found, behavior exhibited formerly by a bird can reappear and acquire a significance in thc balance of exchanges. Many authors have interpreted some phases and some acts of sexual displays of birds as a revival of juvenile behavior first included in feeding sequences (cf. review in Hinde, 1966; Huxley, 1971). Let us consider as an example the crouching soliciting call of Gullus gullus (“cri de sollicitation a I’accouplement,” Guyomarc’h, 1974b). The young chick with a warming-up tendency supplanting a feeding tendency, utters this sound while creeping under the standing hen, and hitting its head on the ventral part of her body. But broody hens at this time of the year are familiarized with this sound and with the association

ONTOGENESIS AND PHYLOGENESIS

243

“sound-sitting down”: during the weeks preceding the parental phase, they have often uttered a similar vocalization associated with an obvious tendency to sit down and to prepare the site for egg laying. The cockerel accompanying the hen to the nest is then strongly stimulated to express the sequence called “nest ceremonial” and to crouch down on his tarsus, cackling gently. Thus, the same ling “cry-behavior” first experienced while a chick reappears periodically when the couple prepare for the expression of parental behavior. The behavior of couples depends in many other ways on behavioral links elaborated by the young. Along with Vidal (1976), I consider that, for young cockerels reared in isolation, the expression of intense filial behavior towards a training model presented sooner or later after hatching, and later avoidance of this object in a sexual choice test, go together. However, cockerels reared in the presence of a similar aged female show, when placed in the experimental arena, intense following reaction towards the model and most of them prefer, without ambiguity in the expression of their sexual behavior, this model to a strange model or a species-specific partner to the familiar model. It appears, then, that an animal acquires during development an image of its sexual partner (in case of strict isolation, this image can be built through self-perception of parts of its own body accessible to individual perception). But the right correspondence between this image and the sexual object occurs only if ties first established with the earlier partner were not very strong and if these ties have been gradually transferred from the maternal object onto the sexual object through a social object. In short, the expression of sexual choice by an adult cockerel depends not only on the intensity of the precocial filial bond it developed earlier towards a maternal object, but also on the modes of construction of the filial bond and of the intermediary social bond. Thus, establishing a new bond necessitates moving a certain distance away from the object of the previous bond. Under natural conditions, at the beginning of exploration of the environment by the brood, the maternal object constitutes the support for all behavior of the young and the filial bond is at first very strong. But, during weaning, this bond loosens at the same time as other inter-young bonds are established within the social group: during this period, aggressive behavior, which develops gradually (Kruijt, 1964, 1973), certainly plays an important part in regulating interindividual distance, and prepares the future orientation of adult sexual behavior. It must be specified that these successive distancings by the individual from its conspecifics do not occur gradually, but rather show marked fluctuations. The progression-regression successions can be determined by diurnal rhythms of activity and rest or may result from some kind of external disturbance. Moreover, some facts make one think that bonds similar to juvenile ones persist throughout adulthood, both in males and in females: there is not a great difference in fact between the situation of the chick womed by its mother during weaning and

244

GASTON RICHARD

coming near the bill that is going to deliver more pecks, and the broader social situation of the dominated cockerel or hen, object for repeated pecks and thrusts from conspecifics, that nevertheless stays within that group. The dominating male, even if it seems more “independent,” nevertheless follows his females, or develops a more or less elaborate strategy to keep them near. Hih avoiding or aggressive reactions towards strange objects either spatially far from or near his bond object, are not unlike juvenile reactions of the same type. On the other hand, the cockerel separated from its congenitors, does not utter distress calls with a structure similar to that of vocalizations of newly hatched chicks, as does a hen separated from her chicks, but rather utters repeated songs and search calls, that is vocalizations already typically elicited in juveniles by social isolation (Guyomarc’h, 1974b). Sometimes even separation of adult males from their usual companions can induce the appearance of more marked regressive behavior. Schutz (1965) has shown that adult ducks previously filially imprinted to heterospecific partners before being sexually imprinted to conspecifics, show, before being separated from their partners, regressive behaviors such as following and search for proximity to heterospecifics resembling the filial imprinting objects. More generally, sexual behavior, which in the male consists of coming closer to a female that presents and has many features in common with the object that served as mother, is often preceded, for chickens and for many other species, by expressions of aggressive behavior, whereas the most usual immediate function of the latter is increasing the distance between an aggressor and the aggressed object. This apparent contradiction may be resolved if the fact is confirmed that effective expression of sexuality towards an object similar to the filial one necessitates first a certain differentiation of attitude (not an obligatory increase in spatial distance) by the subject from the bonded object or its substitute (here, the future sexual partner). Thus, one could explain something of the ambivalence of male sexual displays and the triple structure of motivation subtending them, which has been the interpretation given by many authors since 1950 (interaction between aggression-flight-sex): the display would encompass over a few instants toward the sexual object present in the environment, the warning of the effects of the early experience of the male, attached to, then detached from its mother, and led, at last, towards its adult capacities within the limits of a social subgroup of same-aged companions, where it finishes its psychophysiological maturation. This hypothesis, drawing on data from Vidal and many others, is, however, not complete and will require verification in the years to come. It leaves undecided especially three questions: How does it happen that the young, usually searching actively to maintain contact with its bonded object, manage to become detached from this object and to become positively attached to new objects that it avoided before? How does it happen reciprocally that the parental care led to

ONTOGENESIS A N D PHYLOGENESIS

245

indifference or aggression through weaning? By what mechanisms do filial attachment, seemingly similar in male and female chicks, manage, in nature, to be transferred onto two different types of heterosexual bonds? Of course, answering these questions necessitates complete study of the system [young, environment] (see Triver’s (1976) parent-offspring conflict theory) in which the importance of individual variations of ontogenetic construction and the reciprocal influence of each subsystem on the other must not be neglected. A N D CONSTRUCTION OF COMPLEX PATTERNS OF C. NATURE BEHAVIOR WHICH ASSIMILATE TIME

1 . Individual Patterns of Temporal Assimilation

Appreciation by a developing organism of its own periodicities (biochemical and motor) and of environmental periodicities (abiotic or biotic), then familiarization with certain recurrences and certain coincidences, leads as we have seen, to the expression of coincidence-making patterns of behavior that correspond to a first form of temporal anticipation: anticipation of regularities in the system [embryo, environment] (e.g., the gradual rhythmical construction of chick twitters, and the establishment of “conversation” with the mother). On this basis, temporal discriminations are established, then object discriminations leading to anticipated object presence, that gradually enrich discrimination and enable situations to grow more complex as new sensory and motor channels become functionally mature (e.g., increasing complexity of patterns of behavior gained from visual information and from the early functioning of the locomotor apparatus). Then a new step in complexity is established by comparison and transfer from one situation to another (e.g., mutual support of diverse channels described in the semantics of the tidbit call). Then generalizing the familiar-nonfamiliar dichotomy broadens the effect of temporal assimilation, enabling the establishment of patterns of behavior that can be defined as patterns increasing the probability an individual has tofind itselfat any time, confronted with a conspicuous object in the environment. (These are the ones we could see at work in the rhythmical expression of brood activities.) All this culminates in the form of patterns of behavior that “increase the probability of the young bird presenting itself with specific stimulus which it then goes on to learn” (Bateson, 1973). (Such form of activity ensures balance of the system [chick, model] during the phase of stability on filial imprinting described for Vidal’s chickens.) None of these patterns is exclusive of the others and the most complex ones depend on the previous establishment of less complex patterns (e.g.,the gradual acquisition of semantic value by sound signals).

246

GASTON RICHARD

Three remarks must now be made. (1) Setting up these successive and inclusive patterns of behavior during embryogenesis, and later during postnatal ontogenesis, cannot be described by refemng to the organism alone, but by refemng to an ecoethological balance of the system [organism, environment] which depends on fluctuations and recalibrations of the psychophysiological balance of the organism concerned, and also on fluctuations and recalibrations of the environment subsystem that is opposed to it (Fentress, 1976, Fox, 1972). (2) The interface of feedback exchanges between the organism subsystem and the environment opposed to it is considerably widened during development. The incubating patches, the eggs, the bill, and the feathers of the mother make up, with reserves in the egg, the first embryonic world of the bird. But, with psychophysiological maturation of the embryo and reproductive changes in the mother, the young chick will eventually find itself gradually faced directly with abiotic factors (cold, heat, rain, etc.) and with more complex biotic factors (mother, food, siblings, diverse social companions, etc.). (3) However, it must be considered that the gradual widening of the interface of direct exchanges between the developing organism and the entire environment within which it develops is itself constrained by its inclusion in a system of systems (see Fig. 2) on which phylogenesis acts (see below). 2 . Variability and Diversity of Ontogenetic Construction of Patterns of Temporal Assimilation Schneirla, Lehrman, and Rosenblatt have often insisted on the real plasticity that ontogenetic construction reveals to those who study it from an epigenetic viewpoint. They have been vigorously critical of discontinuities introduced into development interpreted in terms of innately determined stages (Scott, 1958a,b, 1962; Schneirla and Rosenblatt, 1963), and to its irreversibility postulated by those who followed Lorenz’s (1937) opinion on imprinting. Recent analyses have reviewed the problem and have opened it up again, either on the basis of the study of phylogenetic constraints weighing on the species-specific capacities of each individual and its environment (Hinde and Stevenson-Hinde, 1973), or on the basis of possibilities for an organism to reach, by different ways, first divergent, then convergent, a specific type of state (Bateson, 1976). In reality, this requires a clear distinction between the capacity an animal has, at a given moment in its development, to establish a conditioned link (described in classical learning theory terms) and the simultaneous capacity to derivefrom ir a strategy allowing other links to be established later. Selective attention theories and studies inspired by them have contributed to a better statement of these problems (Zeaman and House, 1963; Lovejoy, 1968; Sutherland and Mackintosh, 1971; Mackintosh, 1973; Andrew, 1976). These studies describe for the animal “a limited channel capacity for processing incorn-

ONTOGENESIS AND PHYLOGENESIS

247

ing information which prevents the simultaneous analysis of an indefinite number of events. However, constraints of stimulus selection may not always be a consequence of current limits on capacity but of a past history of exposure to certain relationships between stimuli and reinforcing events” (Mackintosh, 1973). Indeed, what we have developed above concerning variation of organismenvironment ties with time makes us assume a position different from the old conceptions of reinforcement as any environmental element with a similar quantitative effect on all responses of the organism, and comparative psychologists themselves have revised their approach to this problem since 1970 (Hodos and Campbell, 1969; Seligman, 1970; Bolles, 1970; Bitterman, 1975; Malone, 1975). However, there is more, and during its development an animal can learn that a stimulus predicts nothing (and it can learn to ignore this stimulus) or predicts change (and what change) or no change in the expression of a specific reinforcement. Studies by P. P. G. Bateson’s team have shed light on many processes of strategy construction, even if the too exclusive interest of this team for visual aspects of the link between nidifugous birds and their environment may be regretted. It is certain that young birds, as soon as a sensory channel becomes functional, respond more strongly to some stimuli than to others, and that waning of phenomena must take into account endogenous changes in the animal, as well as changes occurring in the environment. But we can say too with Bateson (1964) that it is the balance between familiar and nonfarniliar that regulates in great part successive phases of the development of behavior. This relates to what we said above: none during ontogenesis is a.. discontinuous with previous periods and later periods as is traditionally conceived. It must be stressed too that the animals’ own patterning of its activities (i.e., different motivational states, drives, moods, etc.) impose both discontinuitiesin its perception of the environment and also recurrences that add to the dynamics of the familiarization process: a chick sleeping under its mother escapes for a time from its visual environment, but each individual establishes a specific patterning of sensory modalities. Bateson and Wainwright (1972) illustrate very nicely the active role of the animal with respect to what it learns, and Bateson and Jaeckel(l974, 1976) show that the relationship between exposure time and preference for familiar objects is of a biphasic type: first, there is a greater preference for familiar objects, then a reversal of this tendency, and lastly the establishment of a stronger preference for the familiar. That this relationship cannot be observed in all individuals of an apparently homogeneous stock, and appears clearly only through the summing of a great number of individuals, does not abstract from its value, but rather stresses how individual variability in types of “dialogue” with the environment must be

248

GASTON RICHARD

constantly present in the experimenter’s mind while investigating ontogenetic processes. All the above results in young nidifugous birds building individual composite pictures of parental characteristics lead us to insist again on the fact that the elaboration of the visual image of the parent is vigorously sustained by the permanent “dialogue” between mother and young, mediated by sound utterances. Indeed, alimentary or heat reinforcements linked with tidbitting, for example, play an important part in building this image, but the role of conversation begun well before hatching and continued during semantic exchanges after hatching cannot be minimized in the widening of the familiar world. However, it is logical in a homeostatic system of the kind we are studying (system [organism, environment]), that any increase of one member’s ascendancy over the other produces a slowing down of the latter’s action on the first one. This is just what is observed in reality during behavioral ontogeny of a young bird. Bateson has contributed greatly to building a model conveying the fact that, when a social bond of familiarity is established with one object, the range of social objects the bird responds to positively becomes restricted. There is here, of course, an effect based upon differences between the familiar object and the other objects; it can be expressed as a constraint of the environment on the animal. But, simultaneously, the bird tends to respond more to stimuli that differ only slightly from those which have become familiar through previous exposure. This can be interpreted as the resistance of the “organism” subsystem to constraints imposed by the “familiar environment” subsystem on its continuing efforts to explore the world. Bateson (1973, p. 11 1) expresses this fact by saying: “as the birds learn more about the familiar, objects that are detected by them as being slightly novel will in reality resemble more and more closely the familiar object. At each moment during its development therefore, and under conjoined pressures from the actual environment and experience, the nidifugous bird prepares its future behavior by reinforcing positively the composite images of familiar objects, and negatively those of objects which differ obviously from those it knows. But there is more to it: by its behavior toward the familiar object, it increases the probability of finding itself near it and of remaining near it. It looks for it in its absence and ceases behaving in its presence. As many authors have noted (Bateson, 1964; Kovach er al., 1968; Polt and Hess, 1965; Chantrey, 1972) experience in one situation may facilitate transfer of behavior to another situation. Similarly, what is familiar and unfamiliar in the present may, through transfer over time, affect an animal’s response to future experiences and serve, therefore, to preadapt it to the future. It is obvious that the animal never has direct knowledge of future situations before being plunged into them; its mastery of past strategies must be sufficient to enable it to dominate situations that it ”

ONTOGENESIS AND PHYLOGENESIS

249

recognizes as novel when they are presented. There are these preadaptive properties that give the ontogenetic construction of behavior its own characteristics, and taking them into account allows, as Schneirla already proposed in 1935, adult learning to become simply a particular case of behavioral plasticity. However, relationships between precocious learning and later learning are not simple. Bateson and Chantrey (1972) have shown that, with chickens which have been presented with two stimuli in rapid alternation, learning to discriminate between them takes longer than learning to discriminate between stimuli with which they are unfamiliar. However, if alternation is long (half an hour of exposure for each stimulus), then discrimination between known stimuli is quicker. It seems very important to us that two factors separable by our measuring apparatus can or cannot take on the same identity in a system of “classification of the world” by the arrival, simply as a function of their temporal sequential organization in the environment. Here, time is not an aspect of stimulation as in the previous facts of assimilation, but its role for “sensibilization” must be, nevertheless, appreciated as a part of that function, where behavior plays a fundamental motor role. This can be widened in other respects to the formation of more complex concepts, a point we shall develop in Section 111.

111. TOWARD A MODEL OF PHYLOGENESIS A.

CONVERGENCES A N D DIVERGENCES OF ONTOGENESIS OF PRESENT SPECIES

Principles stated in earlier sections can certainly be generalized from nidi’fugous birds to other groups, as long as ontogenesis is studied within the same limits of a gradual functional transformation of terms and interaction of terms (Hinde, 1961, 1963, 1974) in [organism, environment] Systems belonging to the family of Systems described in the Introduction. In the ontogenesis of either altricial or precocial birds, birth does not have the importance that some authors have assigned it in the development of vertebrates; this continuity cannot be doubted either for heterometabolous or holometabolous insects (Thorpe, 1938, 1945), even if the slow psychophysiological preparation of the next stage of ontogenetic construction escapes those who see only the rapid morphological transformation of molting in metamorphosis. We shall not insist here on similarities in the course of ontogenesis. However, we shall try to define, comparatively, species-specific characteristics observable during development which, once again, reveal the weight of the phylogenetic

250

GASTON RICHARD

past on the egg: the bill of chicks pecks, the bill of ducks dabbles (Lorenz, 1965), even if the feeding behavior of both birds can be described in similar terms of time-assimilating strategies, built gradually. Restricting for the time being our examples to Amniotes, it is important to note the close similarity in the temporal succession of initial functioning of their sensory organs during development (Gottlieb, 197I ) , the striking convergence of hatching mechanisms and movements of those developing in eggs outside the maternal organism (Oppenheim, 1973), the very similar preadaptive roles of embryonic strategies with regard to juvenile strategies (Coghill, 1929; Hemck, 1956; Mittelman, 1960; Kestenberg, 1965; Wolff, 1966; Piaget, 1970; Oppenheim, 1974) and juvenile strategies with regard to adult strategies (Kuo, 1932; Myer, 1969, 1971; Johnson et a l . , 1972; Ewer, 1968, 1969; Karli, 1956; Fox, 1969; Rosenblum, 1971; Eisenberg and Leyhausen, 1972; Hutt, 1973; Leyhausen, 1973; Polski, 1975a,b). But it is no less important to compare phylogenetically and ontogenetically the functions of discrimination and transfer capacities, because these express the result of analogous pressures of natural selection and ensure the possibility of individuals organizing strategies in relation to their environment. Warren’s (1974) excellent review shows to what extent traditional experimentation on learning misled the comparative study of animal behavior: the importance of man’s visual system (differential characteristic of primates among mammals) led to presenting problems to animals and to classifying their performances within this reference system without being concerned fust with describing their specific Urnwelten: a dolphin or a rat may seem very much “lower” than a monkey in front of a visual learning test, whereas their capacities become similar if the same test is presented to the dolphin through the auditory channel (Herman et af., 1969; Herman and Arbeit, 1973) and to the rat through the olfactory channel (Warren, 1974). In the same way, specific motor uniqueness must be taken into account when capacities for organizing the environment by primate, rodent, carnivore hands and by the combination bill-foot claws of birds are compared. This said, it must not be forgotten that mammals “can learn better, learn more, remember more and show more insight” (Ewer, 1968) than most other vertebrates. It must not be forgotten that Chelonians and many other reptiles show little plasticity and mobility when faced with learning problems, that “rhesus monkeys differ from cats and other non-primate species in their ability to develop generalized, transituationally valid response rules during training on a specific problem-rules which mediate the process of positive transfer in a new test situation. Cats and other non-primate mammals develop strategies or rules, they appear to be specific to the particular task on which they are trained, and not generalizable to other situations in which the same type of strategy would be appropriate (Warren, 1966, 1974). Then, monkeys differ from cats in their

25 1

ONTOGENESIS A N D PHYLOGENESIS

greater ability to suppress the process of transfer from previous learning experiences when it would be inappropriate to the task at hand (Meyer, 1960; Wilson et al., 1964; Poland and Warren, 1968; Schweikert and Treichler, 1969). . . Thus. . . macaques acquire a variety of learning sets, involving complex relations for the solution of multiple sign problems like oddity matching from sample, and conditional discriminations (Bessemer and Stollnitz, 197 1; French, 1965). Chimpanzees show language-like behavior (Gardner and Gardner, 1971; Menzel, 1971; Premack, 1971; Rumbaugh and Gill, 1973), solve intermodal matching problems (Davenport and Rogers, 1970) and learn to recognize their reflection in a mirror (Gallup, 1970). Monkeys and great apes appear to be unique among nonhuman mammals in respect to the number and variety of tool using performance they emit (Van Lawick Goodall, 1968)” (Warren, 1974). In all that, it must be considered that at each phylogenetic level, the origins of the distinct types of regulating behavior have roots that plunge into the individual ontogenetic past (Bateson, 1976) and that learning as described for adults is only a restricted particular case of specific experience acquired by the young (Schneirla, 1956). From this point of view, the capacity for expressing delayed responses is particularly important. Etienne (1973) considers it a phylogenetic and ontogenetic precursor of object permanence and on these grounds she compares Aeschna nymphs for which “an extended experience with vanishing and reappearing prey does not modify the form of orientation of searching responses,” domestic chicks “which represent a step in evolution towards behavior not solely controlled by immediately perceived external elements, kittens and human infants for which “the development of object permanence proceeds on the same lines, with the difference that it progresses more quickly and stops at an earlier stage in the kitten than in the infant” (Etienne, 1973, p. 393). Ontogenesis of emotional behavior no doubt enables us to sharpen phylogenetic comparative studies, even if interspecific differences appear to involve more a quantitative than a qualitative dimension. According to Candland (1971), the most elaborate expressions are always built from a general reactivity, observable as early as birth; however, rodents possess only limited potential for expressing emotional responses compared with other mammals and even with chickens which, from this point of view, are very near carnivores. As for human ontogenesis, it is differentiated from that of other mammals by a strong link between the development of socialization and that of emotionality, and the length (in absolute values) of this period of development separates man from the other primates. Temporal anticipation, successive discrimination and familiarization, the combination of central and peripheral physiological factors, a wider and wider access to a vaster and vaster world, constitute the common basis of development in all vertebrates (Brusset, 1971, 1973; Immelman, 1972a,b; Hinde, 1974; Rosenblatt, 1976) and we will not describe them in more detail. However it is ”

252

GASTON RICHARD

important for characterizing species to devote some attention to the analysis of attachment processes and to transfer processes revealed in imprinting exemplified by Allyn (1974) and Hinde and Stevenson-Hinde (1976). It is obviously during the study of the development of relations with the social environment, or more widely, relations with other individuals of the same species or of different species, that it is possible to develop comparisons which could help to establish whether the animal has knowledge of the taxonomic group to which it belongs (Lehrman and Rosenblatt, 197I ) . Even if adaptative characteristics of altricial and precocial species are phylogenetically different (Klinghammer, 1967; Immelman, 1972a), many arguments militate in favor of a single type of imprinting hypothesis, on condition that this imprinting is defined, with Bateson (1966) “as a process:-which restricts social preference to a specific class of objects;--of which the behavioural manifestations become restricted to stimuli first eliciting them. ’’ On these grounds, it is useful to realize to what extent “following” relationships are similar in kind, although differing in their motor aspects: proximity strategies of the chick are expressed through its locomotor system, but altricial birds are capable of equivalent strategies expressed through motor systems in their possession at any time during their development: many parent-young exchanges in altricial birds can be described in approach withdrawal terms (Schneirla, 1965) very similar to those used to describe embryonic behavior, but as soon as these juveniles have access to sufficient postural and locomotor capacities, exchanges take on a form more similar to that of the following reactions of precocial birds (Brosset, 1973). Ocular movements or smiles of a very young human baby [this young is altricial on a motor level but precocial on a sensory level according to Gottlieb (1971)] have often been interpreted as equivalent to the following reaction of nidifugous birds (Gray, 1958; Ambrose, 1963). But in all cases, it is obviously the learning associated with following rather than the form of the following itself which represents the essential factor and which constitutes the point of convergence among diverse species. It is on the mother-young dyad (or parents-young triad), as an early unit of social interactions, that rests, through reciprocal relationships, the capacity for transferring acquired strategies to more complex social situations (Sander, 1962, 1964; Hinde, 1961, 1963, 1974; Allyn, 1974). de Ajuriaguerra (1976) insisted recently on the impossibility of describing the human infant without relationship with the “other” (Baldwin’s “socius,” Wallon’s “alter”) and without the mother-infant relationship during the first exchanges (Winnocott ‘s “holding, Ajuriaguerra’s “maintenance”). Dialogue, established at first on a protopathetic level, is rapidly widened (Hinde, 1963) and for primates, but more especially for man, the face and particularly the eyes, play a considerable role (Fantz, 1963, 1965, 1966). “Eyes are the most light reflective part of a natural face, they contain great contrast within themselves and in relation to surrounding facial ”

ONTOGENESIS A N D PHYLOGENESIS

253

features, they are in continuous movement, and they are the most responsive part of the face, registering changes more quickly and more consistently than other parts” (Allyn, 1974). The importance of the mother’s body as the first clinging object (sustained for monkeys, discontinuous for man), as the first plaything and as the first basis for understanding the world for primates (Hinde, 1974) must make us consider relationships maintained by genitors with the world around them. If there are practically no animal species that lay eggs haphazardly, there are many with eggs that develop along though laying does not happen randomly (rhythms of marine invertebrates). However, for some species (Lamellibranch molluscs that are either fixed or hardly mobile when adults), adult laying strategies of rhythmic coincidence-making combine with complex larval strategies of spatial utilization of the environment: the group fixation of larvae on the substratum favors massive release of sexual products when neighboring individuals reach reproductive maturity. Many sea fish and many arthropods hardly surpass molluscs so far as care for the development of their young is concerned; for other animals, the body of one of the adult genitors is used as support only for embryonic development (crustacea, midwife toads, vipers, etc.); for others again the environment, previously prepared thanks to stereotyped behavior patterns, receives the eggs and protects them from the direct action of abiotic factors through a specific microclimate (spawning grounds of fishes, sand in Pacific Isles for marine tortoises, egg laying of lymantriid moths, etc.). Often, it is the body of the adult and slightly prepared areas in the environment that are simultaneously used as the temporary environment for embryogenesis, at least during the first moments of postembryonic ontogenesis (not only scorpions, lycoside spiders, ovoviviparous cockroaches, but also syngnathid fishes and mouthincubating fishes, are some examples). A certain complexity is reached when adult behavior projects around the body a space defended against any intruders of the same sex and species, as a nesting territory where at least embryogenesis of offspring occurs. For vertebrate ethologists, many examples come to mind, from the stickleback to passerines, megapods included also. Arthropods are no exceptions, as, for example, the nursery webs of Agelenidae and the burrow nests of earwigs. The greatest complexity is reached when, in the Gallinaceae and other nidifugous birds, in most carnivorous mammals, and in primates, close mntheryoung bonds established at the nest site or parturition site are continued in a wider and wider environment. But it is not enough to describe how reciprocal bonds develop between mothers and their young, first in a nest, then in a wide environment collectively explored, or to describe the role of these bonds in the future social integration of the young. We must also analyze in turn in our [organism, environment] System, modes of social life which allow a mother ready to lay, or to give birth, to isolate herself from the group to which she belongs (interindividual distance taking) and

254

GASTON RICHARD

to rrunsfer temporarily onto a geographical nest site her own capacities for attachment. This leads to posing in similar terms the problem of seasonal attachment of a male to a restricted copulation or nest-building territory, and the problem of the corresponding organization of his relationships with conspecific males. Such a generalization of the use of the attachment concept, that makes it describe apparently nonmutual bonds established between an animal and nonsocial objects in the environment (topographical landmarks, for example), is justified also by the quality of the psychophysiological balance shown on this occasion, and by community of outcomes of diverse strategies used by conspecific individuals. The case of raptor-male sticklebacks described by van den Assem (1967) is an example; not having built a nest, these males elaborate substitute tactics that allow them to take over the nest and territory of another male just before the latter fertilizes the eggs he has made a female lay. [The important paper by Immelman (1975) supports the same idea of the “ecological significance of imprinting and early learning.”] Of course, the topographic environment to which an animal becomes attached either temporarily or permanently does not project onto this animal mutual bonds on the same basis as the social partner does. It changes nevertheless at the same time as the individual and its species and can even constitute by its own structure, as well as by the modifications brought to it by building activities, a taxonomic characteristic of great value. The transitory attachment to the place of the eyrie that characterizes the behavior of most young birds of prey during a privileged period of their ontogeny (Brosset, 1973) is an example, but the site and arrangement of spider webs, of bird nests, and of collective buildings by social insects are other examples. These problems of successive attachments to very different objects, of various transfers, of partial regression, lead us to emphasize once again that discretion must be used concerning comparisons of results from different studies that are not always comparable [cf. difficulties interpreting isolation experiments, Brain (1975)], and that, contrary to what was earlier believed, the regression observed in any ontogenesis must not always be considered as pathological, but as an integral part of normal ontogenetic development, facilitating the later progression of relationships of the individual with its dynamic and changing environment. [Kortlandt’s (1955) cormorant data are an example of such a view. J Phenomena of developmental plasticity have now confirmed the possibility of treating with psychological procedures serious syndromes of social stress [rehabilitation of isolated people, Suomi ef al. (1974)l. It would be an error to believe that such plasticity characterizes only primates: what differs, once again, is not the quality of the phenomena, but their quantitative importance and their relative duration. Even insects provide examples of interdependenceof ontogenetic factors and social pressures, as Grass6 has shown for termites. Studying Culotermes flavicollis (it is the same for the other termites), Grasse (1942)

ONTOGENESIS A N D PHYLOGENESIS

255

showed that before achieving psychophysiological maturity, reproductive individuals need to go to a distance from the social group within which they developed. This separation, moreover, is prepared and ensured by the group itself and the [termites, termite nest] System expresses this cyclically in the form of seasonal swarming. It is only after this separation from the colony that genital inhibition imposed by participation in the society is lifted from reproductive adults, which then start to found a new colony. If particular circumstances prevent swarming by at least some adults, these individuals can remain confined in the termitary for a long time, in contact with other individuals, without reaching psychophysiological sexual maturity ( ‘‘achrestogonimes’’). But an additional argument concerning the reality of this social pressure can be drawn from another fact described by Grasse and Noirot (1951): sociotomy. Under diverse circumstances, part of the population of a termite nest may emigrate, and form a new social group elsewhere. In the emigrant’s colony imagos are often observed taking part in the general movement, but none of them flies off once they are in the open as they would at the time of swarming. Equally noteworthy observations on the interaction between young and the entire insect social group, passing through the intermediary of females tending to these young, were made some time ago by Schneirla for Eciton ants, or by von Frisch for bees; they have been amply confirmed and developed since then by Rettenmeyer, E. 0. Wilson, and Lindauer, among others. Jaisson (1976) adds to this the importance for Formica workers of a privileged period following their emergence from their cocoons and which allows them to acquire a familiarity with stimuli from species broods. Montagner (1967), first for Vespa wasps and then for bees, proved to what extent form, frequency, and sequence of stimuli exchanged during trophallaxis between an old nursing worker and a young worker just out of its cell play an organizing role in the future social relationships of the latter. Gautier (1974, 1976) widened this perspective even more with his study on Blaberid cockroaches by describing the many observable interactions between special structures in the natural environment of tropical caves that constitute their habitat in Trinidad (ground cover with bat guano, anfractuosities or reliefs of rockwalls, etc.), biotic factors represented by the quality and distribution of food sources and by the presence or absence of predators, conditions under which larval ontogenesis occurs, etc. The complex results of such interactions are measured by the way the interindividual relationships (sexual relationships, intermale aggressive relationships, adult-nymph relationships) of its adults are organized in relation to the local density of the population and the possibilities offered by the environment to modify this density. We are then really confronted with the necessity for a multifactorial sociobiological analysis of the type recommended by Margaret Mead (1972) (who knew how to study children and to include their development in all culture, thus introducing a dynamic element in the description of the life of a society) or

256

GASTON RICHARD

as recommended by Crook er al. ( 1 976) with ontogenesis a central fact studied in the parental and social group within which it occurs, but also producing repercussions on the phylogeny of social organization through the intermediary of the biological necessity of breeding young. This joins with the idea that is emerging more and more strongly according to which the young itself is considered as an active element in its own learning acquisitions (sucking behavior: Wolff, 1968; Friedman, 1975; Wakerly and Drewett, 1975; predatory behavior: Polsky, 1975a; playing behavior: Poole and Fish, 1975) and even as primary effector of its own socialization (Fragaszy and Mitchell, 1974; Deutsch and Larsson, 1974; Blurton Jones, 1972; Rosenblatt, 1976; Hinde, 1974). Because young transfer new learning from their parents to other individuals, make this parents all the more important as an environment for the development of their young. They themselves should have had a harmonious development (Barnett, 1975) and have gathered experience concerning relationships with the species characteristic environment for use during their own reproductive phase (Lehrrnan and Wortis, 1960; Hinde, 1974). All this leads us irresistibly to call to mind from a phylogenetic point of view the role of interindividual communication in social groups. Trophallactic behavior and its phylogenetic specialization expressed in bee dances plays a very important role in group cohesion of eusocial insects that practice collective rearing of brood. But this is no more than a pattern of behavior allowing an individual to be present at a significant point in the environment at an equally significant moment (see Section 11,C). On the other hand, communication in vertebrates leads phylogenetically to communication in man, which represents a qualitatively new time assimilation pattern, since working in the abstract can include the past as well as the future in a decision about action in the present environment. Two of the most important characteristics of this strategy are that it must be elaborated individually from hereditary capacities peculiar to our species and that the environment within which this elaboration takes place is precisely the parental environment included in the social environment. The slow human development ensures this controlled acquisition of the projection of the vocal motor acts onto the environment and their organization according to a conventional grammatical structure which enables us easily, and in the abstract, to dominate spatiotemporal contingencies of the natural environment, so that physiochemical constraints thereby become less determining. Two properties of communication must be especially called to mind on the level of phylogenetic convergences and divergences: the abstraction property and the property of projecting the abstract onto the concrete. The Kellogs’ or Madame Khots’ studies, remarkable at the time they were carried out ( 1920’s), which distinguished the ontogenetic development of chim-

ONTOGENESIS A N D PHYLOGENESIS

257

panzees from that of human infants at the stage where the infant begins to master abstract language, must be considered in the light of studies such as those of Piaget, Ryan, Goodall, the Gardners, Premack and their teams. It is certain that the radical dividing line of verbal expression exists, but research on other forms of expression of abstract thought proves that evolution towards reasoning strategies in phylogenesis was widely prepared by other types of time assimilation strategies and by a slow elaboration of modes of representing the facts of the concrete world. Conversely, it must be realized that in the evolution of man, from Austrulopithecus to us, as in ontogeny from a few months old baby to an adult, it is direct practical knowledge of objects and their material relationships which remains the foundation of experience of the world. Abstract images of the Pavlovian second signaling system are gradually widened by degrees, by becoming strongly established in the concrete world through representations in the first signaling system. Searching images, known to the experimenter by the risk which the prey of stickleback incur (Beukema, 1968), by the breeding success of tits (Tinbergen, 1960) or by decision making tactics in the environment (Croze, 1970) represent certainly [in spite of Royama’s (1970) criticisms of this concept] a rough form of abstraction belonging to the type of spatiotemporal systems representing details or entities (a series of motor decisions, understanding of proximity of a reinforcement, etc.) abundantly described by experimental psychologists. All problems of short-cuts, locomotor detour, reaching detour, use of instruments, generally lead the animal, after a certain number of trials and after testing diverse kinds of “hypotheses,” to a reorganization of behavior in relation to the task to be carried out. The reorganization, its rate of realization, and its efficacy depend on the phyletic level of the animal considered and, even if the existence of insight, abstraction of forms or of numbers, and categorization of concepts, can be described for many vertebrate species, the real complexity of problems solved differs widely from one species to another. Let us indicate lastly that strategies of diverse individuals of the same species faced with the same problem can differ in some of their details (Koehler, 1950; Etienne, 1973). Logicomathematical knowledge (Piaget), which acquires a large degree of independence from objects themselves because it depends on general coordinated actions exerted by the subject on these same objects or their representations, can be established and broadened only within the social conditions in which human phylogenesis and ontogenesis take place. It would be an error, however, to discuss such a genesis within the outdated framework of an opposition between hereditary factors (innate) and strictly individual experience (acquired). Peeling the human behavioral onion would no longer enable us to reach the “animal core of human behavior by separating superficial layers of modifications im”

258

GASTON RICHARD

posed by cultural factors and by the practice of individual rational thought (Martin, 1974). But mixing Bateson’s cake gave us a picture of a permanent intermixing of characters during ontogenetic construction. What seems important is to appreciate “the value of concentrating on what animals can communicate rather than or before, examining how communication is achieved” (Hinde, 1974), and to what extent capacities for abstraction by animals and man are used within the limits of the [organism, environment] Systems to which they belong. Their use to organize strategies that create real distance from the concrete environment would, in the model of phylogenesis we are building, present properties comparable to those present in the strategies described in our model of ontogeny which ensure, for an individual, gradual distancing from an object and transfemng onto another object the functions of the previously elaborated bond. The animal body and the immediate environment around it, can be used to express a single abstract message: “I am not here” (cryptism) or “I am here” (intimidation display), or “I am another” (mimicry); but they can also ensure precise identification of an individual at a given moment and they can identify its social rank (vocalizations, Marler, 1960; Guyomarc’h, 1971, 1974b) or characterize a personal state of preparation for a give11 species-specific action (the products of emancipation and ritualization of motor acts). They can, finally, be used to characterize a state of an environment with an important biological significance for the species (mobbing gesture). Thus, the body may, during ontogeny as well in phylogeny, be the support, the center, and the place of exchanges for interindividual relationships; and it can also gradually annex part of the environment; and then transform it, thanks to the impact of individual organs used as instruments (bills, claws, teeth, etc.). The example of courtship gardens built by Australian bower birds is representative of this. But it is only in man that such a capacity is widely developed. Indeed, he alone became able, during his own evolution, of furthering the separation that extends by a tool the bodily instrument and that, not only with material tools, but also with language. He thus definitively separates the active qualities of tools from the motor qualities of hands, by transferring to other energy sources the motor force which a tiny act on his part is then sufficient to liberate (releasing a programmed process in automatic machines. for example) (Leroi-Gourhan, 1965); but he separates equally definitively, vocal emissions from their primary emotional concomitants. This separation is gradual during development, but the subtlety of many communication processes makes it sometimes difficult to uncover the real development of phenomena. Studies of Condon and Sander (1974), who describe “a sustained synchrony of organized correspondences between adult speech and neonate body movement (as early as 12 hours to the 14th day after birth) at a macrokinetic level within epochs of less than a second,” question again, but

ONTOGENESIS AND PHYLOGENESIS

259

through specific particulars, the role of rhythms during precocious development and the role of the auditory channel in the maturation of behavioral strategies in diverse vertebrates. It is now accepted that human children respond to the sound of heartbeats (Salk, 1973; Weiland and Sperber, 1970; Tomatis, 1963) and to sounds with human voice characteristics even before they are able to respond to facial stimuli (Hutt et a l . , 1968; Eisenberg, 1969; Eimas et al., 1971); as a counterpart, mothers respond differentially to their children’s cries (Fornby, 1967). But there is more, and Condon and Sander “suggest that the ‘bond’ between human beings should be studied as the expression of a participation within shared organizational forms rather than as something limited to isolated entities sending discrete messages” [convergence with Thorpe and Hall Craggs’ (1976) opinion on bird song]; (see also Demany et al., 1977 on a complex tangle of signals which will at first release mother-child exchanges that provide immediate satisfaction of physiological needs and the expression of elementary emotions, and which will then lead to the pleasure of communicating for the sake of communicating). This interaction will enable both dyad members to adjust their behavior during progressive changes in the other’s behavior (Hinde, 1974), and as the child tries with appropriate signals to influence what the mother is going to do, she will facilitate her child’s social introduction and language acquisition (Ryan, 1973). It is then that behavior depending on attachment (Bowlby, 1969, 1973) is incorporated into complex systems directed towards goals that serve to maintain mutual proximity between mother and child, and to prepare future relationships of that child with other “socius. “Thus, the infant is not passive clay which the effects of experience are imprinted. Just because he shows particular responses, just because his perceptual abilities are organized in particular ways, just because he actively explores his environment, he selects some forms of experience and bypasses others, thereby constructing his own environment. What he learns is constrained and directed by what he is” (Hinde and Stevenson-Hinde, 1973), and according to Mead’s (1972) nice formula: a baby tells one a lot about mothers, even if they already know a lot about babies. But it is not without value for the problem we are developing to stress that the human child is characterized at the beginning of its development by a cultural polymorphism (Levi-Strauss) through which the social group to which it belongs exercises a canalizing effect on development. From this canalization there results a particular type of relationship with the environment, and a structuring of adaptative anticipatory and conditioning possibilities, and also the initial capacity to perceive one’s self in the environment (individuals belonging to tribal societies seem to perceive themselves as widely included in the environment, whereas individuals belonging to individualistic societies perceive themselves as more separate). This, after all, represents only one particular aspect of conceptualizing subjects and objects. ”

260 B.

GASTON RICHARD

FROM THE ONTOGENESIS MODELTO THE

PHYLOGENESIS

MODEL All that has been said in the previous section should enable us to realize to what extent ontogenesis and phylogenesis combine in the expressidn of behavior. But we must acknowledge that Tinbergen’s (1963) formulation of the four fundamental questions asked by a modem ethologist has constituted probably one of the clearest recent stimuli to begin a phylogenetic functional analysis of ontogenetic development. The most important dangers to avoid seem to us to be those of representing phylogenesis by a series of examples from the simplest to the most complex (in form or in behavior) taken from present-day nature, and describing ecological dynamics of secondary successions and not of primary successions (“succession” refers here to the continuous transformation of biocenosis ending in the climax equilibrium, each of the biocenosis being responsible for a part of transformation; the primary succession corresponds to the first implantation of life on earth; the secondary succession reoccupies the same geographic area after total or partial destruction of the first one). Research in the field of evolution has often gone astray because of the considerable weight of the concept of “Great Chain of Being” (Lovejoy, 1965) or the no less important weight of the concept of “reflex” (Canguilheim, 1955), which ends too often actually in favoring the S-R tie, treating activity of living organisms as secondary to reacting to environmental events. The permanent interaction between the organism and its environment, the preadaptive links and their adaptive consequences, the succession of patterns of behavior assimilating time, all renders individual development strictly canalized, but at the same time its results vary individually in relation to the genotype inherited from parents. Then, only one of the phenotypes made possible by this genotype is expressed (behavioral potentials, Kuo, 1967). These properties are also those of phylogenetic development, with the dual condition that it is studied with a suitable time scale and that the definition of a species not be restrictive. Study of phylogenesis in slices of hundreds of thousand of years taken at random within a phylum renders evolution just as discontinuous as the study of the ontogenesis of chickens in slices of a few hours taken at random during the development of an individual. It is necessary to establish with regard to phylogenesis a perspective which embraces 3 thousand million years in the same way as the first 30 days of embryonic and postembryonic life of a chicken. It is then that species in phylogenesis and stage in ontogenesis take on at the same time value as instantaneous reference, and as a link in a chain of transformations [fusion of classification and relationship forming, according to Nowinski (1967)l. Then evolutionary radiation of organisms faced with their environments appears as the radiation of strategies in ontogenesis.

ONTOGENESIS A N D PHYLOGENESIS

26 1

Studies of population geneticists, in particular of Dobzhansky’s team and of Mayr and his disciples, have amply shown that what we name “species” in a classification scheme can only characterize a continuum of space and time from which the inability to exchange genes between organisms at first cross mating emerges gradually. The evolutionary radiation of forms that follows is accompanied by an evolutionary radiation of behavioral strategies and an evolutionary radiation of environmental complexity. This of course leads to a divergence from a picture of the past that would be a simple projection, onto more and more remote periods, of present day [organism, environment] Systems belonging to different classes that human conventions have differentiated from nature. Such a projection would block understanding of phylogenesis in the same way that the learning concept in the 1930’sblocked the use recommended by Schneirla of an ontogenetic analysis in terms of maturatiodexperience and in terms of approachlwithdrawal processes. The consequence of these remarks is that, on the level of diversified evolution, it is obviously ridiculous to try to make a hierarchy of behavior (reflexes, instincts, intelligence. . .). Indeed, no organism can be studied outside the evolutionary environment with which it interacts; no [organism, environment] System can be characterized by a single type of interaction; and especially, the balance of forms and behaviors observable nowadays at a given moment in the development of an animal, can only be interpreted in its entirety through general or particular functions assumed by that form-behavior entity interacting with the environment in a system in the course of change. The difficulty for paleontologists comes from the fact that shapes have left sufficient fossil traces to reconstitute evolutionary lines, but behavior has rarely been preserved. The functional interpretation now indispensable makes appear, on the ground of regularities within phylums, a progression that takes advantage of previous stages by making overlying innovations which they are only the active support (Leroi-Gourhan, 1964). Any “ancestor” of a phylum must have possessed plurispecialized characteristics that gave it possibilities to continue a wider dialogue with an environment also evolving. Contrary to what is sometimes maintained, the “ancestors” do not lack more potential specializations than a 3day-old chicken embryo lacks potential strategies, and if ancestral capacities are slight, evolutionary radiation will take charge and reduce plurispecialization of each group descending from that radiation. With time indeed a monospecializaZion of interactions is installed within [organism, environment] Systems, and that is probably what is responsible for the obvious rigidity of some types of insect strategies for example. This progression is comparable, taking into account transposition of models, with the restriction of exchanges that accompanies canalization of ontogenetic development. In that respect, man, this latest arrived species, preserves, compared to other vertebrates, the greatest degree of ancestral radiation characteristics by his wide

262

GASTON RICHARD

plurispecialization: morphological plurispecialization [the hand, for example, which is a structure capable of taking, hitting, scratching, hanging, pulling, pushing actions (Connolly and Elliott, 1972)], ethological plurispecialization (abstraction strategies which give him important possibilities for spatiotemporal understanding of the environment), and the parallel plurispecialization of the environment where he can live. Of course each of these specializations thus observed exists in more ancient animals within the limits of monospecialization, either in relation to the same structure (the anterior member that hangs, hits, pushes,. . .), or in relation to another structure (the teeth that take, scratch, . . .); this is the weight of the past in man. But never is a plurispecialization unaccompanied by constraints of another kind also tied to the phylogenetic past, and a hand cannot be used simultaneously to hang and to scratch, to take and to push away; abstraction strategies cannot be released from a return to a concrete world, and the physiochemically attainable environments are not without constraints. It is very important to recognize that the phylogenetic passage from plurispecializationto monospecializationwhich translates into the evolutionary canalization of functions in closed [organism, environment] Systems seems to be accompanied by recalibrations of physiological and biochemical homeostasis included in the organism considered in turn as a System (cf. Section I). This thesis, inspired by Piaget (1974), seems most fruitful. Piaget based it on his biological research continued for nearly 50 years on Limnea and Sedum and on his studies concerning human psychogenesis. Studying the convergence of morphological expressions between certain mutation products on the one hand, and other characters that are not hereditary but are repeated in each generation so long as environmental conditions causing this phenotypical expression are maintained (accommodation), Piaget asks the following questions: Which came first in time, the accommodator or the now mutated genotype, and, if the mutation came after the somatotype, could the latter have served as “model” for the first, and how? This is no matter of a naive Lamarckian springing up again, but these questions call, on the contrary, for answers which can utilize all mechanisms that are now known to intervene in evolutionary processes (mutations, recalibrations of [gene, genome] homeostasis under the influence of pressures of the more inducing homeostatic Systems, etc.. . .). They.open up wide perspectives that bring modes of evolution of the natural world (substitution of the phenotypic exogenous formation by genotypic endogenous formation) and modes of evolution of the cultural world (substitution of the cognitive exogenous formation by an endogenous formation: the logicomathematical activity) closer. Through this substitution, which unifies types of evolutionary strategies by attributing to the environment less and less an initiating role and more and more a regulating role in ontogenetic and phylogenetic constructions, Piaget rises well above the false nature-nurture debate, just as Schneirla formerly, for the same reasons, rose above the false innate-acquired debate.

ONTOGENESIS AND PHYLOGENESIS

263

Phylogenetic evolution becomes a continuous unrolling of transformations (recalibrations) which affect an encased entity of homeostases contained in the [biosphere, geosphere] System, through an assimilation of time by living matter of this System. This assimilation is itself the origin of adaptations, and time ceases to be an inert limit within which phenomena occur: for each object, by contrast with the fixed state of its isolation, time becomes the rhythm of its changing when linked with other objects (Ullmo, 1967). Behavior plays a fundamental driving role in this evolution: Through the intermediary of Time assimilated into the Systems, it ensures a continuity of direction of the evolutionary unrolling and progressive complexity of interacting structures. Thus, rhythmical strategies of temporal anticipation and trial and error strategies of unicellular organisms living in a relatively homogeneous tridimensional aqueous environment (primitive ocean) have prepared the way for more complex strategies (to be present at a significant moment in a significant environment where something will be learned), that were and still are those of Metazoan organisms provided with memory and sensorimotor capacities permitting them access to diversified environments that they in turn transform. Functional dynamics in such systems were themselves preadaptive for the widely developed strategies of mankind, which, thanks to the power of generalization that abstract reasoning gives, have ensured a new widening of the species environment onto which behavior is projected. This species environment assumes the pressures of natural selection, and if the nature of these pressures has not changed for 2 thousand million years, the complexity of networks by which their actions are expressed has considerably increased. Our model of phylogenesis must therefore not only take into account transformation of organisms, but also changes in the nature of natural selection that have accompanied evolution. This progress is undeniable for anybody who wants to judge the real importance of successive diversifying pressures exerted by the available Geosphere in successive Systems: the first ones, when the biosphere was constituted only of a small biomass of marine microorganisms and some Metaphytes and Metazoa; then those when the biomass grew up and occupied the whole mass of the oceans, the superficial land surfaces (emerged continents), freshwater masses, finally air; then those where the growing complexity of trophic networks permits more diversity, more intricacy, and more productivity. But it is not sufficient to examine what natural selection is; we must know what it acts on, and how. On these grounds, we can only deplore the elision made by geneticists, and now used in colloquial language; natural selection does not act upon the genome but obviously on the vectors of the genome in the reproductive flow: the individual phenotypes in a population. It is there that are inserted the results of ontogenetic development, which lead, we know, to a particular and unique phenotypic realization among those made possible by the genotypic con-

264

GASTON RICHARD

stitution. But it is the individual thus realized among its population included in a biocenosis, itself belonging to an ecosystem, etc., that bears the weight of the transfer of its genotype to its descendants. Now, if nobody can actually maintain that the “environment” has any actions at all on mutation processes (neither can anybody maintain the opposite now without risking denial in 10 years!), it is obvious that the interactions between organisms and environments that have received the name of natural selection, have important consequences on the quality of the gene-pool elements that will be able to participate in multiple future phenomena.

IV. MUTUAL CONSTRAINTS BETWEEN ONTOGENY AND PHYLOGENY It was normal at a time when feedbacks had not yet taken their place in biological thought or evolution to seem finished in perfect harmony with nature, and Man to be thought of as an end result with all the other organisms at his service (Lovejoy, 1965) to see in ontogeny only a resume of phylogeny, and in an adult individual only the revelation of hereditary characteristics held by its parents. Proof of constraints exerted by phylogeny on ontogeny is plentiful, and we have mentioned some in Section II1,A. In each main phylum, eggs present narrow structural and embryological similarities; however, they differ by their physical and chemical qualities from one species to another. Developmental modes unfold constructions broadly parallel for all species of a phylum, but these modes are sufficiently different in detail to make it difficult, for example, to generalize to all vertebrates laws elaborated from Fish or Batrachia (Coghill, 1929; Oppenheim, 1974; Gottlieb, 1973). Developmental patterns that bring Amniotes closer to each other give, however, each species its particular capacities, and comparison of behavior preceding or accompanying hatching is highly significant on that point (Oppenheim, 1973). But all the rest of the development of the young and of the gradual organization of the environment provide an important sample of examples proving that many species-specific patterns develop under pressure of hereditary constraints, on the motor level as well as on the sensory level. Ontogenesis of birdsong is a good example (Thorpe, 1961; Marler and Mundinger, 1971; Immelman, 1969; Konishi and Nottebohm, 1969). However, it is constraints that bear on learning in which the phylogenetic origin can be recognized most easily-plasticity of processes in conditional reactions, but also learning capacity, reinforcement specificity, and the importance of what can be learned. “Whether or not ontogeny repeats phylogeny, it would seem that phylogeny must have bequeathed a strong predisposition to

ONTOGENESIS AND PHYLOGENESIS

265

learn along lines which lead to the development of patterns which are characteristic of the species or at least of a high proportion of its members” (Hinde, 1974). On a par with the general phylogenetic increase of learning capacities, an increasing interindividual variability gives particular weight to every individual’s experience, this latter besides depending widely on the richness of the environment encountered. These properties are obvious when the precocious manipulation capacities of Mammals are compared with those of the other Vertebrates, but they are revealed even better by transcultural comparisons of primates (Homo sapiens included): every human newborn we have seen is capable of assimilating any particular culture, but on the other hand he takes part in the increase of complexity of human cultures with the succession of generations. But it is impossible to remain now at that level of action of phylogeny or ontogeny. The conception of a continuing evolution, the conception of a probabilistic ontogeny making place for a limited but indeed real variation, compels us to ask ourselves if ontogenetic development does not have some constraining consequences on the continuation of phylogeny. We shall examine that question briefly below. Indeed, the egg and the environment in which it develops bear the weight of the past. But all the unwinding of ontogeny occurs in the midst of a population with characteristics under constant evolutionary modification, whether it be the characteristics of its habitat, the characteristics of its genotype pool, or the characteristics of its relationships with neighboring populations. Now, although young forms as well as adult forms act to occupy environments and to maintain relationships with neighboring populations, transmission of particular genes of the pool falls exclusively to adults. But are not these adults the end product of ontogenetic developmental processes, in which, as we have said (Section 11), successive phenomena of attachment determine reproductive functions? Thus, it is possible to state positively that, in many regards, ontogeny constructs individual bearers of hereditary Characteristics inflecting the gene flow through succeeding generations in a population, and, therefore, the evolutionary radiation of that population. There is no circularity in this argument, but it becomes obvious that, ifthe egg and its natural environment depend on the phylogenetic past, the gradual phylogenetic development depends, in turn, on constraints that bring to bear on it the patterns of ontogenetic development of individuals that, in a population, reach a reproductive state. Some precision will clarify this kind of constraint. Geneticists have insisted on the fact that a natural population possesses active mechanisms maintaining a certain degree of heterozygosity of its genotype, which is not incompatible with a strong resistance to abrupt or important changes in the gene pool (genetic inertia of Darlington and Mather, 1969; genetic homeostasis of Lerner, 1954). But, of course, the effects of this regulation can differ enormously according to the importance of the population affected (Founder principle of Mayr).

266

GASTON RICHARD

What seems fundamental to us is that no genome transmission occurs without intervention of genitors. Therefore, it is absolutely necessary to take into account, considering this transmission, strategies of choosing sexual partners (sexual vigor) and the part they could play in parent-young relationships, or social exchanges during ontogenesis in developing these strategies. Imprinting is one of those ethological facts in which is perfectly expressed the narrow relationship that exists between phenotype construction under the guiding influences of the environment and the transmission to descendants through the intermediary of that phenotype, of the genotype that was transcribed during individual ontogenesis. Competition among young and the importance of play for maturation have often been analyzed from this point of view, but sexual choices are the kinds of behavior that have led to most studies. Among these choices, one that has drawn the most attention of population geneticists is the advantage of rhe rare type, discovered by Petit (1951) and E h a n (1966) and analyzed by Ehrman and Parsons (1976). When two alleles occur with different frequencies in a population there is no elimination of one of them during the following generations and the selective value of each varies as an inverse function of the frequency with which it occurs; in the case of Drosophila, where this phenomenon was first observed, it is the choice of the sexual partners by females that is responsible for the advantage of the rare type, and recent experiments by Petit and Nouaud (1976) give clear indication of the importance of the precopulatory environment in establishing the female’s choice. These ethological considerations, among others now generalized to many species, lead us to reject definitively the concept of panmictic populations, and all the more, to insist on the purely theoretical character of laws like that of Hardy-Weinberg, which are still often used as a reference by many geneticists. But they enable us to give to this “invariant,” i.e., intraspecific exchange of genes, its real value in contributing to the “variation” of the evolutionary pool: the possibility for gene exchange ceases to be a criterion for the taxonomic isolation of a species, and becomes a criterion for maintenance in a population of rich possibilities contributing to many preadaptations. The study of ontogenetic construction of sexual behavior with the successive limits of filial and social attachments is then of great importance, as this behavior plays simultaneously an innovating role and a preserving role in evolution: innovating, as it enables, within the limits of the population, choice of the most genetically dissimilar partner (the most heterozygotic); preserving, as it ensures, within the limits of the species, choice of the most similar partner (also from the genetic point of view, but on another level: species-specific genome). The slow individual maturation of sexual behavior, the successive transfer of attachments that it assumes, the innovating-preserving surroundings, and the particular role played by the sexual partner in natural selection are probably the causes in phylogenesis of the reinforcement of the stereotype of courtship display se-

ONTOGENESIS A N D PHYLOGENESIS

267

quences and introduction in these sequences of ritualized acts, the value of which as “time markers” and as “state markers” can be compared to the same value taken by “superstitious acts” (Skinner, 1948) in a sequence of operant behavior. These remarks enable facts of communication to be rooted deeply in phylogenetic change itself, ensuring understanding, at the same time, of the general manifestation of interindividual communication, and of the gradual complexity of its use by the most recent groups in evolutionary radiation. But they enable us also to understand how use of individual communication potentials established during development must have some efSect on the future through the balance between innovation and preservation that characterizes a population, especially if the latter is constituted by eusocial animals, since the multiplier effect of individual behavior estimated on a collective level is then maximum [Wilson (1 975) defines eusocial “as the formal equivalent of the expressions ‘truly social’ or ‘higher social’ which are commonly used in the study of social insects”]. We find ourselves here in agreement with Crook et al. (1976): “The survey of mammal social systems reveals the great importance of the rearing conditions in determining the kind of system that evolves.” It is at the same time the type of group structure, the more or less lasting permanence of male-female bonds, the importance of mother-young bonds and male-young bonds that constitute the fundamental characteristics expressing mutual interrelationships of ontogenesis and phylogenesis. Widening this problem, we could hope that more precise studies will be undertaken on the way that adult behavior is elaborated in young, not only in a monospecific group (population) but in a wide polyspecific group (biocenosis) where natural selection pressures combine all ontogenetic pressures in the general evolution of the system. It is then, and only then, that the coalescence of ethology and developmental psychology beyond their different approaches will be realized harmoniously (Blurton-Jones, 1972).

V.

CONCLUSION

This article aims at a more complete understanding of the fact of the evolution of organisms. It suggests not only that ontogenesis depends on the phylogenetic past of the egg and the environment in which it develops but also that the phylogenetic flow is orientated by genetic flow in many populations toward radiating evolution within natural ecosystems. This genetic flow depends in great part on the behavior involved in choice behavior of a sexual partner (choice at the same time innovating and preserving), which is gradually elaborated during ontogenesis within the limits of individual variability and is all the wider when the species considered is phylogenetically younger.

268

GASTON RICHARD

This permanent intricacy of ontogenetic facts and phylogenetic facts, and also the reciprocal interactions that constitute population dynamics, lead us to express, with new terms of time assimilation, strategies applied to living matter, behavior projected by animals onto their respective environments, as well as stimulation exerted by these environments on animals. Dialectic opposition of two equal subsystems [organisn-denvironment] that interpenetrate by mutual feedback enables the emerging qualities of the System thus composed to be interpreted as inescapable consequences of the quantitative functioning of the entity in evolution. A succession of time assimilation strategies can thus emerge from comparative observations of ontogenesis of actual species belonging to diverse phyla. But differences between phyla enable transposition onto the phylogenetic level of the properties of such a model, thus ensuring at the same time the possibility of extending it towards the future and the possibility of basing it on the past. If, indeed, rhythmic coincidence-making strategies, anticipation strategies leading to be present in a specific place at a specific moment, and abstraction capacities which enable the past, the present, and the future to be united in one continuous entity, appear as successive capacities that widen the field of interaction of organisms with their environments, it can be considered that the future will produce a strategy that will enable our successors to dominate dialectics maintained by space and time. As Jaegle (1976) has written, these dialectics are no doubt only the reflection in our consciences of a real contradiction in nature, the two poles of which are precisely space and time; but the existence of such a “reflection” constitutes, in our opinion, the beginning of a preadaptation that should lead to this unifying strategy. But our ontophylogenetic model must also lead us to consider the past. Long before rhythmic coincidence-makingstrategies could characterize functioning of [organisdenvironment] Systems, rhythmical preadaptations surely existed on the level of chemistry of organic substances in the prebiotic ocean. And it seems that the first anticipatory strategy enabling a new assimilation of time to living matter of the moment must have been the one that consisted of a multimolecular structure, preserving information about its own structure and about its functions with respect to the relatively homogeneous environment in which it existed. Nucleic acids have played an important part in establishing and maintaining this strategy, which was obviously fundamental for the hppearance of a certain order (conservator, like all orders) in the results of reproductive functions of the system considered. All this brings us to rethink a certain number of problems with respect to behavior for our final conclusions. It remains essential to analyze morphophysiological causes of behavior; to study the dependency with respect to ecological factors and the impact on the environment where it is expressed; to establish ecoethological balances and to express them in terms of “survival”; but it seems to us no less essential to widen the comparative line of study and, to this

ONTOGENESIS AND PHYLOGENESIS

269

end, to better interpret roles played by behavior in the assimilation of matter to structures and in the assimilation of time to matter. It is only then that man’s own strategies can be better described. “What you inherit from your fathers, acquire it, and make it yours” Goethe wrote in Fuusr, and Malraux said: “C’est seulement chez I’heritier que se produit la metamorphose d’ou nait la vie” (It is only in the heir that the metamorphosis is produced from which life is born).

Acknowledgments During the preparation of this paper, I have been greatly helped by the comments of J. Y. Gautier and M. Vancassel. I am very grateful to A. Cloarec, who wrote the first English translation, to M. C. Busnel, R. A. Hinde, C. Beer, and J. Rosenblatt for their comments on the manuscript, and to R. A . Dawkins and Cambridge University Press who allowed me to use a published figure. But my wannest thanks go to J. Rosenblatt for his excellent and friendly efficiency in elaborating the last text. I also thank W. Cunningham and N. Jachim for help in typing the manuscript.

References Allyn, G . 1974. Mammalian socialization and the problem of imprinting. Terre Vie 2, 209-271. Ambrose, J . A. 1963. The concept of a critical period for the development of social responsiveness in early infancy. In ”Determinants of Infant Behaviour 11” (B. F. Foss, ed.), pp. 201 -225. Wiley, New York. Andrew, R. J. 1964. Vocalizations in chicks and the concept of “stimulus contrast.” Anim. Eehav. 12, 64-76. Andrew, R. J. 1976. Attentional processes and animal behaviour. In “Growing Points in Ethology” (P. P. G . Bateson and R. A. Hinde, eds.), pp. 95-133. Cambridge Univ. Press, London and New York. Apostel, G. 1967. Logique et dialectique. In “Logique et Connaissance Scientifique” (J. Piaget, ed.), pp. 357-374. Encyclopkdie de la Pleiade, Gallimard, Paris. Asdourian, D. 1967. Object attachment and the critical period. Psychonom. Sci. 7, 235-236. Baerends, G. P. 1970. A model of the functional organization of incubation behaviour. In “The Herring Gull and its Egg” (G. P. Baerends and R. H. b e n t , eds.), Behaviour, Suppl. 17, pp. 263-3 12. Baerends, G. P. 1976. The functional organization of behaviour. h i m . Eehav. 24, 726-738. Baerends, G. P., and Kmijt, 1. P. 1973. Stimulus selection. In “Constraints on Learning” (R. A. Hinde and J. Stevenson-Hinde, eds.), pp. 23-50. Academic Press, New York. Barnett, S. A. 1975. Ethology and development. Psychol. Med. 5 , 323-326. Bateson, P. P. G. An effect of imprinting on the perceptual development of domestic chicks. Narure (London) 202. 421 -422. Bateson, P. P. G . 1966. The characteristics and context of imprinting. B i d . Rev. Cambridge Philos. Soc. 41, 177-220. Bateson, P. P. G . 1973. Internal influences on early learning in birds. In “Constraints on Learning” (R. A. Hinde and J. Stevenson-Hinde, eds.), pp. 101-1 16. Academic Press, New York. Bateson, P. P. G . 1976. Rules and reciprocity in behavioral development. In “Growing Points in Ethology” (P. P. G. Bateson and R. A. Hinde. eds.), pp. 401-421. Cambridge Univ. Press, London and New York. Bateson, P. P. G . , and Chantrey, D. F. 1972. Retardation of discrimination learning in monkeys and chicks previously exposed to both stimuli. Nature (London) 237, 173-174.

270

GASTON RICHARD

Bateson, P. P. G., and Hinde. R. A. (eds.). 1976. “Growing Points in Ethology.” Cambridge Univ. Press, London and New York. Bateson, P. P. G . . and Jaeckel, J. B. 1974. Imprinting: Correlations between activities of chicks during training and testing. Anim. Behav. 22, 899-906. Bateson, P. P. G., and Jaeckel, J. B. 1976. Chicks’ preferences for familiar and novel conspicuous objects after different periods of exposure. Anim. Behav. 24, 386-390. Bateson, P. P. G., and Klopfer, P. H. (eds.). 1973. “Perspectives in Ethology,” Vol. I . Plenum, New York. Bateson, P. P. G., and Klopfer, P. H. (eds.). 1976. “Perspectives in Ethology,” Vol. 2. Plenum, New York. Bateson, P. P. G., and Wainwright, A. A. P. 1972. The effects of prior exposure to light on the imprinting process in domestic chicks. Behaviour 42, 279-285. Beer, C. G . 1961. Incubation and nest building behaviour of black-headed gulls: I-Incubation behaviour in the incubation period. Behaviour 18, 62-106. Beer, C. G . 1963a. 111-The pre-laying period. Behaviour 21, 13-77. Beer, C. G. 1963b. IV-Nest-building in the laying and incubation periods. Behaviour 21, 155-176. Bessemer, D. W., and Stollnitz, F. 1971. Retention and discrimination and an analysis of learning set. In “Behavior of Non-Human Primates” (A. M. Schrier and F. Stollnitz, eds.), Vol. 4 , pp. 1-58. Academic Press, New York. Beukema, J. J. 1968. Predation by the three-spined stickleback Gasrerosieus aculeurus: The influence of hunger and experience. Behaviour 31, 1-126. Bitterman, M . E. 1975. The comparative analysis of learning. Science 188, 699-709. Blurton-Jones, N . 1972. “Ethological Studies of Child Behaviour. ” Cambridge Univ. Press, London and New York. Bolles, R. C. 1970. Species-specific defense reactions and avoidance learning. Psycho/. Rev. 77, 32-48. Bowlby, J . 1969. “Attachment and Loss.” Hogarth, London. Bowlby, I . 1973. “Separation: Anxiety and Anger.” Hogarth, London. Brain, P. 1975. What does individual housing mean to a mouse? Life Sri. 16, 187-200. Brosset, A. 1971. L’imprinting chez les Columbides-Etude des modifications comportementales au cours du vieillissement. Z. Tierpsychol. 29, 279-300. Brosset, A. 1973. Etude comparative de I’ontogentse des comportements chez les Rapaces Accipitrides et Falconides. Z. Tierpsycho/. 32, 386-417. Candland, D. K . 1971. The ontogeny of emotional behavior. In “Ontogeny of Vertebrate Behavior” (H. Moltz, ed.), pp. 95-154. Academic Press, New York. Canguilheim. G. 1955. “La Formation du Concept de Rkflexe aux 17‘et 18‘ Siecles.” Presses Univ. de Fr.. Paris. Chantrey, D. F. 1972. Enhancement and retardation of discrimination learning in chicks after exposure to the discriminanda. J . Comp. Physiol. Psycho/. 81, 256-261. Coghill, G. E. 1929. “Anatomy and the Problem of Behavior.” Hafner, New York. (Reprint, 1964.) Collias, M. 1952. The development of social behavior in birds. Auk 69, 127-159. Condon, W. S . , and Sander, L. W. 1976. Neonate movement is synchronized with adult speech: interactional participation and language acquisition. Science 183, 99- 101. Connolly. K., and Elliott, J. 1972. The evolution and ontogeny of hand function. In “Ethological Studies of Child Behaviour” (N. Blurton-Jones, ed.). pp. 329-383. Cambridge Univ. Press, London and New York. Comer, M. A , , Bakhuis, W. L., and van Wingerden, C. 1973. Sleep and wakefulness during early life in the domestic chicken, and their relationship to hatching and embryonic motility. In “Behavioral Embryology” (G. Gottlieb, ed.), pp. 245-277. Academic Press. New York. Crook, J. H., Ellis, J. E., and Goss-Custard, J. D. 1976. Mammalian social systems: Structure and function. Anim. Behav. 24. 261-274.

ONTOGENESIS AND PHYLOGENESIS

27 1

Croze, H. 1970. Searching image in carrion crows. Hunting strategy in a predator and some antipredator devices in camouflaged preys. Z. Tierpsychol. Beih. No. 5 . Darlington, C. D. 1957. “Le Mystere de la Vie.” Fayard, Paris. Darlington, C. D., and Mather, K. 1949. “The Elements of Genetics.” Allen and Unwin, London. Davenport, R. K., and Rogers, C. M. 1970. Intermodal equivalence of stimuli in apes. Science 168, 279. Dawkins, R. 1976. Hierarchical organization: A candidate principle for ethology. In “Growing Points in Ethology” (P. P. G . Bateson and R. A. Hinde, eds.). pp. 7-54. Cambridge Univ. Press, London and New York. de Ajuriaguerra, J. 1976. L’Enfant, de I’Ebauche a I’Etre Humain. LeSon Inaugurale au College de France, Paris. Delattre, P. 1971. “Systeme, Structure, Fonction, Evolution. Essai d’Analyse Epistemologique.” Maloine, Paris. Demany, L., McKenzie, B., and Vurpillot, E. 1977. Rhythm perception in early infancy. Nature 266, 710-719. Deutsch, J., and Larsson, K. 1974. Model-oriented sexual behavior in surrogate reared rhesus monkey. Brain Behav. Evol. 9 , 157-164. Ehrman, L. 1966. Mating success and genotype frequency in Drosophila. Anim. Behav. 14. 332339. Ehrman. L., and Parsons, P. A. 1976. ”The Genetics of Behavior.” Sinauer Assoc. Eimas, P. D., Siqueland, E. R., Jusczyk, P., and Vigorito, J. 1971. Speech perception in infants. Science 171, 303-306. Eisenberg, J. F., and Leyhausen, P. 1972. The phylogenesis of predatory behaviour in mammals. Z. Tierpsychol. 30,59-93. Eisenberg, R. A. 1969. Auditory behavior in the human neonate: Functional properties of sounds and their ontogenetic implications. In!. Audiol. 8 , 34-45. Etienne, A. 1973. Developmental stages and cognitive structures as determinants of what is learned. In “Constraints on Learning” (R. A. Hinde and J. Stevenson-Hinde, eds.), pp. 371-396. Academic Press, New York. Evans, R. M. 1972. Development of an auditory discrimination in young domestic chick. h i m . Behav. 20, 77-87. Evans, R. M. 1973. Differential responsiveness of young ring-billed gulls and herring gulls to adult vocalizations of their own and other species. Can. J. Zoo/. 51, 759-770. Evans, R. M. 1975a. Responsiveness to adult mew calls in young ring-billed gulls: Effects of exposure to calls alone and in the presence of visual imprinting stimuli. Can. J. Zool. 53, 953-959. Evans, R. M. 1975b. Stimulus intensity and acoustical communication in young domestic chick. Behaviour 55, 73-80. Ewer, R. F. 1968. “Ethology of Mammals.” Logos Press, London. Ewer, R. F. 1969. Some observations on the killing and the eating of prey by two dasyurid marsupials. Z. Tierpsycho/. 26, 23-28. Fantz, R. L. 1963. Pattern vision in newborn infants. Science 140, 296-298. Fantz, R. L. 1965. Visual perception from birth as shown by pattern selectivity. Ann. New York Acad. Sci. 118, 783-814. Fantz, R. L. 1966. Pattern discrimination and selective attention as determinants of perceptual development from birth. In “Perceptual Development in Children” (A. H. Kidd and J. L. Rivoire, eds.), pp. 143-173. International Univ. Press, New York. Fentress, J. C. 1976. Dynamic boundaries of patterned behaviour: Interaction and self organization. I n “Growing Points in Ethology” (P. P. G. Bateson and R. A. Hinde, eds.), pp. 137-170. Cambridge Univ. Press, London and New York. Fornby, D. 1967. Maternal recognition of infant’s cry. Dev. Med. Child Neurol. 9 , 293-298.

272

GASTON RICHARD

Fox, M. W . 1969. Ontogeny of prey killing behaviour in Canidae. Behaviour 35, 259-272. Fox, M. W. 1972. Socio-ecological implications of individual differences in wolf litters: A developmental and evolutionary perspective. Behaviour 41, 298-3 13. Fragaszy, D. M., and Mitchell, G.1974. Infant socialization in primates. J. Hum.Evol. 3,563-574. French, G . M. 1965. Associative problems. In “Behavior in Non-Human Primates” (A. M. Schrier, H. F. Harlow, and F. Stollnitz, eds.). Vol. I , pp. 167-209. Academic Press, New York. Friedman, M. I. 1975. Some determinants of milk ingestion in suckling rats. J. Comp. Physiol. 89, 636-647. Gallup, G.G. 1970. Chimpanzees: Self recognition. Science 167, 86. Gardner, B. T., and Gadner, R. A. 1971. Two-way communication with an infant chimpanzee. In “Behavior of Non-Human Primates” (A. M. Schrier, H. F. Harlow, and F. Stollnitz, eds.), Vol. 4. pp. 117-184. Academic Press, New York. Gautier, J. Y . 1974. Processus de differenciation de I’organisation sociale chez quelques Blattes du genre Blaberus: aspects ecologiques et ethologiques. These Universite de Rennes. Gautier, J. Y. 1976. Contribution a I’etude du phenomene d’ordre de dominance chez les Blattes. Biol. Behav. 1, 353-365. Gautier, J . Y . , Lefeuvre, J . C., Richard, G., and Trehen, P. 1978. “Ecdthologie.” Masson, Paris. Gottlieb, G. 1966. Species identification by avian neonates: Contributory effect of perinatal auditory stimulation. Anim. Behav. 14. 282-290. Gottlieb, G. 1971. Ontogenesis of sensory function in birds and mammals. In “The Biopsychology of Development” (E. Tobach. L. R. Aronson, and E. Shaw. eds.). pp. 67-128. Academic Press, New York. Gottlieb, G. 1973. “Behavioral Embryology.” Academic Press, New York. Gottlieb, G . 1974. On the acoustic basis of species identification in wood duckling. J. Comp. Physiol. Psycho/. 87. 1038-1048. Gottlieb, G. 1975a. Development of species identification in ducklings. I. Nature of perceptual deficit caused by embryonic auditory deprivation. J. Comp. Physinl. Psychol. 89, 387-399. Gottlieb, G. 1975b. Development of species identification in ducklings. 11. Experiential prevention of perceptual deficit caused by embryonic auditory deprivation. J. Comp. Physiol. Psychol. 89, 675-784. Gottlieb, G. 1 9 7 5 ~ Development . of species identification in ducklings. 111. Maturational rectification of perceptual deficit caused by auditory deprivation. J. Comp. Physiol. Psychol. 89. 899-91 2. Gottlieb, G. 1976. Conception of prenatal development: behavioral embryology. Psychol. Rev. 83, 215-234. Grasse, P. P. 1942. L’essaimage des termites. Essai d’analyse causale d’un complexe instinctif. Bull. Biol. Fr. Belg. 16, 347-382. Grasse, P. P.,and Noirot, C. 1951. La sociotomie: Migration et fragmentation de la Termitiere chez les Anoplotermes et les Trinervifermes. Behaviour 3(2), 146- 166. Gray, P. H . 1958. Theory and evidence of imprinting in human infants. J . Psychol. 46, 155-166. Gray, P. H. 1960. Evidence that retinal flicker is not a necessary condition of imprinting. Science 132, 18-34. Guiton, P. 1958. The effect of isolation on the following response of Brown Leghorn chicks. Proc. R . Soc. Edinburgh 27, 9-14. Guiton, P. 1959. Socialization and imprinting in Brown Leghorn chicks. h i m . Behav. 7 , 26-34. Guiton. P. 1961. The influence of imprinting on the agonistic and courtship responses of the Brown Leghorn cock. h i m . Behav. 9. 167-177. Guyomarc’h. J . C. 1971. Les cris rnaternels des Gallinaces et leur ontogenese. J . Psvchol. 3 4 , 381-400. Guyornarc’h. J . C. 1972. Les bases ontogenetiques de I’attractivite du gloussement maternel chez la poule dornestique. Rev. Comp. Anim. 6, 79-94.

1

ONTOGENESIS AND PHYLOGENESIS

273

Guyomarc’h, J. C. 1973. RBle de I’autoperception auditive dans I’orientation du choix des poussins sans expkrience maternelle. C . R . Acud. Sci., Ser. D 276, 1717-1720. Guyomarc’h, J . C. 1974a. Le rde de I’expirience sur la semantique du cri d’offrande alimentaire chez le poussin. Rev. Comp. Anim. 8, 219-236. Guyomarc’h, J. C. 1974b. Les Vocalisations des Gallinaces. Structure des Sons et des Repertoires; Ontogenese Motrice et Acquisition de leur Semantique. These, Univ. de Rennes, Rennes. Guyomarc’h, I. C., Yris, M. A., and Fontenelle, G. 1973. Influence de I’exphience prenatale sur le rhythm d’activite du poussin domestique. Bull. SOC. Sci. Breragne 48, 49-58. Hamburger, V . 1973. Anatomical and physiological basis of embryonic motility in birds and mammals. In “Behavioral Embryology” (G. Gottlieb, ed.), pp. 49-75. Academic Press, New York. Herman, L. M., and Arbeit, W . R. 1973. Stimulus control and auditory discrimination learning sets in bottlenose dolphin. J . Exp. Anal. Behav. 19, 379-394. Herman, L. M., Beach, F. A,, 111, Pepper, R. L., and Stallings, R. B. 1969. Learning-set formation in the bottlenose dolphin. Psychonom. Sci. 14, 98-99. Herrick. C. J . 1956. “The Evolution of Human Nature.” Harper, New York. Hess, E. H. 1973. “Imprinting. Early experience and the Developmental Psychobiology of Attachment.” Van Nostrand-Reinhold, New York. Hinde, R. A. 1961. The establishment of the parent-offspring relation in birds, with some mammalian analogies. In “Current Problems in Animal Behaviour” (W.H. Thorpe and 0. L. Zangwill, eds.), pp. 175-193. Cambridge Univ. Press, London and New York. Hinde, R. A. 1962. Some aspects of imprinting problem. Symp. Zool. SOC. London 8, 129-138. Hinde, R. A. 1963. The nature of imprinting. In “Determinants of Infant Behaviour” (B. M. Foss, ed.), pp. 227-233. Methuen. London. Hinde, R. A. 1966. “Animal Behaviour. A Synthesis of Ethology and Comparative Psychology.” McGraw-Hill, New York. (2nd Ed., 1970.) Hinde, R. A. 1974. “Biological Bases of Human Social Behaviour.” McGraw-Hill, New York. Hinde, R. A,. and Stevenson-Hinde, J. 1973. “Constraints on Learning. Limitations and Predispositions.” Academic Press, New York. Hinde. R. A., and Stevenson-Hinde. J . 1976. Towards understanding relationships: Dynamic stability. In “Growing Points in Ethology” (P. P. G. Bateson and R. A. Hinde, eds.). pp. 451-479. Cambridge Univ. Press, London and New York. Hinde, R . A., Thorpe, W .H., and Vince, M. A. 1956. The following response of young coots and moorhens. Behaviour 9. 214-242. Hodos, W..and Campbell, C. B. G. 1969. Scdu Nururue: Why there is no theory of comparative psychology’? Psychol. Rev. 16, 337-350. Hoffman, H . S . 1968. The control of distress vocalization by an imprinting stimulus. Behaviour 30, 175-191. Hoffman, H. S . , Rattner, A. M., and Eiserer, L. A. 1972. Role of visual imprinting in the emergence of filial attachment in ducklings. J. Comp. Physiol. Psychol. 81. 399-409. Hogan, J . A. 1973. How young chicks learn to recognize food. In “Constraints on Learning” (R. A. Hinde and J . Stevenson-Hinde, eds.), pp. 119-140. Academic Press, New York. Hogan, J. A . 1975. Development of food recognition in young chicks. Discrimination. J. Comp. Physiol. Psycho/. 89, 95-104. Hutt, S. J . 1973. Constraints on learning: Some developmental considerations. In “Constraints on Learning” (R. A . Hinde and J . Stevenson-Hinde, eds.), pp. 457-466. Academic Press, New York. Hutt, S . J.. Hutt, C., Lenard, H. S., von Bernuth, H., and Muntjewerff, W. J . 1968. Auditory responsivity in the human neonate. Nurure (London) 218, 888-890. Huxley, J . 1971. ”Ritualization of Behaviour in Animals and Man.” Symp. R. Acad.. London. Immelman, K . 1969. Okologische und stammesgeschichtliche Betrachtungen Zum Pragungsphiinomen. Zool. A n t . 183, 1-12.

274

GASTON RICHARD

Immelman, K. 1972a. Sexual and other long term aspects of imprinting in birds and other species. Adv. Srudy Behav. 4, 147-174. Immelman, K. 1972b. The influence of early experience upon the development of social behaviour in estrildine finches. Proc. Inr. Ornirhol. Congr., /5rh, pp. 316-338. Immelman, K. 1975. Ecological significance of imprinting and early learning. Annu. Rev. Ecol. Syst. 6, 15-37. Impekoven, M. 1976. Responses of laughing gulls (Lams arricilla) chicks to parental attraction and alarm calls, and effects of prenatal auditory experience on the responsiveness of such calls. Behaviour 56, 250-278. Impekoven, M., and Gold, P. S. 1973. Prenatal origin of parent-young interactions in birds: A naturalistic approach. In "Behavioral Embryology" ( G . Gottlieb, ed.), Vol. I , pp. 325-356. Academic Press, New York. Jaegle, P. 1976. "Essai sur I'Espace et le Temps." Editions Sociales, Paris. Jaisson, P. 1976. L'impregnation dans I'ontogentse des comportements de soins aux cocons chez la jeune fourmi rousse, Formica polycrena, F. Behaviour 52, 1-37. Jaynes, J., 1956. Imprinting: The interaction of learned and innate behavior. I. Development and generalization. J. Comp. Physiol. Psychol. 49, 201-206. Jaynes, J . 1957. Imprinting: The interaction of learned and innate behavior. 11. The critical period. J. Comp. Physiol. Psychol. 50, 6-10. Johnson, R. N.. DeSito, M. J., and Koenig, A. B. 1972. Social and developmental experience and interspecific aggression in rats. J. Comp. Physiol. Psychol. 79, 237-242. Karli, P. 1956. The Norway rat's killing response to the white mouse: An experiment analysis. Behaviour 10, 81-101. Kestenberg, J. S. 1965. The role of movement patterns in development: I. Rhythms of movement. Psychoanal. Q.34, 1-36. Klinghammer, E. 1967. Factors influencing choice of mate in altricial birds. In "Early Behavior" (H.W. Stevenson, E. H.Hess. and H.L. Reingold, eds.), pp. 5-42. Wiley, New York. Koehler, 0. 1950. The ability of birds to count. Bull. Anim. Behav. 9. 41-45. Konishi. M . , and Nottebohm, F. 1969. Experimental studies in the ontogeny of avian vocalizations. In "Bird Vocalizations" (R. A . Hinde, ed.). Cambridge Univ. Press, London and New York. Kortlandt, A. 1955. Aspects and prospects of the concept of instinct (vicissitudes of the hierarchy theory). Arch. Neerl. Zool. 11, 155-284. Kovach, J. K., Paden, P., and Wilson, G . 1968. Stimulus variables in the elicitation of short range reversibility of early approach and following responses. J. Comp. Physiol. Psychol. 66, 175178. Kmijt. J. P. 1964. Ontogeny of social behaviour in Burmese red junglefowl. Behaviour Suppl. No. 12. Kruijt. J. P. 1973. Expkrience precoce et developpement du comportement social chez Callus Callus spadiceus. In "Problemes de Methodes en Psychologie Comparee" ( M . Richelle and J. Ruwet, eds.), pp. 135-153. Masson. Paris. Kuo, Z. Y. 1932. Ontogeny of embryonic behavior in aves. The influence of embryonic movements upon behavior after hatching. J. Comp. Physiol. Psychol. 14, 109-122. Kuo, Z. Y. 1967. "The Dynamics of Behavior Development." Random House, New York. Lane, H. 1961. Operant control of vocalizing in the chicken. J. Exp. Anal. Behav. 4, 171-177. Lehrman. D., and Rosenblatt. J. 1971. The study of behavioral development. In "Ontogeny of Vertebrate Behavior" (H. Moltz, ed.), pp. 2-29. Academic Press, New York. Lehrman, D., and Wortis, R. P. 1960. Previous breeding experience and hormone induced incubation behavior in the ring dove. Science 132. 1667-1668. Lerner, I. M. 1954. "Genetic Homeostasis." Oliver & Boyd, Edinburgh. Leroi-Gourhan, A. 1964. "Le Geste et la Parole, I , Technique et Langage." Albin Michel, Paris.

ONTOGENESlS AND PHYLOGENESIS

275

Leroi-Gourhan. A. 1965. “Le Geste et la Parole, 2, La Mtmoire et les Rythmes.” Albin Michel. Paris. Leyhausen, P. 1973. On the function of the relative hierarchy of moods as exemplified by the phylogenetic and ontogenetic development of prey-catching in carnivores. In “Motivation of Human and Animal Behaviour” (K. Lorenz and P. Leyhausen, eds.), pp. 144-247. Van Nostrand-Reinhold, New York. Lorenz, K . 1937. The companion in the bird’s world. Auk 54, 245-273. Lorenz, K . 1965. “Evolution and Modification of Behavior.” Chicago Univ. Press, Chicago, Illinois. Lovejoy, A. D. 1965. “The Great Chain of Being.” Harper,New York. Lovejoy, E. 1968. “Attention on Discrimination Learning. ” Holden-Day, San Francisco, California. McFarland, D. I. 1971. “Feedback Mechanisms in Animal Behavior.” Academic Press,New York. Mackintosh, N . J . 1973. Stimulus selection: Learning to ignore stimuli that predict no change in reinforcement. I n “Constraints on Learning” (R. A. Hinde and J. Stevenson-Hinde, eds.), pp. 75-100. Academic Press, New York. Maier, N. R. F., and Schneirla, T. C. 1964. “Principles of Animal Psychology.” Dover, New York. (1st printing, 1935.) Malone, J. C. 1975. The “paradigms” of learning. Psychol. Rec. 25(4), 479-489. Marler, P., 1960. Bird songs and mate selection. In “Animal Sounds and Communication,” Publ. No. 7, pp. 348-367. Am. Inst. Biol. Sci., Washington, D.C. Marler, P., and Mundinger, P. 1971. Vocal learning in birds. I n “Ontogeny of Vertebrate Behavior” (H. Moltz, ed.), pp. 389-450. Academic Press, New York. Martin, R. D. 1974. The biological basis of human behaviour. I n “The Biology of Brains” ( W . B. Broughton, ed.), London. Inst. Biol. pp. 215-256. Mayr. E. 1963. ”Animal Species and Evolution. Belknap Press, Cambridge, Massachusetts. Mayr, E. 1974. Behavior programs and evolutionary strategies. Am. Sci. 62, 650-659. Mead, M. 1972. “Blackbeny Winter; My Early Years.” (Fr. Ed.: “Du Givre sur les Ronces.” Stock, Paris, 1974.) Menzel, E. W . 1971. Communication about environment in a group of young chimpanzees. Folia Prirnatol. 15, 220-232. Meyer, D. R. 1960. The effects of differential probabilities of reinforcement on discrimination learning by monkeys. J. Comp. Physiol. Psyrhol. 53, 173-175. Meyer. F. 1967. Situation epistemologique de la biologie. In “Logique et Connaissance Scientifique (J. Piaget. ed.), pp. 781-821. Gallimard, Paris. Miles, R. C. 1965. Discrimination learning sets. I n ”Behavior of Non-Human Primates” ( A . M. Schrier and F. Stollnitz. eds.), Vol. 1 . pp. 51-95. Academic Press, New York. Mittelman, B. 1960. Intrauterine and early infantile motility. Psyi~hounul.Srudy Child. 15, 104127. Montagner. H. 1967. Le mecanisme et les consequences des comportements trophallactiques chez les Gutpes sociales. Bull. Biol. Fr. Belg. 100, 109-323. Morin. E. 1977. “La Methode. La Nature de la Nature,” Seuil, Paris. Myer, J . S. 1967. Early experience and the development of mouse killing by rats. J. Comp. Physiol. Psycho/. 67, 46-49. Myer. J . S . 1971. Experience and the stability of mouse killing by rats. J. Comp. Physiol. Psycho/. 7 5 , 264-268. Norton Griffiths, M. 1967. A Study of the Feeding Behaviour of the Oystercatcher Haernatopus osrralegus. D. Philos. Thesis, Oxford Univ., Oxford. Nowinski. C. 1967. Biologie, theorie du developpement et dialectique. In “Logique et Connaissance Scientifique” ( J . Piaget. ed.). pp. 862-892. Gallimard, Paris. ”

276

GASTON RICHARD

Oppenheim, R. W. 1973. Prehatching and hatching behavior: Comparative and physiological considerations. In “Behavioral Embryology” (G. Gottlieb. ed.), pp. 164-402. Academic Press, New York. Oppenheim, R. W. 1974. The ontogeny of behavior in the chick embryo. Adv. Study Behav. 5 , 133-172. Pappert, C. 1967. Methodes, techniques et problemes epistemologiques-Epistemologie de la cybernetique-Remarques sur la finalite. In “Logique et Connaissance Scientifique” (J. Piaget, ed.), pp. 424-438. Gallimard, Paris. Petit, C. 1951. Le r6le de I’isolement sexuel dans l’evolution des populations de Drosophila melonogaster. Bull. Biol. Fr. Belg. 85, 392-418. Petit, C., and Nouaud, D. 1976. Ecological competition and the advantage of the rare type in Drosophila melanogmter. Evolution 29. 763-176. Piaget, J. 1967a. “Biologie et Connaissance Scientifique. Gallimard, Paris. Piaget, J. (ed.). 1967b. “Logique et Connaissance Scientifique.” Gallimard, Paris. Piaget. J. 1970a. “Genetic Epistemology.” Columbia Univ. Press, New York. Piaget, J. 1970b. Piaget’s theory. In “Carmichael’s Manual of Child Psychology” (P. H.Mussen, ed.), pp. 703-732. Wiley, New York. Piaget, J. 1974. “Adaptation Vitale et Psychologie de I’lntelligence; Selection Organique et Phenocopie.” Hermann, Paris. Piaget, J., and Inhelder, B. 1969. “The Psychology of the Child.” Routledge & Kegan Paul, London Poland, S . F., and Warren, J . M. 1968. Cat’s performance on visual probability learning problems after prolonged training. J. Comp. Physiol. Psychol. 65, 545-546. Polsky, R. H. 1975a. Hunger, prey feeding, and predatory aggression. Behuv. Biol. 13, 81-93. Polsky, R. H. 1975b. The Ontogeny of Predatory Behaviour in the Golden Hamster. Ph.D. Thesis, Univ. of Leicester, Leicester, England. Polt, J. M.. and Hess, E. M. 1965. Effects of social experience on the following response in chicks. J. Comp. Physiol. Psychol. 61, 268-270. Poole, T. B., and Fish, J. 1975. An investigation of playful behaviour in Rattus norvegicus and Mus musculus. J. Zool. 175, 61-71. Premack, D. 1971. On the assessment of language competence in the chimpanzee. In “Behavior of Non-Human F’rimates” (A. M. Schrier and F. Stollnitz, eds.), Vol. 4, pp. 168-228. Academic Press, New York. Rosenblatt, J . S. 1976. Stages in the early behavioral development of altricial young of selected species of non-primate mammals. In “Growing Points in Ethology” (P. P. G. Bateson and R. A . Hinde, eds.), pp. 345-384. Cambridge Univ. Press, London and New York. Rosenblum, L. A. 1971. The ontogeny of mother-infant relations in macaques. In “Ontogeny of Vertebrate Behavior” (H. Moltz. ed.), pp. 315-367. Academic Press, New York. Royama, T. 1970. Factors governing the hunting behaviour and selection of food by the great tit. J. Anim. Ecol. 39, 619-660. Rumbaugh, D. M.. and Gill, T. V. 1973. The learning skiils of great apes. J. Hum. Evol. 2 , 171. Ryan, J. F. 1973. Early language development. In “The lntegration of the Child in the Social World” (M. P. M. Richards, ed.). Cambridge Univ. Press, London and New York. Salk, L. 1973. The role of the heart beat in the relation between mother and infant. Sci. Am. 228, 26-29. Salzen, E. A. 1962. Imprinting and fear. Symp. Zool. Soc. London 8, 199-217. Salzen, E. A., and Meyer, C. C. 1967. Imprinting: Reversal of a preference established during the critical period. Nature (London) 215, 785-786. Salzen, E. A., and Meyer, C. C. 1968. Reversibility of imprinting. J. Comp. Physiol. Psychol. 66, 269-275. ”

ONTOGENESIS AND PHYLOGENESIS

277

Sander, L. W. 1962. Issues in early mother-child interaction. J . Am. Acad. Child Psychiarr. 1, 141- 165. Sander, L. W. 1964. Adaptive relationships in early mother-child interactions. J. Am. Acad. Child Psychiatr. 3 , 231-265. Saucier, D., and Astic, L. 1975. Etude polygraphique du sommeil chez le poussin a I’eclosion. Evolution aux 3‘ et 4O jours. Electroencephalogr. Clin. Neurophysiol. 38, 303-306. Schleidt, W. M., Schleidt, M., and Nagg, M. 1960. Storung den Mutter-Kind Beziehung bei Triithiihnern durch Gehorverlust. Behaviour 16, 256-260. Schneirla, T. C. 1952. A consideration of some conceptual trends in comparative psychology. Psychol. Bull. 49. 559-597. Schneirla, T. C. 1956. Interrelationships of the “Innate” and the “Acquired” in instinctive behavior. I n “L’lnstinct dans le Comportement des Animaux et de I’Homme” (P. P. Grass?, ed.), pp. 387-452. Masson. Paris. Schneirla, T. C. 1965. Aspects of stimulation and organization in approachlwithdrawal processes underlying vertebrate behavioral development Adv. Study Behav. 1, 1-74. Schneirla, T. C., and Rosenblatt, J. S . 1963. “Critical periods” in the development of behavior. Science 139, 110-1 15. Schiitz, F. 1965. Sexuelle pragung bei Anatiden. Z . Tierpsychol. 22, 50-103. Schweikert, G. E.. and Treichler, F. R. 1969. Visual probability learning and reversal in the cat. J . Comp. Physiol. Psychol. 67, 269-272. Scott, J. P. 1958a. “Animal Behavior. ” Chicago Univ. Press, Chicago, Illinois. Scott, J. P. 1958b. Critical periods in the development of social behavior in puppies. Psychosom. Med. 20, 42-54. Scott, J. P. 1962. Critical periods in behavioral development. Science 130, 949-958. Seligman, M. E. P. 1970. On the generality of the laws of learning. Psychol. Rev. 77, 406-418. Seligman, M. E. P., and Beagley, G. 1975. Learned helplessness in the rat. J . Comp. Physiol. Psychol. 88, 534-541. Seligman, M. E. P., Rosellini, R. A., and Kozak, M. J. 1975. Learned helplessness in the rat. Time course, immunization, and reversibility. J. Comp. Physiol. Psychol. 88, 542-547. Skinner, 9 . F. 1948. “Superstition” in the pigeon. J. Exp. Psychol. 38, 168-172. Skinner, 9 . F. 1975. The shaping of phylogenic behavior. J. Exp. Anal. Behav. 24, 117-120. Sluckin, W . 1962. Perceptual and associative learnings. Symp. Zool. Soc. London 8, 193-198. Sluckin, W. 1972. “Imprinting and Early Learning,” 2nd Ed. Methuen, London. Sudhaus, W. 1976. Recapitulations in the ecoethology of the dipper (Cinclus c i n c h ) . Beirr. Vogelkd. M ,467477. Suomi, S. J., Harlow, H. F., and Novak, M. A. 1974. Reversal of social deficits produced by isolation rearing in monkeys. J . Hum. Evol. 3, 527-534. Sutherland, N. S . , and Mackintosh, N. J. 1971. “Mechanisms of Animal Discrimination Learning.” Academic Press, New York. Thorpe, W. H. 1938. Further experiments on pre-imaginal olfactory conditioning in an insect and its relations to the problem of host selection. Proc. R. Soc. London, Ser. B . 124, 56-81. Thorpe, W. H. 1945. The evolutionary significance of habitat selection. J . Anim. Erol. 14, 67-70. Thorpe, W. H. 1961. “Bird Song: The Biology of Vocal Communication and Expression in Birds” Cambridge Univ. Press, London and New York. Thorpe, W. H., and Hall Craggs, J . 1976. Sound production and perception in birds as related to the general principles of pattern perception. In “Growing Points in Ethology” (P. P. G. Bateson and R. A. Hinde, eds.), pp. 171-189. Cambridge Univ. Press, London and New York. Thorpe, W. H., and Jones, J. 1937. Olfactory conditioning in a parasitic insect and its relations to the problem of host selection. Proc. R. Soc. London, Ser. B 124, 56-81. Tinbergen, L. 1960. The natural control of insects in pine woods. Arch. Neerl. 2001.13, 265-343.

278

GASTON RICHARD

Tinbergen, N. 1951. ”The Study of Instinct.” Oxford Univ. Press (Clarendon), London and New York. Tinbergen, N. 1963. On aims and methods of ethology. Z . Tierpsychol. 20, 410-433. Tinbergen, N. 1965. Behaviour and natural selection. Proc. 1111. Zool. Congr., 16rh, Washingron, D.C. 6, 00-00. Tomatis, A. 1963. “L’Oreille et le Langage.” Le Rayon de la Science, Seuil, Paris. Trivers, R. L. 1974. Parent-offspring conflict. Am. Zool. 14, 249-259. Tschanz, B. 1968. Trottellumen: Die Entstehung der personlichen Bezeihungen zwischen Jungvogel und Eltern. Z . Tierpsychol. 4, 103 pp. Tschanz, B., and Hirsbrunner-Scharf, M. 1976. Adaptation to colony life on cliff edges: A comparative study of Guillemot and razorbill chicks. I n “Function and Evolution in Behaviour” (G. Baerends. C. Beer, and A. Manning, eds.), pp. 358-380. Ullmo, J. 1967. Les concepts physiques. In “Logique et Connaissance Scientifique” (J. Piaget, ed.), pp. 623-705. Gallimard. Pans. van den Assem, J . 1967. Territory in the three spined stickleback Gasrerosfeusaculearus. Behaviour Suppl. No. 16. Van Lawick Goodall, J. 1968. Behaviour of free-living chimpanzees of the Gombe stream area. Anim. Behav. Monogr. No. 3. Vidal, J. M. 1976. Empreinte Filiale et Sexuelle. Reflexions sur le Processus d’Attachement d’apres une Etude Expkrimentale sur le Coq Domestique. Thtse, Univ. de Rennes, Rennes. Vowles, D. M. 1970. Neuroethology, evolution, and grammar. In “Development and Evolution of Behavior: Essays in Memory of T. C. Schneirla” (L. R. Aronson, E. Tobach, D. S . Lehnnan, and J. S . Rosenblatt, eds.), pp. 194-215. Freeman, San Francisco, California. Waddington, C. H. 1957. “The Strategy of the Genes.” Allen & Unwin, London. Waddington, C. H. 1962. “New Patterns in Genetics and Development.” Columbia Univ. Press, New York. Wakerley, J. B., and Drewett, R. F. 1975. Pattern of sucking in the infant rat during spontaneous milk ejection. Physiol. Behav. 15. 277-281. Waller, P. F., and Waller, M. B. 1963. Some relationships between early experience and later social behavior in ducklings. Behuviour 20, 343-363. Warren, J. M. 1966. Reversal learning and the formation of learning sets by cats and rhesus monkeys. J. Comp. Physiol. Psychol. 61, 421. Warren, J. M. 1974. Possibly unique characteristics of learning by primates. J. Hum. Evol. 3, 445-454. Weiland, J. H., and Sperber, Z. 1970. Patterns of mother-infant contact: The significance of lateral preference. J. Gener. Psychol. 117. 225-236. Weiss, P. A. 1974. “L’Archipel Scientifique: Etude sur les Fondements et les Perspectives de la Science.” Maloine. Paris. Wilson, E. 0. 1975. “Sociobiology-the New Synthesis. ” Belknap Press, Cambridge, Massachusetts. Wilson, W. A., Oscar, M., and Bittennan, M. E. 1964. Visual probability-learning in the monkey. Psychonom. Sci. 1, 7 I . Wolff, P. H. 1966. The causes, controls and organization of behaviour in the neonate. Psychol. Issues, Monogr. Ser. 5( I), Monogr. No. 17. Wolff, P. H. 1968. Sucking pattern of infant mammals. Brain Behav. Evol. 1, 354-367. Zajonc, R. B., Reimer, D. J., and Hausser, D. 1973. Imprinting and the development of object preference in chicks by mere repeated exposure. J. Comp. Physiol. Psychol. 83, 434-440. Zeaman, D., and House, B. J. 1963. The role of attention in retardate discrimination learning. In “Handbook of Mental Deficiency: Psychological Theory and Research” (N. R. Ellis, ed.). pp. 159-223. McGraw-Hill, New York.

Subject Index

A Activity, energy requirements and, 57-58 Adult behavior, ontogenesis and, 240-245 Aggression, in monkey, 18 I - I89 All-male groups, in monkey, 169-170 Attachment behavior at home and in strange situation of infant, 31-34 maternal, 34-36 correlations of maternal and infant behaviors, 26-31 developmental changes in, 11-14 direction of effects discussion of findings, 44-47 in limited time period, 40-41 practical implications of, 47-49 over several periods of time, 41-44 three views of, 39-40 individual differences in infant behavior, 14-15 maternal behavior, 15-17 interpretation of findings, 36-38 interrelationships among behaviors infant, 17-19 maternal, 20 maternal and infant, 20-26 study of aims of, 5-6 data analysis, 7-8 data collection, 6-7 statistical procedures, 9-10 strange situation, 8-9 subjects, 6 Attachment theory, 2-5 Aunt behavior, in monkey, 197-201

B

Body mass,energy requirements and, 56 Body size of chimpanzee, 144 of gorilla, 136-137 of man, 149-150 of orangutan, 140 Brain, hormones and reproductive function and, 118-120 Breeding cycle, prolactin secretion and, 113I16 C

Chimpanzee, reproduction in anatomy of female, 145-146 anatomy of male, 144-145 behavior, 143-144 Copulatory behavior, hormones and, 106- 109 Courtship hormones and, 100-103, 112-1 13 photostimulation and, 123 Crying, 11 individual differences in, 14 interrelations between infant and maternal behaviors at, 23-24 maternal response to, 11, 23-24 individual differences in, 15-17 lack of, 27-28

D Dove, reproductive behavior in, 97-98 hormones and, 98-1 18 new directions in, 118-123

E

Bodily contact behaviors relevant to, I 1- 13 individual differences in, 14-15, 16-17 interrelations among, 17-18,20-23,28-31

Ecology, of monkey, 162 Embryo, ontogenesis and, 234-240 Estrogen, see Hormones 279

280

SUBJECT INDEX

F Face-to-face interaction individual differences in, 15. 17 interrelations among behaviors at, 19 interrelations between infant and maternal behaviors at, 24-25 Feeding costs and benefits of, 58-60 energetic costs and. 56-58 as economic problem, 53-55 economics of food choice in, 60-61 laboratory experiments on, 61 natural interpretation of. 61-65 other determinants of, 65-67 search images and, 67-68 patch exploitation and, 73-80 a posteriori information, 83-88 a priori information, 80-83 patterns of, 68-70 meal initiation, 70-71 meal size, 7 1-72 other influences on, 73 Food, group size and spacing and, 201-209 Food abundance, food choice and, 66-67

G Gonadotrophins, see Hormones Gonads, developmentof, photoperiodic stimulation and, 121-123 Gorilla, reproduction in anatomy of female, 138-139 anatomy of male, 136-1 38 behavior, 135-136 Grooming, in monkey, 189-195 Group composition, in monkey, 166-167, 209-210 Groupdynarnics, in monkey, 167-169.209-21 1 Group size, in monkey, 166-167 food and, 20 1-209 Group spread, in monkey, 170-173

H Hormones brain research and, 118-120 copulatory behavior and, 106-109

courtship and nest building and, 100-103, 112-113 female reproductive behavior and physiology and, 103-106 incubation and squab care and, 109-1 16 reproductive synchrony and, 116- I18

I Incubation, hormones and, 109-1 16 Individual differences in infant behavior, 14-15 in maternal behavior, 15-17 Infant, attachment and, see Attachment Intergroup relations, in monkey, 199-201 Interindividual spacing, in monkey, 173-176 food and, 201-209

M Man, reproduction in anatomy of female, 151 anatomy of male, 149- 15 I behavior, 147-149 Meal patterns. 68-70 initiation and, 70-7 I other determinants of, 73 size and, 71-72 Monkey ecological features of, I62 food in relation to group size and spacing, 20 I -209 social behavior in aggression, 181- 189 grooming, 189- I95 intergroup, 199-201 of neonates, 197-199 relations among adult males and their social roles in the group, 177-181 sexual behavior, 195-197 social organization of group dynamics, 167- 169 group size and composition, 166-167. 209-210 group spread, 170-173 interindividual spacing, 173- 176 solitaries and all-male groups, 169-170 time budget of, 162-166 Mother, attachment and, see Attachment

28 1

SUBJECT INDEX

N Neonates, monkey, social interactions of, 197199 Nest building, hormones and, 100-103 Nutrition, food choice and. 65-66

0 Obedience, of infant, behaviors relevant to, 26 Ontogenesis adult behavior and, 240-245 convergences and divergences of, 249-259 embryonic development and, 234-240 phylogenesis and, 229-234, 260-264 mutual constraints between, 264-267 temporal assimilation and, 245-249 Orangutan, reproduction in anatomy of female, 142 anatomy of male, 140-142 behavior, 139-140 Ovariectomy, hormones and, 104-106 Ovaries, development of, photoperiodic stimulation and, 121

P Penis of chimpanzee, 145 of gorilla, 137-138 of man, 150 of orangutan, 141 Photoperiod energy requirements and, 57 reproductive behavior and, 120- I23 Phylogenesis, ontogenesis and, 229-234, 260264 convergences and divergences of, 249-259 mutual constraints between, 264-267 Relaying phase, hormones and, 103-104 Prolactin, see Hormones

R Reproduction, see Sexual selection Reproductive behavior, in ring dove, 97-98 hormones and, 98-1 18 new directions in, 118-123 Reproductive success, male relations and, in monkey, 211-218

Reunion behavior relevant to, 13-14 individual differences in, 15 interrelations between infant and maternal behavior at. 25-26

S Search images, food choice and, 67-68 Semen of chimpanzee, 145 of gorilla, 138 of man, 151 of orangutan, 141-142 Seminal vesicles of chimpanzee, 145 of gorilla, 138 of man, 150-151 of orangutan, 141 Sensory cues, hormones and, 113 Separation behavior relevant to, 13-14 individual differences in, 15 interrelations among infant and maternal behaviors at, 25-26 Sexual behavior, in monkey, 195-197 Sexual crouch, hormones and, 106-109 Sexual selection, 131-135 in chimpanzee anatomy of female, 145-146 anatomy of male, 144-145 behavior, 143-144 in gorilla anatomy of female, 138-139 anatomy of male, 136-138 behavior, 135- 136 in man anatomy of female, 151 anatomy of male, 149-151 behavior, 147-149 in orangutan anatomy of female, 142 anatomy of male, 140-142 behavior, 139-140 Social behavior aggression, I81 -189 grooming, 189-195 intergroup, 199-201 of neonates, 197-199

282

SUBJECT INDEX

relations among adult males and their social roles in the group, 177-181 sexual behavior, 195- 197 Social organization group dynamics, 167-169 group size and composition, 166-167, 209210 group spread, 170- 173 interindividual spacing, 173- 176 solitaries and all-male groups, 169-170 Social roles, of adult mate monkeys, 177-1 8 1 reproductive success and, 211-218 Solitaries, in monkey, 169-170 Squab care, hormones and, 109-1 16 Strange situation, 8-9 behavior at home related to in infant, 31-34 maternal, 34-36

T Temperature, environmental, energy requirements and, 56-57 Temporal assimilation, ontogenesis and, 245249 Testes of chimpanzee, 144-145 of gorilla, 137 of man, 150 of orangutan, 140-141 Testosterone, see Hormones Time budget, of monkey, 162-166