Advances in The Study of Behavior, Volume 15

Advances in

THE STUDY OF BEHAVIOR VOLUME 15

Contributors to This Volume WILLIAM W. BEATTY T. M. CAR0 W. J . CARR DARLENE F. KENNEDY S. N . KHAYUTIN PAUL MARTIN MICHAEL J . MEANEY KLAUS R. SCHERER DAVID F. SHERRY JANE STEWART

Advances in THE STUDY OF BEHAVIOR Edited by

JAY S . ROSENBLATT Institute of Animal Behavior Rutgers University Newark, New Jersey

COLINBEER Institute of Animal Behavior Rutgers University Newark, New Jersey MARIE-CLAIRE BUSNEL Laboratoire de Physiologie Di@&entielle Groupe Ge'ne'tique et Comportements Paris, France PETERJ . B. SLATER Department of Zoology The University St. Andrews Fife, Scotland

VOLUME 15 1985

ACADEMIC PRESS, INC. (Harcourt Brace Jovanovich, Publi\her\)

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Contents

CotitriBic/or.s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pr+uce . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

ix xi

Sex Differences in Social Play: The Socialization of Sex Roles MICHAEL J . MEANEY. JANE STEWART. AND WILLIAM W . BEATTY I. I1 . I11. IV .

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Determinants of Sex Differences in Social Play . . . . . . . . . . . . . . The Function of Social Play . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 4 32 45 48

On the Functions of Play and Its Role in Behavioral Development PAUL MARTIN AND T . M . C A R 0 I. I1 . I11. IV . V. VI . V11.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Defining Play . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Existing Evidence Concerning the Functions of Play . . . . . . . . . . Play May Have No Major Benefits . . . . . . . . . . . . . . . . . . . . . . . . Theoretical Problems in Detecting the Benefits of Play . . . . . . . . Methodological Issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V

59 61 66 78 85 93 97 98

v1

CONTENTS

Sensory Factors in the Behavioral Ontogeny of Altricial Birds S . N . KHAYUTIN

I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105 I1. Organization of Natural Behavior in the Nestling . . . . . . . . . . . . . 108 111. Development of Acoustic Sensitivity . . . . . . . . . . . . . . . . . . . . . . . IV . Role of Audition in the Organization of Defense Behavior . . . . . . V . Ontogeny of Some Visual Mechanisms . . . . . . . . . . . . . . . . . . . . . V1. Complexity of Behavior Organization in Early Postembryonic Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VII . Discussion and Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

118 128 134 138 143 149

Food Storage by Birds and Mammals DAVID F . SHERRY

I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153 I1. Memory and the Recovery of Stored Food . . . . . . . . . . . . . . . . . . 160 111. Social Consequences of Caching . . . . . . . . . . . . . . . . . . . . . . . . . . 168 IV . Economics and Decision Making . . . . . . . . . . . . . . . . . . . . . . . . . . 171 V . Food Storing and Food Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176 VI . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

181 183

Vocal Affect Signaling: A Comparative Approach KLAUS R . SCHERER

I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189 I1 . Empirical Evidence on Vocal Indicators of Emotion . . . . . . . . . . . 191 111. A Psychobiological Approach to Emotion . . . . . . . . . . . . . . . . . . . IV . Emotional Determinants of Vocalization .................... V . The Component Patterning Theory of Vocal Affect Expression . . VI . Cross-Species Universality in the Component Patterning of Vocal Expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VI1. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

198 206 215 235 237 238

CONTENTS

vii

A Response-Competition Model Designed to Account for the Aversion to Feed on Conspecific Flesh W. J . CARR AND DARLENE F. KENNEDY

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. The Aversion by Norway Rats to Feed on Conspecific Flesh . . . . III. A Response-Competition Model . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Constraining Intraspecific Predation via Response-Competition . .

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Contents of Previous Volumes . . . . . . . . . . . . . . . , . . , . . , . , . . . . . . . . . . . . . . . . , . . , . . , . .

245 248 263 268 270

215 279

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

WILLIAM W. BEATTY ( I ) , Departtnent University, Fargo, North Dakota 58105

of Psychology, North Dakota State

T. M. C A R 0 (59), Sub-Department of Animal Behuviour, University of Cambridge, Madingley, Cambridge CB3 8AA, England

W. J. CARR (245), Department of Psychology, Beaver College, Glenside, Pennsylvania I9038 DARLENE F. KENNEDY (245), Department of Psychology, Beaver College, Glenside, Pennsylvania I9038

S. N. KHAYUTIN (103, USSR Academy of Sciences, Institute of Higher Nervous Activity and Neurophysiology, Moscow I 1 7485, USSR PAUL MARTIN (59), Sub-Department of Animal Behaviour, University of Cambridge, Madingley, Cambridge CB3 8AA, England MICHAEL J . MEANEY ( l ) , Center for Studies in Behavioral Neurobiology, Department of Psychology, Concordia University, Montreal H3G I M 8 , Canada KLAUS R. SCHERER (189), Department of Psychology, University of Giessen, 0-6300 Giessen, Federal Republic of Germany DAVID F. SHERRY (153), Department of Psychology, University of Toronto, Toronto, Ontario M5S I A l , Canada JANE STEWART ( l ) , Center for Studies in Behavioral Neurobiology, Department of Psychology, Concordia University, Montreal H3G l M 8 , Canada

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Preface The aim of Advances in the Study of Behavior is to serve the increasing number of scientists who are engaged in the study of animal behavior by presenting their theoretical ideas and research to their colleagues and to those in neighboring fields. Since its inception in 1965, this publication has not changed its aim, to serve “. . . as a contribution to the development of cooperation and communication among scientists in our field.” We acknowledge that in the interim new vigor has been given to traditional fields of animal behavior by their coalescence with closely related fields and by the closer relationship that now exists between those studying animal and human subjects. Scientists studying animal behavior now range from ecologists to evolutionary biologists, geneticists, endocrinologists, ethologists, comparative and developmental psychobiologists, and those doing research in the neurosciences. As the task of developing cooperation and communication among scientists whose skills and concepts necessarily differ in accordance with the diversity of phenomena that they study has become more difficult, the need to do so has become greater. The Editors and publisher of Advances in the Study of Behavior will continue to provide the means to meet this need by publishing critical reviews, by inviting extended presentations of significant research programs, by encouraging the writing of theoretical syntheses and reformulations of persistent problems, and by highlighting especially penetrating research that introduces important new concepts.

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ADVANCES IN THE STUDY OF BEHAVIOR. VOL. 15

Sex Differences in Social Play: T h e Socialization of Sex Roles* MICHAEL J. MEANEYAND JANE STEWART CENTER FOR STUDIES IN BEHAVIORAL NEUROBIOLOGY DEPARTMENT OF PSYCHOLOGY CONCORDIA UNIVERSITY MONTREAL, CANADA

WILLIAMW . BEATTY DEPARTMENT OF PSYCHOLOGY NORTH DAKOTA STATE UNIVERSITY FARGO, NORTH DAKOTA

Introduction ........................ ............ Determinants fferences in Social Play . . . . ...... A. Social Play in Mammals.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Sex Differences in Social Pla ..................... C. Neuroendocrine Basis of Sex rences in Social Play.. . . . . . . . . . . D. Social Influences in Social Play.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. The Function of Social Play . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Developmental Significance of Social Play. . . . B. Relationship between Sex Differences in Adult Behavior and the Nature of the Contribution of Social Play to Social Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Sex Differences in the Response to Social Deprivation.. . . . . . . . . . . . D. Possibility of Immediate Consequence of Social Play . . . . . . . . . . . . . . IV. Conclusion . . . . . . . . . .................................... References . . . . . . . . . ....... ............. I.

11.

2 4 4 14 17 28 31 32 32

34 44 45 46 48

*We are publishing two articles on the subject of play in this volume of Advances in rhe Srudy of Behavior. The two articles are quite different from one another and, since this series has not published any articles on play in previous volumes, we felt that having these two articles would provide our readers with a limited survey of this interesting and important topic in animal behavior [the Editors].

I

Copyright 0 198.5 hy Acddcmic Press. Inc. All rights of reproductinn In any forni reserved. ISBN 0-12-004.515-X

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MICHAEL J. MEANEY ET AL.

I.

INTRODUCTION

Sex differences in social behavior exist in all mammalian species. The very act of copulation requires that the participants be engaged in different behaviors. These differences also extend to courtship or proceptive behaviors, such that males are normally attracted to the social cues of females and females are normally attracted to the social cues of males. In most species, however, there are sex differences in social behavior that extend beyond these rather obvious differences in mating behavior. Reports of sex differences in behaviors such as social grooming, infant care, territorial defense, and dominance-related activities are common, especially in primate species (for a review, see Mitchell, 1979). Variations occur across species in the extent to which the occurrence of these and other nonsexual, social behaviors are sexually dimorphic. Nevertheless, in most species of social-living mammals, there exist sex roles within groups. One problem that has received considerable attention has been the description of the factors that influence the development of sex differences in social behavior. The majority of the work on this problem has focused on the influence of perinatal hormonal events and, in particular, on the influence of gonadal steroids. Thus, in many species the expression of a particular, sexually dimorphic behavior has been associated with the early exposure to gonadal hormones (for reviews, see Beatty, 1979; Goy & McEwen, 1980). This developmental influence has been attributed to an organizational effect of gonadal hormones (Phoenix, Goy, Gerall, & Young, 1959). According to this organizational hypothesis, hormones act during an early period of neurogenesis to organize the CNS in such a way that an individual is predisposed to respond to a particular stimulus in a certain way. An organizational effect is an empirical concept, and it is defined by instances in which the probability of the occurrence of a particular behavior can be statistically related to the presence or absence of a hormone during some previous period of development. In examining this hypothesis, behavioral endocrinologists have described several hormonal events that, in part, account for the development of sex differences in social behavior. The development of social behavior, including behaviors that are sexually dimorphic, is also dependent on the early social experience of an animal. There is strong evidence from several mammalian species, and in particular from rhesus monkeys, that the deprivation of social contact during the preadult period interferes with the ability of an animal to exhibit normal social behavior. Behaviors such as male mounting (e.g., Harlow, 1969; Gerall, Ward, & Gerall, 1967; Hard & Larsson, 1968), female presenting (Harlow, 1969), agonistic behavior (Lore & Flannelly, 1977; Mason, 1961), and affiliative behaviors (Harlow, 1969) have all been found to be influenced by the absence of early social contact. Thus, in many species the ability to express male-typical or female-typical patterns of behavior is dependent on certain early experiences with other animals.

SOCIAL PLAY

3

Considered in this way, the degree to which an animal expresses the behaviors typical of the male or female role within any group is dependent on early social interactions with conspecifics as well as on perinatal and concurrent hormonal events. In most species these early social interactions occur in the context of play behavior, and it is interesting to note that there are, in many species, sex differences in the social play of young animals (see Table I). The range of species (literally from pinnipeds to primates) in which sex differences in social play have been observed is impressive. These sex differences in the social play of infant and juvenile animals suggest that the opportunities for early social learning may depend on the gender of the young. The possibility exists, then, that these sex differences in social play contribute directly to sex differences in adult social behavior. The two questions that emerge from these considerations, and the questions upon which we have focused this article, are (1) what are the determinants of sex differences in social play and (2) what are the functions of sex differences in the socialization process as a whole. In the pages that follow we shall argue that social play does serve to facilitate the social development of young animals and that sex differences in social play are directly related to sex differences in adult social behavior. In answer to the question of the determinants of sex differences in social play, it appears that perinatal hormones, independent of their actions on adult social behaviors, exert organizational effects on social play. The sex differences observed in one form of social play, play-fighting, appear to be due, in part, to the actions of perinatal androgens. Sex differences in social play, however, also seem to be influenced by the differential behavior of the adults, especially the mother, toward the male and female infants. The behavior of the adults toward male infants appears to enhance the forms of social interactions that best serve the social development of males, and the same appears to be true of the behavior of adults toward female infants. Thus, both perinatal hormone actions and adult-infant interactions serve to promote sex differences in social Play. This illustration of sex differences in the socialization of infant and juvenile behavior is not universal across species. Likewise, sex differences in adult social behavior also vary across species. This variation can serve as the basis for a comparative analysis. The approach taken here with respect to the function of play has been to compare the social play of males and females in species in which there are well-documented sex differences in adult social behavior with that of species in which sex differences in adult social behavior are far less pronounced. We believe that this form of analysis may be one of a few ways in which to address meaningfully the question of the function of social play. There are several pitfalls in attempting to generate conclusions based on the behavior of species that vary greatly in their morphology, ecology, and social organization. It is unlikely that we have avoided all of them. The present analysis

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MICHAEL J . MEANEY ET A L .

TABLE I S U M M A R Y OF

EVIDENCE FOR

S t X D l b F E R t N C t S IN

PLAY-FIGHTING ACROSSSPECIES Finding

6>9

Species studied

6-9

Primate Hominoideu (apes and man)

Humans

Blurton-Jones (1976); Braggio et a / . (1978); Blurton-Jones and Konner ( 1 973) van Lawick-Goodall (1968)

Chimpanzees Cercopithecoideu (old-world

monkeys) Cercopithecinae

Rhesus monkey

Bonnet monkey Stumptail monkey

Harlow ( I 965); Hinde and Spencer-Booth (1967); Symons ( 1974) Simonds (1977) Bertrand (1969)

Olive baboon Hamadryas baboon

Owens (1975a.b) Kummer 1968)

Pupio

Cercopithecus

Vervet monkey

Bramlett (1978); Raleigh

Talapoin monkey Patas monkey

Wolfheim ( 1977) Seay et al. (1972)

(1979)

Colobinae

Hanuman langurs

Jay (1963); Hrdy (1977)

does, however, provide a number of hypotheses that can in the future be directly refuted by observations from the appropriate species. In this way we believe that the analysis provided in this article forms a context within which a fruitful debate about social development might occur.

11.

A.

DETERMINANTS OF SEXDIFFERENCES I N SOCIAL PLAY

SOCIALPLAYI N MAMMALS

In this section we shall outline the various forms of social play that have been reported to occur among juvenile mammals. In addition, we shall consider the problem traditionally associated with play behavior, that of the definition of play as a behavioral category.

5

SOCIAL PLAY

TABLE I (Continued) Finding Species studied

Ceboideu (new-world monkeys) Suirniri Squirrel monkey Cullitrichinue Common marmoset Nonprimate species Cunis Timber wolf Coyote Domestic dog F r lidue Domestic cat Rodentiu Norway rat

Golden hamster

d > ?

6 5 9

Baldwin and Baldwin ( 1974) Abbott (1978)

Bekoff (1974, P.c.; Traylor, 1982) Bekoff (1974) Bekoff ( 1974) Barrett and Bateson (1978) Meaney and Stewart (1981a,b); Poole and Fish (1976); Olioff and Stewart (1978) Goldman and Swanson (1975)

Mongolian gerbil

Meaney (unpublished)

OViS

Domestic sheep Pinniped Stellar sea lion

Sachs and Harris ( 1978) Gentry (1974)

1. Play-Fighting

The most commonly reported form of social play is that of play-fighting, this behavior has also been referred to as rough-and-tumble play (e.g., BlurtonJones, 1976; Harlow, 1969) or as mock combat (Calhoun, 1962). The behavioral components of play-fighting vary from species to species but are generally predictable from a knowledge of those components involved in the fighting of adults. As Aldis (1975) has noted, the apparent “goal” of the participants involved in play-bout is to “mouth” or to play-bite an opponent (see Figs. 1-3). Both of these behaviors may be interpreted as an inhibited form of biting. In many species play-fighting also involves an attempt to get on top of (to dominate) the other animal, and descriptions of play-fighting invariably include a reference to wrestling-like behaviors (see Figs. 4-6).

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MICHAEL J . MEANEY ET AL.

FIGS. 1-3. Play-fighting in wolf cubs and in juvenile vervet monkeys. Note the open mouth approach in each case. All photographs in the text are by M. Meaney and D. Cantin.

SOCIAL PLAY

7

Fig. 3.

This apparent similarity between the behavioral components that make up play-fighting and those that constitute one feature of the agonistic encounters of adults, then, is one of the defining features of play-fighting. Naturally this raises the question of how one in turn can discriminate between play-fighting and intraspecific aggression. Traditionally, play-fighting has been distinguished from “real” fighting by its seeming lack of seriousness. Even though this may appear a somewhat nebulous and unsatisfying description, it is not hard to find evidence for the differences between play-fighting and intraspecies aggression. An example comes from the work of Poole (1966) with polecats (Mustella putorius). Poole reports that five out of seven of the behaviors that appear in the attack component of the agonistic encounters of adults also appear in the play-fighting of juveniles, as do three out of four of the behaviors that constitute the defensive components. The two attack behaviors that were absent in play-fighting (sustained neck-biting and sideways attack) are behaviors that serve the function of inflicting injury on an opponent. The defensive behavior not seen in play-fighting was that of defensive threat. The “screaming” vocalization recorded from attacked adults was also not heard during play-fighting. These latter two behaviors may be seen as a response to the attack components of neck-biting and sideways attack. Thus, in the play-fighting of polecats, the more extreme forms of both the attack and the defensive components of adult aggression are not observed. Similarly, in the play-fights of juvenile Norway rats, the distress vocalizations that are common in the agonistic encounters of adults are rarely

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MICHAEL J . MEANEY E T AL.

FIGS.4-6. Play-fights in several species (shown here in wolf cubs, hamadryas baboons, and Norway rats) culminate in one animal on top of another.

SOCIAL PLAY

9

Fig. 6.

recorded (Calhoun, 1962; Meaney & Stewart, 198 la). Another distinguishing feature of play-fighting among rats is that, unlike adult agonistic encounters, roles (i.e., attacker/target) are frequently reversed; an animal that is dominated for a brief period during a play-bout will often immediately pounce on the other animal and then dominate it (Poole & Fish, 1976). Symons (1974) has reported that in the rhesus monkeys the facial expressions that characterize the combatants in an aggressive encounter are not seen in the play-fighting of juveniles. Particularly noteworthy is that in the play-fighting of rhesus monkeys “there are no gestures of threat or submission” (p. 321). Rather, in many species there are facial expressions (van Hoof, 1972; Symons, 1974) and body postures (Bekoff, 1974) that are unique to play-fighting. In children (Blurton-Jones & Konner, 1973) the feature most commonly associated with play-fighting is a laugh-play face. Thus, while play-fighting is similar to the fighring components of an agonistic encounter, it bears little resemblance to the ritualized forms of intraspecies aggression (particularly the communication of threat) that predominate within the stable social groups of most mammals. In addition, play-fighting contains only the milder forms of attack and defense seen in the fighting of adult animals. Most notably absent in play-fighting are components that lead to the infliction of injury in an opponent and, thus, the components associated with “defeat.” It is probable that, although one animal may gain the upper hand in the course of a wrestling bout, there is no defeat or complete submission. Thus,

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MICHAEL J . MEANEY ET AL.

the immediate function for the participants of a play-fight is apparently different from that for animals involved in an agonistic encounter whether it involves direct fighting or ritualized gestures.

2.

Chase Play

Harlow (1969) has described a form of play that occurs between juvenile rhesus monkeys and that has been termed approach-avoidance play. This form of play involves one animal approaching and then quickly retreating from another animal. The end point of this sequence is often a chase in which the animal that has been approached chases the animal that has withdrawn. Owens (1975a) has described a very similar pattern of social play in juvenile olive baboons, referred to as dodging play. Here again the pattern seems to be an invitation for chase. We have observed a similar form of social play in juvenile Norway rats. Among rats the sequence involves an approach and pounce followed almost immediately (<.5 sec) by a quick retreat that usually involves two leaps away from the target animal. Once again the pattern is often followed by a chase. This form of play is similar to the solicitation pattern of the adult female rat (see McClintock & Adler, 1978). The immediate consequence of this form of play is also the same as that of the solicitation pattern of the adult female since both behaviors often elicit a chase response (see also Thor & Holloway, 1983). Among adults the entire sequence seems to facilitate copulatory behavior in male rats (Caggiula, Shaw, Antelman, & Edwards, 1976).

3 . Play-Mothering Lancaster (1971), working with vervet monkeys, has provided the most detailed descriptions of this form of play. Play-mothering emerges from the attraction of juveniles toward the infants in the group. The juveniles often sit beside the mother, awaiting the opportunity to “play” with the infant. Once with the infant, under the scrutiny of the mother, the juvenile engages in several of the species-specific, behavioral components of maternal behavior (e.g., carrying, grooming). Probably the most complex skill involved here is in procuring the infant from its mother. In our studies with vervets we have found that for the younger females only about one-third of these attempts to secure the infant are successful and that about the same portion result in the mother threatening the juvenile (see Figs. 7-10). The period of time the juvenile is afforded with the infant seems to depend on its ability to keep the infant acquiescent, since at the infant’s cry the mother reclaims her offspring. Thus, in our work with this species we have found that the older, subadult females are able to hold onto the infant for a much longer period of time than the younger, juvenile females. Play-mothering has been reported in several other primate species (also see Hrdy, 1976), including chimpanzees (van Lawick-Goodall, 1968), rhesus

SOCIAL PLAY

11

monkeys (Chamove, Harlow, & Mitchell, 1967), barbary apes (Burton, 1972), squirrel monkeys (Baldwin, 1969),olive baboons (Owens, 1975a), and hanuman langurs (Hrdy, 1977; Jay, 1963). In general, the descriptions of play-mothering in these species are similar, focusing on holding, carrying, and grooming of infants. The greatest species variation in this form of play appears to be the degree of reluctance of the mother to part with her infant rather than in the behavior of the juveniles toward the infants (see Hinde, 1971). Most reports of play-mothering refer to the persistence of the juveniles in obtaining access to infants. In the vervet monkeys, females from 6 months to 4 years of age interact more often with infants than do adult females (Struhsaker, 1967). We find that among adult females, nulliparous females spend more time with the infants than do multiparous females (including multiparous females who do not have infants at the time). 4.

Play in General

These, then, are the three most prominent forms of social play that occur among juvenile mammals. In each case some argument might be raised to defend the application of the term play to these behavior patterns. Indeed, much has been written debating the merits of considering play as a definable behavioral category. Problems relating to the defining of boundaries around play as a behavior have emerged from the apparent absence of any immediate biological significance. Recent attempts to define play have ignored this feature and concentrated on behavioral differences (e.g., play markers such as the play faces of several primate species). These attempts to define play, however, fly in the face of the fact that there are age changes in social play: The play behavior of animals at one age is different from that of animals at a later age (see Chalmers, 1980; Meaney & Stewart, 1981a; Owens, 1975a). An example of such an age-related change can be seen in the play-fighting of rats. As described earlier, in young rats (between 21 and 45 days of age) play-fighting is marked by dominance reversal (Poole & Fish, 1976). Between 45 and 55 days of age, however, stable dominance relations begin to emerge from the play-fights of male pups. Typically, during this later age one male pup dominates a play-fight far more often than does any other (Meaney & Stewart, 1981a). The role-reversal marker of play-fighting in juvenile male rats is absent after day 45. Other markers, such as the absence of distress vocalizations, remain, and play-bouts appear to the casual observer to be the same throughout the juvenile period. Age-related changes are not unique to rodents. Several authors have reported that the vigor of playfighting in juvenile males in many primate species increases with age (the physical strength of the animals is also increasing). These age-related changes challenge strict definitions of play based on the presence or absence of behavioral markers. As Chalmers (1980) has pointed out, it is fruitless to devote time and effort to defining what play is and what it is not.

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MICHAEL J . MEANEY ET AL.

FIGS.7-10. In the vervet monkey, as in several primate species, juvenile females show an intense interest in the infants of the group. It is common to see a mother-infant pair in the company of juvenile females. The juveniles sit beside the pair and often attempt to

SOCIAL PLAY

13

touch or hold the infant. This frequently results in the mother being groomed by juvenile females.

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MICHAEL I . MEANEY ET AL.

Rather it would appear to be more useful to dedicate efforts to describing patterns of social development in a species and to identifying, at many levels, the factors that influence the performance of particular early social behaviors (cf. Lazar & Beckhorn, 1974). By deemphasizing the label play, it might be easier to get on with the problem of studying the development of social behavior. This would appear true regardless of whether one’s interests are phylogenetic or ontogenetic. Play is, then, what many young animals do, and the question is how does this behavior and the socialization process as a whole contribute to social development?

B.

SEXDIFFERENCES I N SOCIALPLAY

In most of the mammalian species in which the social play of males and females has been compared, sex differences have been found. Although there are more data on play-fighting than on either play-mothering or chase play, this holds true for each of the three forms of social play that were discussed in the previous section. Fortunately, the direction and degree of these sex differences are not universal, and thus a comparative approach is an interesting venture. 1 . Pluy-Fighting

A summary of the data on sex differences in play-fighting is presented in Table I. It can be seen that in most of the species in which this question has been examined males engage in more play-fighting than do females. This sex difference has been observed in several primate species and also in two rodent species (the golden hamster and the Norway rat) as well as in domestic sheep and in sea lions. In each of the studies summarized in Table I, the sex difference has been established on the basis of differences in the frequency with which juvenile males and females have been observed to engage in play-fighting. Several papers have also reported a sex difference in the intensity of playfighting. Typically, it is claimed that males play-fight more vigorously than do females. A common finding among various primate species is that among animals of less than 1 year, play groups are composed of both males and females; as the animals grow older and as the intensity with which the male play increases, the females leave the play groups. Play groups of juveniles are reported to be composed of males only (see DeVore, 1963; Kummer, 1968; Owens, 1975a). In these primate species, then, the factors that seem to contribute to the sex difference in play-fighting appear to be characterized by the intensity with which males play-fight and, possibly, by the tendency of females to avoid play-fights of male-typical intensity. These features do not account for the sex difference in the play-fighting of subadult primates. First, Goy (1978) has found that in rhesus monkeys the sex difference in play-fighting is apparent prior to the period when females and males form separate play groups (i.e., during the infant stage).

15

SOCIAL PLAY

Second, Goldfoot and Wallen (1978) found that female rhesus monkeys reared only with females did not differ from females reared with males in the frequency with which they engaged in play-fighting. Thus, apart from sex differences in the intensity with which juveniles engage in play-fighting, there is very likely also a sex difference in the tendency to initiate and become involved in a play-fight. The nature of the sex difference in play-fighting has also been examined in the Norway rat. In this species, unlike most primate species, males and females play together throughout the preadult period. The difference, however, is one of degree since, as in several primates, male pups tend to play-fight more with males than with females whereas female pups tend to play-fight no more with females than with males (the exception to this is during the period just prior to puberty when both males and females play-fight more with animals of the opposite sex than with animals of the same sex; Meaney & Stewart, 1981a). Over all ages studied, males initiate (i.e., pounce on another animal) more play-fights than do females (Meaney & Stewart, 1981a; Poole & Fish, 1976). In contrast, females are more likely to withdraw from a play-initiation (i.e., immediately after being pounced on) than are males. In addition, once involved in a playfight, females are more likely to withdraw prior to the formation of a “dominance” relation (i.e., one animal on top of another; see Fig. 11) than are males (Meaney & Stewart, 1981a). In the Norway rat, then, the difference in the frequency with which male and female pups are observed to be engaged in playfighting is due to the tendency of males to initiate play-fights more often than females and the tendency of females to withdraw from play-fights more than males. Apart from the purported sex difference in the intensity of play-fighting in some primate species, there is no evidence that when females do engage in playfights they do so in a manner that is otherwise qualitatively different from that of males (also see Goy, 1970). In the Norway rat the behavioral components of play-fighting are the same for both males and females (Meaney & Stewart,

9 FIG. 1 I . Depicted here is a summary of the sex differences in the social play of the Norway rat. The top sequence shows the pattern of play most commonly seen in males, that of the complete play-fight sequence. The lower sequence shows the hit-and-run pattern of social play (pounce + withdrawal) and the withdrawal prior to the completion of the play-fight sequence. Both of these behaviors are observed considerably more often in females than in males.

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MICHAEL J . MEANEY ET A L .

1981a; Poole & Fish, 1976). Thus far, it appears reasonable to conclude that the sex differences in play-fighting do not include differences in the manner in which animals play-fight. Females do not differ from males in their potential to playfight. It is, therefore, unlikely that there are sex differences in the motor systems involved in play-fighting. The greater tendency of females to withdraw from play-fights suggests that females may react differently from males to the tactile stimulation derived from play-fighting (see Bell & Costello, 1964; Wolff, 1966). Table 1 also reveals that there are some conspicuous exceptions to the sex differences just discussed. Although the studies with canids involved small sample sizes, the results consistently show that females engage in play-fighting as frequently as do males. Moreover, in our work with wolves (Traylor, 1982), we have found that there are no sex differences in the behavioral components of play-fighting in this species. The absence of sex differences in the play-fighting of these carnivores does not appear to be due to the inclusion of predatory patterns of behavior (e.g., stalking) that might mask sex differences in intraspecies patterns of social behavior. Even when predatory patterns are excluded, there are still no sex differences in the frequency with which juvenile male and female wolves engage in play-fighting. Likewise there appears to be no sex difference in the frequency of play-fighting in kittens. Given the apparent absence of sex differences in play-fighting in four species of carnivores, it is interesting to note that in preliminary studies on juvenile northern grasshopper mice (Onychomys Ieucogaster), a predatory rodent species, Davies and Kemble ( I 983) have observed that juvenile males and females engage in play-fighting at similar rates. Thus, although sex differences in play-fighting are common in mammalian species, they are not universal.

2.

Chase Play

This pattern of play has been far less well studied than has play-fighting. Nevertheless, sex differences have also been reported in chase play, particularly among primates. Harlow ( 1969) reports that among juvenile rhesus monkeys females engage in more approach-avoidance play than do males. Owens (1975a) has presented a similar finding with olive baboons with respect to dodging play. In some recent work we have found that female Norway rat pups exhibit more hit-and-run play than do male pups. In both olive baboons and Norway rats, it appears that males are most often the targets of this play and do most of the chasing.

3. Pkuy-Mothering This intriguing pattern of juvenile activity has been most often observed in primate species. In the species in which this pattern of play has been scored, it has been found to be predominantly a female-performed activity. Among hu-

SOCIAL PLAY

17

mans a large number of studies (reviewed by Berman, 1980) have found that juvenile females are more responsive to infants than are same-aged males. Moreover, fantasy play with infant-like dolls is far more common among young females than among young males. Similar results have also been reported for vervet monkeys (Lancaster, 1971), rhesus monkeys (Chamove et al., 1967), and squirrel monkeys (Baldwin, 1969). In the vervet we found that males account for less than 5% of the play-mothering directed toward infants. In the rhesus monkey there appears to be a qualitative difference in the response of male and female juveniles to infants. Whereas females exhibit care-giving behaviors, the males are often hostile and aggressive toward the infants. As is the case with play-fighting, however, the pattern of sex differences described above is not universal. Among juvenile Barbary apes, it is the males that exhibit the greater interest in the infants (Burton, 1972). It is noteworthy that in this species the adult males participate a great deal in the care and the socialization of the infants (Burton, 1972). Among nonprimates the response of juveniles to infants has been little studied. This, of course, might be simply because there is little if any significant interaction between the two age groups. One, possibly analogous behavior has been reported by Schaller (1972) in his work with lions. Schaller reported that juvenile lionesses spend more time play-fighting with young cubs than do males. Although the infant-directed behavior in this case is not what is traditionally considered as care-giving, it suggests that juvenile lionesses are more responsive to cubs than are same-aged males. In the Norway rat, prepubescent males and females are strongly attracted to neonates and will engage in many components of maternal behavior if exposed to pups for a few hours (Bridges, Zarrow, Denenberg, 1973; Mayer & Rosenblatt, 1979a,b). Contact seeking declines sharply in animals tested first around 24 to 25 days of age, but animals exposed at an earlier age remain responsive while females become more responsive under the influence of ovarian estrogens (Mayer, Freeman, & Rosenblatt, 1979; Mayer & Rosenblatt, 1979b).

C . NECJROENDOCRINE BASISOF SEXDIFFERENCES I N SOCIAL PLAY In this section we shall present a review of the research that has examined the influence of gonadal and adrenal steroid hormones on social play, as well as some preliminary work describing the neural system(s) that underlie social play. The work done on this topic has focused primarily on play-fighting in species in which males engage in a higher frequency of play-fighting. The following analysis, therefore, deals mostly with the development of this more male-typical form of social play. Future efforts should address this issue with respect to other forms

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MICHAEL J . MEANEY E T AL.

of social play, such as play-mothering, that are observed to occur more often in females than in males, and this is one of the goals of our vervet project.

I.

Hormonal Influences on Play-Fighting

When trying to determine the relationship between hormones and play-fighting, the first step is simply to identify those hormones that influence the playfighting of young animals. The second step is to determine the temporal characteristics of any hormonal influence on play-fighting. The literature on hormonebehavior interaction (for reviews see Beatty, 1979; Eleftheriou & Sprott, 1975a,b; Goy & McEwen, 1980) demonstrates that there are, generally speaking, two ways in which hormones influence behavior. The first concerns the activational effects of hormones on behavior. When the presence or absence of a hormone at or near the time of observation can be related to the probability of occurrence of a behavior, the hormone can be said to have an activational effect. That is, the hormone is considered to “activate” or in some cases to “deactivate” a particular behavior. The effects of hormone replacement therapy following castration on the sexual behavior of adult male and female rats (e.g., Beach, 1956) are classic examples of activational effects. The second way in which hormones are said to influence behavior is by their organizational actions on the CNS during some early developmental period (i.e., a period of neurogenesis). Such actions are thought to predispose an individual to respond preferentially to particular external stimuli and to the effects of circulating hormones (Phoenix et al., 1959). Instances in which the probability of the occurrence of a particular behavior can be related to the presence or absence of a hormone during some previous period of development represents an organizational effect. The altered sexual behavior of adult female rats treated neonatally with testosterone (see Baum, 1979, for a review) is an example of an organizational effect. It should be noted that neither organizational nor activational effects are defined by the processes by which they influence behavior because these hormonal effects may be mediated by various neurochemical events (both intracellular and extracellular). Rather they are defined by the temporal characteristics of the hormonal effects. It is for this reason that much of the research described in this section has focused on the temporal boundary of a hormonal effect.

2. Gonadal Steroids In the rhesus monkey juvenile males engage in far more play-fighting than do their female peers (see Table I). Goy and Phoenix (1971) found that genetic females that were exposed prenatally to high levels of testosterone (the major testicular androgen circulating in the blood) engaged in play-fighting at rates that were indistinguishable from those of normal males. Similarly, in the Norway rat, females treated with testosterone on days I and 2 of life did not differ from normal male pups in the frequency with which they engaged in play-fighting

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19

(Meaney & Stewart, 198 I b; Olioff & Stewart, 1978). Male rat pups castrated on day I (thus eliminating the primary source of endogenous testosterone) engaged in play-fighting at rates that were significantly less than those of intact males and that were not different from those of normal females (Meaney & Stewart, 1981b). Finally, male pups treated on days 1 to 10 with the antiandrogen Flutamide engaged in play-fighting at rates that were less than those of control males and that were similar to those of normal females (Meaney, Stewart, Poulin, & McEwen, 1983). These results with Flutamide are identical to those with day 1 castration. Thus, in both the rhesus monkey and the Norway rat, the early exposure to androgens during a critical period for brain development' appears to influence the frequency of play-fighting seen during the juvenile period. Since neonatally androgen-treated females, otherwise lacking testicular secretions, engaged in male-typical levels of play-fighting, it seems as though later circulating levels of androgens do not influence the expression of play-fighting. Direct tests have supported this conclusion. Joslyn (1973) has found that in contrast to prenatal treatment, the postnatal testosterone treatment of female rhesus monkeys did not influence the frequency with which they engaged in play-fighting. Similarly, Goy (1970) has reported that male rhesus monkeys that were castrated at birth play-fought as frequently as did intact males. In the rhesus monkey, then, androgen exposure beyond the critical period for sexual differentiation did not affect the expression of play-fighting. A similar finding has emerged from studies with Norway rat pups. Male rat pups castrated on either days 10, 20, or 23 did not differ from intact males in the frequency with which they engaged in play-fighting (Beatty, Dodge, Traylor, & Meaney, 1981; Meaney & Stewart, 1981b). Moreover, intact male pups injected daily with 200 k g of testosterone did not differ from controls in their play-fighting (Meaney & Stewart, 1983). Thus, in neither the rhesus monkey nor the Norway rat was the expression of male-typical levels of play-fighting found to be dependent on the presence of testosterone during the juvenile period (i.e., during that period when the sex difference is observed). Androgens are secreted not only by the testes but also by the adrenals. In humans some data relevant to the present question have been collected in children with an adrenal abnormality that results in a high exposure to adrenal androgens. This condition has been referred to as congenital adrenal hyperplasia (CAH) and is a genetic abnormality in which the adrenal cortex fails to produce cortisone. Instead there is an excessive secretion of adrenal androgens from the 'It is important to note that the carly neonatal period in the Norway rat and prenatal period in the rhesus monkey are periods of neurogenesis. These periods have also been found to be critical periods for the sexual differentiation of copulatory behavior and of its putative neural substrates (for a review, see Coy & McEwen, 1980).

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MICHAEL J . MEANEY ET AL.

prenatal period up until the time when the disorder is detected and treated. CAH females are born with masculinized genitalia and unless the condition is detected early they are often reared as males. The population of interest here are CAH females in which the detection has occurred early. There are two advantages to studying these children. First, when the detection occurs early in postnatal life, the endocrine condition can be rectified, thus limiting the period of excessive androgen exposure primarily to the prenatal stage. Second, these females are reared as females. Such girls have been found to engage in male-typical forms of play and to be identified as “tomboys” more often than control subjects (usually unaffected, same-sex siblings) (Ehrhardt, Epstein, & Money, 1968; Ehrhardt & Baker, 1974). These results are, of course, similar to those of Goy (1978) and of Meaney & Stewart (198 1 b) with perinatally androgenized female monkeys and rats. Taken together these findings present strong evidence for an organizational effect of testicular androgens on the tendency of an animal to engage in playfighting. In contrast to this developmental effect, there is, apparently, no activational influence of circulating testosterone on play-fighting. The expression of ma1e;typical levels of play-fighting is dependent on the presence of androgens during a critical period for neural differentiation but not during the period when the behavior is actually observed. Although this pattern of androgen effects is rare (usually behaviors that are influenced by testicular steroids during a perinatal period are also activated by these hormones), it is not surprising when one considers the changes in androgen levels that normally take place between the time of birth and that of puberty. Thus, Resko, Feder, and Goy (1968) found that while androgen titers are high at the time of birth in the Norway rat, there begins a period of quiescence by about days 8 to 10 that is uninterrupted until just prior to puberty. The sex difference in play-fighting is, of course, observed well before puberty. It is unlikely, then, that the expression of play-fighting could be dependent on the presence of androgens since androgen levels are very low during the prepubertal period. Organizational effects, however, are entirely plausible since androgen levels are reasonably high for at least the first week after birth [note that Beatty et a / . (198 I ) found that castration on days 1 or 6, but not later, decreased the frequency of play-fighting in male pups]. Even though perinatal androgens influence the social play of both rhesus monkeys and Norway rats, in neither species does there appear to be any suppressive effects of ovarian hormones on females. In the rhesus monkey, females ovariectomized on the day of birth play-fought as often as did intact females (Goy, 1970). Also in the Norway rat, day 1 ovariectoniy did not influence the frequency of play-fighting of female pups (Meaney & Stewart, 1981b). Thus, the sex differences in the play-fighting of these species is apparently not due to any obvious influence of ovarian hormones on females. Birke and Sadler (1983) have reported that neonatal exposure to the synthetic

SOCIAL PLAY

21

progestin medroxyprogesterone decreases play-fighting in general and play-initiation in particular in both male and female rat pups. The mechanism underlying this effect is as yet unclear; progestins act at a variety of androgen-sensitive target sites and in some cases mimic or potentiate the effects of androgens, whereas in other cases they antagonize androgenic effects (see Bardin & Catterall, 1981; Janne, Kontula, Vihko, Feil, & Bardin, 1978). It is interesting, however, that during the neonatal period in the rat, both serum and adrenal progesterone levels are higher in females than in males (Shapiro, Goldman, Bongiovanni, & Marino, 1976). Thus, progesterone may act as an endogenous “antiandrogen,” at least with respect of play-fighting and may serve to promote female-typical play-fighting. Because this sex difference in progesterone levels seems to be due to adrenal rather than ovarian secretions, the absence of an effect of neonatal ovariectomy reported by Meaney and Stewart (198 1b) is not necessarily inconsistent with the findings of Birke and Sadler (1983). At the very least these findings leave open the possibility that the development of female-typical play-fighting is not merely due to the relative absence of androgenic stimulation. This question should be reevaluated in studies that examine play-fighting in greater detail and do rely simply on the frequency with which play-bouts occur. One question that arises concerning testosterone effects is its mechanism of action at the intracellular level (see Fig. 12). Testosterone is a prohormone; that is, once inside a cell, testosterone can be converted into an estrogen (estradiol) through an aromatization pathway or into another androgen form (usually 5adihydrotestosterone) through a Sa-reductase pathway. Both forms of testosterone conversion have been found to occur in the neonatal rat brain (George & Ojeda, 1982; Martini, 1978; McEwen, Lieberburg, Chaptal, & Krey, 1977). Moreover, the neonatal rat brain also contains functional receptors for both androgens and estrogens (Fox, Vito, & Wieland, 1978; Lieberburg, MacLusky, Roy, & McEwen, 1978; Meaney, McGinnis, & McEwen, 1982; Vito, Wieland, & Fox, 1979), an observation supporting the possibility that one or both of these testosterone metabolites might be involved in the sexual differentiation of play-fighting. This question is of particular interest to behavioral endocrinologists in view of the major organizational role attributed to testosterone-derived estradiol in the sexual differentiation of copulatory behavior in the Norway rat (e.g., McEwen et al., 1977). In a broader sense an examination of this issue also allows for a more detailed comparison between the neuroendocrine determinants of play-fighting and those of what might be functionally related behaviors (see later). Given the aforementioned considerations, it is conceivable that the organizational effect of testosterone on play-fighting might be due to ( 1 ) testosteronederived estrogen, (2) testosterone-derived Sa-dihydrotestosterone, or (3) testosterone itself. To examine these possibilities Meaney and Stewart (1981b) compared the frequency of play-fighting of female pups treated on days 1 and 2 with either testosterone, Sa-dihydrotestosterone, or with estradiol to that of intact

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MICHAEL J . MEANEY ET A L .

Cellular membrane

.

Nuclear membrane

Blood stream

..... + + t o new

E 3

plasma binding protein cytoplasmic receptor protein

4

steroid hormone

-

FIG. 12. A current model of steroid hormone action. ( I ) The free steroid (i.e., that not bound to plasma binding proteins) diffuses into the cell (2), where it binds to a cytosolic receptor protein forming an “activated” hormone-receptor complex. (3-4) The hormone-receptor complex is then able to cross the nuclear membrane, where it binds to the chromatin (5) resulting in messenger RNA (mRNA) production. (6) The mRNA diffuses into the cytosol, where it induces the synthesis of new proteins.

male and female pups. The results showed that neither testosterone-treated females nor 5a-dihydrotestosterone-treated females differed from intact males in the frequency with which they engaged in play-fighting. Each of these three groups engaged in more play-fighting than did either estrogen-treated or control females. These results with the Norway rat parallel those previously found with the rhesus monkey. Goy (1978) also found that Sa-dihydrotestosterone as well as testosterone masculinized the play-fighting of female rhesus monkeys. In both the Norway rat and the rhesus monkey, then, the testosterone effect on playfighting is a “true” androgen effect (i.e., it is not mediated by testosteronederived estradiol).

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23

The nature of this androgenic effect has been further characterized in studies examining the role of the intracellular androgen-receptor system in the brain. Within various brain regions of the neonatal rat-notably the hypothalamus, septum, preoptic region, and amygdala-there exist intracellular receptor proteins that bind specifically and with high affinity to testosterone and Sa-dihydrotestosterone (Lieberburg, MacClusky, & McEwen, 1980; Meaney, McGinnis, Aitken, & McEwen, 1984a). The apparent mechanism of hormonereceptor interaction is summarized in Fig. 12. The importance of the androgenreceptor system in the sexual differentiation of play-fighting was first indicated by the finding that Flutamide, which seems to block the translocation of androgen receptors into the nuclear compartment (see Meaney et a l . , 1983), prevents the masculinization of play-fighting (Meaney et ul., 1983). This was confirmed in a study examining play-fighting in male rat pups bearing the Xlinked Tfm mutation. Tfm rats exhibit a profound deficiency in neural, androgen receptors (McGinnis, Davis, Meaney, Singer, & McEwen, 1983; Naess, Hang, Attramadal, Aakvaag, Hanson, & French, 1976). Meaney et ul. (1983) found that Tfm males engaged in play-fighting significantly less frequently than did normal males and no more frequently than females. These findings suggest that the effects of testosterone or Sa-dihydrotestosterone on the development of maletypical play-fighting are mediated by the androgen-receptor system. Moreover, recent data (cited later in the text) suggest that the brain is the critical target site for this androgenic effect. 3. Adrenal Hormones

The influence of neonatal hormones on social play is not limited to androgens. Meaney, Stewart, and Beatty (1982) have found that glucocorticoids administered neonatally also influence the development of play-fighting in the Norway rat and that the effect is sex dependent. Prepubertal male rats that were injected either on days 1 and 2 or on days 3 and 4 with corticosterone engaged in less play-fighting than did control males (dexamethasone, a synthetic glucocorticoid, produced a comparable effect). Males treated with corticosterone on days 9 and 10 were unaffected. Thus, as with the androgen effect, glucocorticoids are effective only within the first week of life. Corticosterone treatment of females at any one of these ages did not affect the frequency with which they engaged in playfighting. Thus, the effect was both time dependent and sex dependent. Also, as was the case with testosterone, corticosterone has no activational, or “deactivational,” effect on the play-fighting of male pups. Males injected with corticosterone daily between day 26 and day 40 play-fought as frequently as did control males (Meaney & Stewart, 1983). There currently exists evidence for the idea that this organizational, glucocorticoid effect on play-fighting is mediated by intracellular glucocorticoid receptor proteins (see Fig. 12) and that it is not due to any interference by adrenal

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hormones with androgen secretion or with the interaction between androgens and their receptors, First, glucocorticoids do not affect circulating testosterone levels in neonatal rats (Meaney et a l . , 1982). Second, corticosterone, unlike the androgen receptor-blocker Flutamide, does not block the translocation of androgen receptors into the cell nucleus in testosterone-primed rats (Meaney, unpublished). Moreover, there are glucocorticoid receptors in the neonatal rat brain (within the hippocampus, septum, and amygdala) that bind with high affinity and specificity to both corticosterone and dexamethasone (Meaney, Sapolsky, & McEwen, 1985). Thus, there exists the intracellular mechanisms by which these adrenal hormones might independently exert their effects on the neural circuitry that underlies play-fighting.

4 . Neural Basis of Play-Fighting Play-fighting represents one of the few behaviors that is organized by early hormone exposure but the expression of which is independent of later activational effects of hormones. What probably occurs is that the exposure to high levels of androgens during a period of neural differentiation promotes the growth of a sex-specific neural circuitry and that this circuitry in turn mediates the sex difference in play-fighting that is observed in juvenile animals. Our still preliminary investigation into the neural system that underlies play-fighting has revealed evidence that supports this hypothesis. Meaney, Dodge, and Beatty (1981) found a sex-dependent effect of amygdaloid lesions on the play-fighting of juvenile Norway rats. Amygdaloid lesions made on days 21 or 22 reduced the levels of play-fighting in male pups to those of normal females. The same lesions had no effect on female pups. This finding suggests that an androgen-related sex difference in some portion of the amygdaloid complex might, in part at least, mediate the sex difference that is observed in the play-fighting ofjuvenile Norway rats. Because the amygdala is a target site for both testosterone and 5a-dihydrotestosterone, it is possible that androgens might act directly on this limbic region to masculinize play-fighting. Meaney and McEwen ( 1984) examined this question by studying the play-fighting of females that received bilaterate implants of testosterone-bearing cannulae ( 1 :5/testosterone:cholesterol) in the amygdala between day 1 and day 5 of life (the cannulae were removed on day 5). Testosterone-implanted females actually engaged in somewhat more play-fighting than did male pups and, of course, substantially more than did control females who received cholesterol implants. This finding further suggests that the amygdala is a critical target site for the androgenic effect on play-fighting. At this point it is worth considering what occurs at the cellular level. As outlined in Fig. 12, the concentration of androgen receptors in the nuclear compartment of the cell is a function of the free, plasma androgen levels to which the cell is exposed as well as of the concentration of androgen receptors available in

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the cytoplasm. There do not appear to be sex differences in cytosolic androgen receptor concentrations in the amygdala during the first week of life (Meaney et a / ., 1984a); however, circulating testosterone levels are higher in males than in females during this period (Resko et al., 1968; Weisz & Ward, 1979). This sex difference in testosterone levels provides a mechanism whereby there would be greater androgen receptor occupancy in males than in females. Indeed we (Meaney et a / . . 1982, 1984a) have recently found that during the first week of life androgen receptor occupancy in nuclear fractions prepared from various brain regions is higher in male pups than in female pups. This sex difference in nuclear androgen receptor concentrations was greatest in the amgydala. These data provide more direct support for the idea that under the conditions of normal development, androgenic action within the amygdala is greater in males than in females and thus that there exists a neuroendocrine mechanism by which an anatomical/neurochemical sex difference might develop within this limbic region. In this regard it is interesting to note that there is evidence of hormonedependent sex differences in amygdaloid morphology. Staudt and Dorner (1976) have found a sex difference in the nuclear cell size in the central and medial portions of the amygdala. Dyer, MacLeod, and Ellendorf (1976) found a sex difference in the efferent projections of the corticomedial nucleus of the amygdala. Nishizuka and Arai (1981) found a greater number of shaft synapses (i.e., synapses on the shafts of dendrites) in cells of the medial amygdaloid nucleus of male rats. Significantly, all of these sex differences in the structure of the amygdala were shown to depend on the presence of androgen during the neonatal period. What is not clear is whether changes in the anatomy of the developing amygdala are produced by a direct action of androgens (presumably involving an androgen receptor mechanism) or depend upon the aromatization of testosterone to estradiol. Estradiol is known to stimulate the growth of neural processes (neurites) in cultures of hypothalamic tissue from the brains of neonatal mice (Toran-Allerand, 1976) and may be responsible for the differentiation of the sexually dimorphic nucleus in the preoptic area of the rat brain recently described by Gorski, Gordon, Shyrne, and Southam (1978). With this caveat in mind it is still tempting to speculate that androgen-dependent changes in the development of the amygdala may be responsible, in part, for the sex differences in playfighting. Because the amygdala in the neonatal rat also contains receptors for corticosterone (e.g., Meaney et al., 1984a), this structure may also be involved in the sex-dependent effects of neonatal exposure to corticosterone on playfighting. It is possible, then, that androgens and glucocorticoids might act at the same neural site(s) to influence the development of play-fighting. Certainly this idea is consistent with the findings that the temporal boundary for the androgen effect on play-fighting coincides with that for glucocorticoids (i.e., the first week of life). Here again, it is important to note that within the amygdala there exists both

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androgen and glucocorticoid receptors. With these considerations in mind, it is interesting to note the effects of these steroids on peripheral tissue. In thymic lymphocytes, glucocorticoids stimulate the degradation of RNA and cell death (Cidlowski, 1982), and this action is antagonized by androgens (Sasson & Mayer, 1981). In several tissue preparations, androgens have been shown to stimulate RNA synthesis (see Fig. 12). In skeletal muscle, androgens have protein anabolic effects and glucocorticoids protein catabolic effects (e.g., Mayer & Rosen, 1975), and Dahlberg, Snochowski, and Gustafsson (1981) have reported evidence for the idea that these hormonal effects on muscle tissue are mediated by androgen and glucocorticoid receptors. Although we know of no comparable evidence that implicates a similar role for androgens in the CNS, there exist considerable data suggesting that glucocorticoids exert a catabolic effect on the CNS during the neonatal period (e.g., Cotterrell, Balazs, & Johnson, 1972; Balazs & Cotterrell, 1972; Weichsel, 1974). It is, therefore, possible that within particular limbic regions, such as the amygdala (specifically the corticomedial region of the amygdala, which contains both androgen and glucocorticoid receptors), endogenously elevated glucocorticoids may antagonize the cellular actions of the higher, circulating androgen levels in neonatal males and, thus, block the masculinization of those neural structures that underlie the sex differences in play-fighting. This hypothesis forms the basis of some of our current work on this question. Additional studies on the effects of brain lesions made shortly after weaning have revealed qualitatively similar influences on the play of males and females. Septa1 lesions increase play-fighting in both sexes (Beatty, Dodge, Traylor, Donegan, & Godding, 1982) while extensive damage to the medial preopticanterior hypothalamus has the opposite effect (Dodge, 198 1). More restricted lesions, confined to the medial preoptic area, did not affect play-fighting in young male rats (Leedy, Vela, Popolow, & Gerall, 1980) or in rhesus monkeys (Goy, Kemnitz, Slimp, Irving, & Neff, 1979). Preliminary studies indicate that ventromedial hypothalamic lesions do not affect play-fighting in juvenile rats of either sex. On the basis of these and other findings, it is possible to dissociate the endocrine influences on play-fighting from those on other forms of social behavior. Joslyn (1973), for example, found that while juvenile female rhesus monkeys injected regularly with 2 mg of testosterone exhibited a dramatic increase in social rank, eventually dominating their male peers, they showed no increase in the frequency with which they engaged in play-fighting. Moreover, while the potential of an animal to engage in intraspecies aggression has been related to concurrent levels of both androgens (e.g., Beeman, 1947; Brain & Nowell, 1969; Rose, Gordon, & Bernstein, 1972) and glucocorticoids (see Leshner, 1975), play-fighting occurs independent of the circulating levels of

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these hormones (Meaney & Stewart, 1983). Meaney et 01. (1982) found that while the neonatal exposure of male rats to corticosterone decreased the frequency with which they engaged in play-fighting, it did not affect the potential of the animals to exhibit either male or female copulatory behavior. Meaney and Stewart (1983) found that although testosterone treatment of juveniles resulted in precocious male copulatory behavior (cf. Bauni, 1972), i t did not affect playfighting. Although the study of the neurology of play is just beginning, it is already apparent that the neural control of play is different from that of sexual and aggressive behavior. This is probably not surprising since the endocrine influences are different as well. Thus, the neuroendocrine factors that influence the occurrence of play-fighting can be dissociated from those that influence other forms of social behavior. That is an important point when one considers the potential developmental consequence of play-fighting, for it allows us to discount the possibility that a relationship between play-fighting and, say, later success in adult agonistic encounters (see Taylor, 1980) is simply due to the fact the two behaviors share the same neuroendocrine mechanisms. Play-fighting, then, may be considered as an independent behavioral system and not merely as the immature version of some form of adult social behavior.

5 . Hortnonul Influences on Play-Mothering The question of hormonal influences on play-mothering has been examined in humans and the data here are derived from work with clinical populations. In CAH children, girls have been found to engage in less mothering behavior, such 1968; as doll play and baby care, than do normal controls (Ehrhardt et d., Ehrhardt & Baker, 1974). It will be recalled that these children were exposed to high levels of adrenal androgens. Again, it is interesting to note that the CAH children in this study were reared as females and developed a female gender identity (Ehrhardt & Baker, 1974). Ehrhardt and Money (1967) found that girls whose mothers were treated with “masculinizing progestogens” (these are progestogens that have androgenic as well as progestational actions) showed less doll play than did normal controls. In both of these studies, then, the perinatal exposure to androgens or to androgen-like substances decreased the maternallike behaviors of young girls. It is important to note that in both of these studies the “androgenic” treatment was confined to the perinatal period. These studies, then, appear to offer evidence for an organizational effect of steroid hormones on play-mothering in children. Similarly, genetic males with the androgen-insensitivity syndrome (i.e., genetic males that are functionally deprived of androgen due to insensitivity to their own androgens, whose external genitalia are female, and who are thus raised as girls) have been found to engage in doll play more frequently than control females and to exhibit a greater interest in infant care

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(Money, Ehrhardt, & Masica, 1968). In the genetic males, this insensitivity to androgens appears to be related to female patterns of responsiveness to infants or infant-like objects. Although this question has not been directly examined in other species, it is noteworthy that in both the vervet monkey (Gartlan, 1968; Lancaster, 1971) and the rhesus monkey (Chamove et al., 1967) play-mothering has been observed in females long before puberty. Since the prepubertal period is characterized by a general gonadal quiescence, it is unlikely that the behavior is activated by gonadal hormones. The human data do make it appear that sex differences in playmothering, like those in play-fighting, are associated with the perinatal exposure to the sex steroids. Furthermore, it would appear that as is the case with playfighting, there are organizational effects, but no activational ones.

INFLUENCESI N SOCIAL PLAY D. SOCIAL The argument presented in the preceding section stressed the role of perinatal hormones in determining sex differences in social play. This should not be interpreted to mean that sex differences in social play are the inevitable consequence of early hormonal events. Rather, it appears that the adults (often, but not exclusively the mother), through the differential treatment of male and female infants, also promote the pattern of sex differences that was outlined earlier. Certainly, to those who have embraced social learning theories as explanations for sex differences in human social behavior, this is not a revelation. What is interesting though is that analogous social processes also occur in nonhuman species. In humans, mothers have been found to behave differently toward their male and female offspring, even early in infancy (Goldberg & Lewis, 1969; Levine, Fishman, & Kagan, 1967; Moss, 1967; Thomas, Leiderman, & Olson, 1972). For instance, mothers vocalize and smile more to their female infants than to their male infants. Fagot (1974) observed that, among children of a similar age, mothers left their sons to play on their own more often than their daughters. Evidence of differential treatment by mothers of male and female infants has also been observed in several other species. Even shortly after birth mothers behave differently toward male and female offspring. In the Norway rat, the mothers spend more time licking the anogenital region of their male pups than of their female pups (Moore, 1981; Moore & Morelli, 1979). Similarily, in bonnet macaques (Simonds, 1974), the mother as well as neighboring adult females exhibit an intense interest in the genitalia of newborn, male infants. In several primate species, as the infants grow older, this gender-dependent maternal behavior takes on a form that more directly contributes to sex differences in the juveniles’ social interactions. In the rhesus monkey, Mitchell ( I 968) found that mothers of male infants withdrew from, played with, and presented to their

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infants more often than did mothers of females. Mothers of females protected and restrained their infants more than did mothers of males. Similarly, in both the Japanese (Itani, 1959) and pigtail monkey (Jensen, Bobbitt, & Gordon, 1967), mothers have been observed to withdraw from male infants earlier and more often than from female infants. Also in pigtail monkeys, mothers bite male infants more frequently than they do female infants, and in general there is a greater mutual antagonism in mother-male infant pairs than in mother-female infant pairs (Jensen, 1966). In the rhesus monkey, mothers reject their sons more frequently than their daughters (e.g., Hinde & Spencer-Booth, 1967; White & Hinde, 1975). Given these findings, it is not surprising that there is a sex difference in both the degree to which infants become independent of their mother and the age at which they achieve this independence. In chimpanzees (Nicolson, 1977), pigtail monkeys (Erwin, Anderson, & Bunger, 1975; Jensen et al., 1967), Japanese monkeys (Itani, 1959), bonnet monkeys (Simonds, 1974), and rhesus monkeys (Hinde, 1971), males become independent of their mothers sooner than do females. In contrast, in many species females tend to remain in proximity with their mothers for long periods after sexual maturity (Kummer, 1968; Pusey, 1978; Rowell, Din, & Omar, 1968). In these species, then, mothers seem to promote the independence of male infants and to remain in closer contact with female infants.2 These differences in maternal behavior toward male and female offspring appear to be related to sex differences in the behavior of the young. Thus, Mitchell (1968) found that male rhesus monkeys bit their mothers more often than did female infants (seemingly a reasonable way to “assure” one’s independence). In chimpanzees, male infants have also been observed to behave more aggressively toward their mother than do female infants (Clark, 1977). In the Norway rat, juvenile males attempt to mount and to play-fight with their mother more so than do females. In contrast, females groom their mother more than do males (Meaney & Stewart, 1981a). Perhaps not surprisingly, in this rodent 21n their cross-cultural studies, the Whitings and their colleagues have reported that mothers are much more likely to delegate their work to their daughters than to their sons (see Ember, 1973). and one common explanation for this finding is simply that the daughters are, generally, close by. Indeed, in the African cultures studied, young girls do remain closer to the home than do the males (e.g., Draper, 1973; Ember, 1973; Munroe & Munroe, 1971; Nerlove, Munroe, & Munroe, 1971). Thus, girls engage more often in household chores and infant-care than do males (e.g., Ember, 1973; Whiting & Edwards, 1973). The process whereby daughters remain in close proximity to their mothers (seemingly a function of both the daughter’s seeking proximity to the mother and the mother’s restraint on her daughter) facilitates the socialization of the daughter into the female role. Likewise the boys’ movement away from the home leads to increased contact with male peers (see Whiting & Edwards, 1973; Clark P? a / . . 1969) and, eventually, with adult males. This male-peer contact may be enhanced by a preference for similar activities, such as play-fighting. This male-male contact, then, would facilitate the socialization of the sons into the male role. In the following section we argue that the primary function of social play is to facilitate this acculrururion process.

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species as well, female offspring remain with their mother longer than do male offspring (Calhoun, 1962). In humans also there are sex differences in the behavior of infants that may serve to elicit differential maternal behavior (see Bell, 1971; Harper, 1971, for reviews). Newborn females exhibit higher rates of reflexive smiling than do newborn males (Freedman, 1974). In contrast, male infants have been found to be more irritable than female infants (Moss, 1974). Observations of mother-child dyads in natural settings have shown that young boys (12-36 months) left their mothers more often than did young girls (Anderson, 1972; Ley & Koepke, 1982). Considered in this way the behavior of both the mother and the infant can be seen as contributing to sex differences in mother-infant interactions. Male and female infants also elicit differential behavior from adults other than their mother. In rhesus monkeys (Breuggeman, 1964), stumptail monkeys (Estrada, 1978), and baboons (Rowell et a/., 1968), there is evidence that adult males exhibit more infant care and general interest toward male infants than toward female infants. In addition, adult male rhesus monkeys have also been observed to initiate play-fighting with male infants more often than with female infants (Hinde & Spencer-Booth, 1967; Redican & Mitchell, 1974). Thus, Redican (1976) observed that, among wild-born rhesus monkeys, “mothers interacted more positively with female infants and adult males with male infants.” In studies of humans, Tasch (1952) and Kotelchuck (1976) found that fathers engaged more often in play with their sons than with their daughters. Lamb (1977) and Rebelsky and Hanks (1971) reported that fathers vocalized more with their sons than with their daughters. In general, fathers seem to spend more time with their sons than with their daughters (cf. Parke & Suomi, 1981). Again the role of the infant needs to be considered in the context of these findings. Mitchell (1968) has reported that male rhesus infants elicit more play-fighting from adults than d o female infants. Thus, in these species the interaction between adult males and male infants would seem to enhance the play-fighting behavior of male infants. Immature males and females also differ in the behavior that they direct toward the adults in their group, other than their mother. One intriguing example of this has been reported by Seyfarth, Cheney, and Hinde (1978) in free-ranging baboons. They observed that while both immature males and females directed a considerable amount of grooming toward adult females, the young females tended to groom adult females that ranked higher than their mother and were most likely to groom lactating mothers. This attention to lactating mothers served to bring the immature female into contact with the infants and provided an opportunity for infant care. Also, it afforded the opportunity for amicable contact with higher-ranking adult females. This type of social interaction might well benefit the subadult female, considering that in most species of old world monkeys females tend to remain in their natal group (Seyfarth et id., 1978).

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These sex differences in adult-infant interactions appear to promote sex differences in the social experiences of the young. Field studies of several primate species (e.g., DeVore, 1963; Jay, 1963) have confirmed that females tend to spend more time with their mothers and other adult females, whereas males spend more time at the periphery of the group where they form same-sexed play groups (see Clark, Wyon, & Richards, 1969, for a similar finding in humans). This pattern would result in a greater exposure of juvenile females to mothers and their infants (thus providing the opportunity for play-mothering) and males would experience greater contact with same-sexed peers (providing a greater opportunity for play-fighting and greater contact with other subadult and adult males). This behavior would enhance the familiarity between adult and juvenile males and thus facilitate the integration of the juveniles into the group. As Simonds (1974) writes, “Females establish their network primarily through grooming and remain closely associated with their mother. Males rely more heavily on the play group, which includes participating sub-adult and adult males” (p. 15). Thus, the early social interactions of male infants seem to bring them into contact with adult males, whereas those of female infants keep them in contact with their own mothers and other adult females. These findings suggest that sex differences in the social behavior of infants and juveniles emerge, in part, through the social interactions with the mother and other adults. Direct evidence for the contribution of the mother to the socialization of her offspring can be seen in findings of Mitchell, Ruppenthal, Raymond, and Harlow (1966). Primiparous rhesus mothers restrained male infants as much or more so than female infants, thus retarding the independence of their male young. Sons of primiparous mothers engaged in very little play-fighting and “cooed” frequently (“cooing” is generally more common in female infants). The male offspring of these overprotective mothers were, then, more female-like in their early social behavior than were the infants of more experienced mothers. The influence of adults is also seen in a study of Milch and Missakian-Quinn (1977) with children that were reared with minimal contact with adults (peer reared). The absence of adults was associated with a decrease in the sex differences in play roles and in assertiveness. Suomi (cited in Parke & Suomi, 1981) has also addressed this issue based on some preliminary findings which suggested that sex differences in the social behavior of juvenile rhesus monkeys are enhanced by the presence of adult males.

E.

SUMMARY

As discussed earlier, sex differences in the social play (and thus in the social experiences) of juveniles have been found to be influenced by the actions of perinatal hormones. The nature of this influence appears to be in organizing the circuitry of the CNS such that animals are predisposed to respond to a particular

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stimulus in a certain way (see Phoenix et al., 1959). The result of this early hormonal experience is that males and females seem to differ in their preferred forms of social play. The study by Mitchell et al. (1966) with primiparous mothers suggest that these sex differences in social play are not the inevitable consequence of hormonal events. Note, however, that in juveniles reared in peer groups sex differences in play-fighting have been observed (Goldfoot & Wallen, 1978; Goy & Phoenix, 1971; Meaney & Stewart, 1981b). Thus, while the behavior of the mother and other adults may to some extent override the influence of early hormonal events, their influence is not absolutely necessary for the development of sex differences in social play. In the normal socialization process, however, both the influence of the mother and other adults, and of early hormonal events seem to contribute in the same direction to the pattern of sex differences in social play described earlier.

111.

THEFUNCTION OF SOCIAL PLAY

Certainly one of the most conspicuous features of social play is the apparent lack of any immediate consequence it holds for the participants. For some, this has actually been considered as a defining feature of play (see Loizos, 1967). What remains puzzling is that young animals devote so much time and energy to behavior of such dubious value. How might the potential for the expression of such a behavior have evolved? The absence of any observable, immediate function for social play has led many researchers to consider the possible developmental consequences of social play. The focus here is on the preparatory function of social play, the suggestion being that social development is somehow facilitated through the experiences afforded during play encounters. Thus, it is argued that in the course of social play, animals learn skills that prepare them for the social life of an adult. This argument suggests an adaptive value for social play and therefore an answer to the question of how play might have evolved. But what of the actual evidence in favor of such a developmental role for social play'? A.

DEVELOPMENTAL SIGNIFICANCE OF SOCIAL PLAY

The strongest evidence for a developmental role for social play is that which has come from the work of Harlow, Mason, and their associates at Wisconsin. This research has involved a social deprivation paradigm in which young rhesus monkeys have been deprived of contact with their mother, peers, or both for varying periods of time. The effects of these procedures have been examined in animals from the infant to the adult stages. The resulting behavioral anomalies (and there are many) have been related to the absence of certain forms of social

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contact. Particularly relevant for the present discussion are the findings of pronounced sociopathology in monkeys deprived of contact, and thus also of play, with peers. While this paradigm has resulted in some truly intriguing findings, its usefulness has been questioned. As Lehrman (1953), Bekoff (l976), and many others have argued, the interpretation of findings from deprivation paradigms is difficult since it is hard to identify exactly what the animal is being deprived of. Certainly an animal deprived of any interaction with peers is an animal without social play (as Suomi & Harlow, 1976, have argued), but it is also an animal without other forms of social contact, including simply the visual, olfactory, auditory, and tactile stimuli associated with another animal. “The problem remains whether it is peer contact or the act of playing that results in normal behavior, and this would be very difficult to test experimentally” (Dolhinow & Bishop, 1970, p. 175). For, as Symons (1974) has stated, when you do allow immature monkeys contact with peers-they play. This problem has shrouded the interpretation of the peer-deprivation findings as definitive evidence for a role for social play in normal social development. With respect to the more general question of whether social play serves a developmental function in the normal socialization process, however, the problems presented here may not necessarily be relevant. These problems refer to the question of identifying the critical factors that contribute directly to the development of social behavior. In addressing this question, the social deprivation studies have failed to identify social play as a critical factor for the reasons cited earlier. It is possible, however, that a factor can indirectly serve to promote social development simply by leading to the experiences that do themselves directly contribute. We argue here that there is evidence for such a role for social play. This argument is based on the assumption that the social deprivation studies have established the importance of peer-peer interaction, albeit without identifying the critical component of these interactions. In most, if not all, of the species listed in Table I, the most predominant form of peer-peer interaction is that of social play. In many species, peer-peer interactions may almost be equated with social play. Considered another way, it is the tendency of young animals to engage in social play that leads to peer-peer contact. Thus, even if it is peer contact and not the act of playing itself that facilitates social development, social play can be seen as being functional in that it enhances the level of peer interactions that an animal experiences. An analogous argument could be made for the role of exploration in object learning. The tendency to explore may not contribute directly to object learning, but it does indirectly, by bringing an animal into contact with salient objects. In a similar way social play can be considered as serving a role in social learning. The question, then, concerns the function of these early social experiences that occur during social play. If one is concerned with normal social development, then the findings of

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sociopathology in rhesus monkeys deprived of peer contact have established a role for social play in the socialization process. As a conclusion to this arguement, it may be more correct to state that the tendency or the motivation to engage in social play leads to the social interactions that are necessary for normal socialization to occur. It is yet another question as to how these social interactions contribute to social development and what is the critical feature of the interaction.

BETWEEN SEX DIFFERENCES I N ADULTAND B . RELATIONSHIP JUVENILE SOCIALBEHAVIORAND THE NATUREOF THE CONTRIBUTION OF SOCIAL PLAYTO SOCIALDEVELOPMENT

There are two ways in which social play may contribute to social development. The first concerns the function discussed in the previous section. Social play might serve to increase the social interactions between a young animal and significant others. Through this contact an animal might become familiar with the other animals in its group, this we refer to as an acculturation function (see Bekoff, 1976, 1978). The second way that social play may contribute to social development is through the learning of specific motor patterns that are involved in social behavior-a motor-learning function. This motor learning would be a function attributable to the act of playing. In this section we shall consider playmothering and play-fighting in relation to these two possible functions. In addition we also shall examine the relationship between sex differences in social play and sex differences in adult social behavior. If we assume for a moment that the social interactions of juveniles serve some developmental function for adult social behavior, then to the degree that there are sex differences in the adult social behavior of a particular species so too should there be sex differences in the forms of social play that contribute to the development of adult social behavior. Specifically, we might expect that juvenile males would engage more frequently in those forms of social play that contribute to male-typical, adult social behavior and that juvenile females would engage more frequently in those forms of social play that contribute to female-typical, adult social behavior. From a knowledge of the sex differences in adult social behavior, then, we should be able to predict sex differences in juvenile social behavior. There is a corollary to this reasoning that bears directly on our original question of whether there is a function for social play. If play is without any developmental consequence for adult social behavior, then it is most unlikely that there should be any meaningful relationship between sex differences in adult social behavior and sex differences in social play. The existence of such a relationship would argue for a developmental role for social play, since it is improbable that

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any such relationship would exist unless the behaviors were functionally related.3 1. Play-Mothering

Lancaster (1971) and, more recently, Meaney, Stewart, Lozos and Ervin (submitted) have presented some rather clear evidence for a motor-learning function for play-mothering. Lancaster reported that young female vervet monkeys were rather clumsy in their initial efforts to care for an infant. They had difficulty in orienting the infant's body and in getting the infant to cling to them. Often this resulted in the juvenile carrying the infant with one leg while walking along on the remaining three (see Figs. 13 and 14). Soon, however, the juveniles learned how to carry the infant properly and to instill sufficient confidence in the infant that it would cling when the juvenile tried to walk with it. At this stage the juveniles had developed adequate maternal skills such that they could pacify the infant and thus avoid having the mother attempt to retrieve her offspring. Meaney er a / . observed the infant care of juvenile (2-4 years of age) and subadult (5-6 years of age) females in a captive troop of vervet monkeys through two birthing seasons (over a period of 14 months). For the 2 years prior to the study, infants had been removed from the troop. Thus, the first birthing season represented a renewed, or in the case of certain juveniles, a new opportunity for exposure to infants. Over the first birthing season and through the following autumn, these nulliparous females improved in their ability to carry infants to the point that, by the second birthing season they were indistinguishable from multiparous females. Jay (1963) also has reported that in langurs females that had experience with infants were better at keeping infants quiet and were able to hold them for a longer period of time than were inexperienced females. Play-mothering, then, affords the opportunity for juveniles to gain what might be valuable experience in infant care in a relatively benign setting. This may be especially important for primates considering their low reproductive rate (compared with rodents, for example). It would be interesting to examine, across primate species, the relationship between the degree of play-mothering in juveniles and the competency of primiparous mothers. This attraction of juveniles toward infants results not only in interactions with the infants but also in interactions with the mothers of infants. In free-ranging baboons (Cheney, 1978; Seyfarth et al., 1978), Juvenile females are highly attracted toward the infants in the group and, in particular, toward the infants of high-ranking adult females. In the course of these interactions, juveniles spend a considerable amount of time grooming the adult females. Thus, the Juveniles are "Note that we have already dismissed the possibility that this relationship exists simply because the behaviors share a common ncuroendocrine basis (see Section II,C,4).

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FIGS. 13- 14. The juvenile vervet females in our troop are quick to retrievt: and carry an unattended infant (in this sequence the mother, not seen, was about 3-4 m away). The carrying of infants by juveniles is often clumsy, and the juvenile often must support the infant who commonly does not cling to the inexperienced female.

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SOCIAL PLAY

SUMMARY OF EVIDENCE tOR

SEX

TABLE I1 DlbFERENCtS IN PLAY-MOTHERING ACROSSSPtClES Finding

Species studied Hominoidea Humans Cercopithecoidea Rhesus monkey Olive baboon Vervet monkey Barbary ape Ceboidea Squirrel monkey

P > 6

P = 6

Berman ( 1980, for a review) Chamove et ul. (1972) Owens (1975a.b) Gartlan ( 1968); Lancaster (1971) Burton (1965) Baldwin and Baldwin ( 1974)

afforded a form of amicable contact with high-ranking females that would otherwise be unlikely to occur (cf. Weisbard & Goy, 1976). Cheney (1978) has suggested two very plausible functions for this adult-juvenile interaction. First, it may facilitate the integration of the juvenile females into the adult female structure (an acculturation function). Second, the interactions between juvenile females and high-ranking adult females may allow the former to establish a relationship with dominant animals and thereby, through association, derive some of the benefits connected with a high social status. Thus, Cheney (1978) observed that juvenile females interact more often with the infants of highranking mothers than with those of low-ranking mothers. In considering these arguments, it is important to remember that in baboons, as with most old-world monkeys, females rarely migrate from their natal group (Packer, 1975, 1978). The relationship between sex differences in play-mothering and sex differences in the parental behavior of adults appears to be rather clear. Presented in Table I1 are the results of studies with various species in which play-mothering and related infant-directed activities4 have been observed in juveniles. Note that in all but one of these species play-mothering is performed almost exclusively by juvenile females. The exception is found in the juvenile Barbary macaques. It is interesting that in this species the adult male performs a crucial role in the socialization of the infant (Burton, 1972) as well as a considerable amount of infant care (Burton, 1972; Lahiri & Southwick, 1966). In some baboon species 41n some cases the studies listed here (i.e., Cheney, 1978; some of the work in the Berman, 1980, review) refer to reports of attraction toward infants rather than actual parental behavior.

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(chacma and olive) as well there is a certain amount of paternal behaviorhowever, probably much less than in Barbary macaques (Bolwig, 1959; DeVore, 1963). It is interesting to note, then, that Owens (1975a) has observed infant-care behavior in juvenile male olive baboons, although less so than in juvenile females. In the remaining species listed in Table 11, the role of the adult male is far less pronounced and the role of primary infant caretaker is performed by the female. Among humans, for example, there is no known society in which infant care is primarily the role of the male (e.g., Whiting & Whiting, 1974). Rossi (1977) makes the point from cross-cultural studies of foster parenting (e.g., occasioned by the death of the natural mother) that without exception the foster parent is a woman. In summary, then, the juvenile female’s attraction to infants provides for experience in infant care and for social interactions with adult females. These experiences are of dubious value to the juvenile male, since in most species adult males participate in infant care much less than do adult females. An exception, of course, is the adult male Barbary macaque, and thus it is interesting that in this species juvenile males have considerable contact with infants.

2 . Play-Fighting The most obvious hypothesis regarding play-fighting is that it provides a context in which animals may learn the skills necessary to behave appropriately in agonistic encounters. In most socially living, mammalian species the agonistic encounters of adults are characterized by ritualized forms of aggression, including specialized vocalizations, facial expressions, body postures, or attacks to nonvital areas of the body that serve the function of defeating an opponent without causing serious injury. Often the simple expression of threat is sufficient. These behaviors serve as a form of social communication (see Altmann, 1967). Successful adult social behavior, then, can be seen as including the ability to communicate and to interpret the communications of conspecifics. In this regard it is interesting to note that animals reared in the absence of peer contact have been found to behave inappropriately in agonistic conflicts. In particular they seem less able to inhibit the attack of other animals than are socially reared animals (e.g., Mason, 1961, with rhesus monkeys; Lore & Flannelly, 1977, with Norway rats). Some authors have attributed this social-skill deficit to the inadequate learning of the communicative skills used in the course of aggression. In addition, there is direct experimental evidence that peer-deprived rhesus monkeys are unable to interpret the facial expressions of conspecifics (Miller, Caul, & Mirsky, 1967) and that they exhibit inappropriate facial expressions such as staring (threat communication) at a dominant male (Mitchell, 1972). Taken together these findings have led some to propose that one of the learning experiences associated with play-fighting is the development

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of communicative abilities, particularly those that are relevant to agonistic bouts (e.g., Dolhinow, 1971; Jolly, 1972; Mason, 1965). This proposed relationship between play-fighting and adult aggression can be considered both in terms of the motor-learning function and the acculturation function that were described earlier. If play-fighting was a context in which an animal might learn motor skills used in aggression, then we might expect to observe components of these skills, especially communicative skills, in the play-fights of juveniles. A comparison of play-fighting and adult aggression, however, reveals considerable dissimilarity. Symons (1974), for instance, has described how the facial expressions commonly seen in the agonistic encounters of adult rhesus monkeys are not expressed during the play-fighting of young rhesus. Moreover, in the course of playfighting, both participants behave offensively and there is little evidence of the submissive gestures that among adults seem to inhibit the attack of an opponent. The agonistic bouts of older animals usually involve a “threat” display and a “submissive” response such that direct fighting in most species does not frequently occur. As Symons points out, in the play-fighting of rhesus monkeys “there are no gestures of threat or submission” (1974, p. 321). Rather, the facial expressions (van Hoof, 1972; Symons, 1974) and body postures (e.g., Bekoff, 1974) that are observed during play-fighting are unique to the play context. If these gestures serve any communicative function at all it is to signal to another animal that what follows is playful (see Bekoff, 1977) and nor aggressive! It is also improbable that play-fighting serves as a context in which the motor skills that are used in the direct fighting of adult animals are learned. Rather, it appears that in most species these skills emerge early in life in their adult form. Thus, rhesus monkeys begin to exhibit adult-like aggression by about 7 months of age (Symons, 1978). Wolves exhibit intraspecies aggression even as young cubs that is marked by elevated hackles (piloerection) and the “agonisticpucker” expression (facial expression) components of fighting in adults (see Bekoff, 1974; Mech, 1970). In coyotes, cubs actually go through a period of intense fighting prior to the onset of play-fighting (Rekoff, 1974; Ryon, 1979).s In fact the Norway rat is one of the few species in which a juvenile period of play-fighting actually precedes the onset of adult-like aggression. Even in the Norway rat, however, the behavioral components of play-fighting that are used in aggression appear in their adult form even at the very onset of play-fighting

51t is interesting to note that the potential for the expression of both play-fighting and aggression coexist in animals of the same age. This is not unique to subadults. The adult males and/or females in many species play-fight with subadults and in some cases among themselves. At the same time, of course, they are capable of exhibiting aggression. These observations argue against the idea that a motivational system for aggression emerges from a system for play-fighting. It also further supports the notion proffered earlier-that play-fighting represents an independent behavioral system.

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(Meaney & Stewart, 1981a; Poole & Fish, 1976). The same is true in young polecats (Poole, 1966). Taken together these observations argue strongly against a motor-learning role for play-fighting, at least with respect to adult aggression. This appears to be the case with regard to both the communicative and the physical fighting components of aggressive behavior. The final problem associated with a possible relationship between play-fighting and aggression is the apparent inconsistency within species in the degree to which these behaviors are sexually dimorphic. For example, while juvenile male hamsters engage in more play-fighting than do juvenile females (Goldman & Swanson, 1975), among adults the female is far more pugnacious than is the male (Payne & Swanson, 1972). Similar inconsistencies have also been reported in vervet and talapoin monkeys (Raleigh, Flannery, & Ervin, 1979; Wolfheim, 1977). An analogous finding is reported by Blurton-Jones and Konner (1973) in their study of London and !Kung (an African hunter-gatherer group) children. They report that !Kung girls play-fight more frequently than do London girls; however, the English girls show a greater frequency of aggressive acts than do the !Kung girls. Clearly there is no easily identified relationship between sex differences in play-fighting and sex differences in aggression.h Rather, what we have chosen to consider here is the relationship between sex differences in play-fighting and sex differences in dominance-related b e h a v i ~ r s What . ~ we argue here is that on the basis of comparative data such a relationship does exist and that an analysis of the nature of this relationship reveals a possible acculturation function of playfighting. There are two basic sex differences in dominance-related behavior that have been reported across several species. The first is a sex difference in the way in which males and females achieve status or rank within a dominance hierarchy. The factors that Contribute to the status of males are, seemingly, different from those that contribute to the female's status, Among primates this issue has been 6Apart from these empirical considerations, there are also conceptual problems in considering a relationship between sex differences in play-fighting and sex differences in aggression. These problems concern formulating general statements about sex differences in aggression. This seems to be more of a question of sex differences in the conditions that elicit aggression rather than sex differences in thc tendency to engage in aggressive behavior. In the Norway rat, for example, male aggression tends to occur in situations that involve territorial intrusion or the maintenance of withingroup social structure. In females, conspecific aggression is usually associated with the defense of young (see Barnett, 1975). Thus, a sex difference in the overall frequency with which aggression occurs probably reflects the fact that the situations that elicit aggression in males occur more frequently than do those that elicit aggression in females. 'We use the term dominance to refer to a relationship between two or more animals and not to the aggressiveness of an animal (cf. Hinde, 1974). In this sense the term is best considered as reflecting the social structure of a group and the relationship bctween the animals in the groups.

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studied in rhesus and Japanese macaques (Kawai, 1958; Loy, 1975; Sade, 1967) and in the yellow baboon (Papio cyrzocephalus; Lee & Oliver, 1979). In each of these species, prepubertal animals, regardless of gender, rank just below their mothers (i.e., “dependent rank,” see Kawai, 1958). Females maintain this rank as adults. Accordingly, females defeat other females that rank below their mothers, including the daughters of lower-ranking females. These relationships tend to remain stable (e.g., Owens, 1975b) although some changes may occur through affiliative behaviors such as social grooming (Rowell, 1966). In contrast, once males are sexually mature they achieve a rank that is independent of that of their mother. In males, the ultimate rank achieved is usually associated with age/size and success in direct confrontation with other males (i.e., “basic rank,” see Kawai, 1958). Thus, in the rhesus monkey, for example, only males establish dominance through physical aggression (Angermeir, Phelps, Murray, & Howanstine, 1968).8 A relationship between the rank of a mother and that of her daughter has also been reported in Norway rats (Calhoun, 1962). In this species, daughters inherit nesting sites (a resource, that at least in fixed colonies, is dependent on rank) from their mothers. In the Norway rat, there is no evidence of a relationship between the rank of a mother and that of her male offspring. Another factor that in some species has been found to contribute to the dominance status of females is that of “reproductive value” (Hrdy & Hrdy, 1976). In hanuman langurs, reproductive value declines with age, thus younger adult females are dominant over older females. In the male, however, younger males usually defer to older males and may be peripheralized (Mohnot, 1978; a reasonably common pattern among males of many species, both primate and nonprimate). Thus, at least in the hanuman langur, the relationship between age and dominance status is qualitatively different for males and females. Although common, this pattern of sex differences in the achievement of dominance status is not universal. The best-studied exceptions are the canids. In wolf packs, usually only the alpha female gives birth to a litter (Mech, 1970; Rabb, Woolpy, & Ginsburg, 1967). Hence, all the cubs within a pack share the same matrilineal association. In wolves, both males and females achieve dominance status through agonistic encounters with siblings. The same appears to be true, at least for the strains that have been studied, in the domestic dog (Scott & Fuller, 1965). Among coyotes, the dominance hierarchies of females are characterized by higher levels of aggression than are those of males (Ryon, 1979). Thus, in these canid species there do not appear to be sex differences in the manner in which animals achieve dominance status. It is interesting to note that in these species there are no sex differences in play8Whiting and Edwards (1973). in their cross-cultural studies on socialization, have described a similar sex difference among children in the achievement of dominance.

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fighting (see Table I). It appears, then, that the presence or absence of sex differences in play-fighting may be predicted from a knowledge of how males and females achieve dominance status. The second sex difference in dominance-related behavior concerns the function of dominance relationships in general. Loy (1973, on the basis of longitudinal studies with rhesus and Japanese monkeys, has argued that dominance relations have the important function of providing for an “orderly integration of new individuals” into the group. The problem of integrating into a group as well as the cost for males of not belonging to a group (we refer, here, only to mixed-sex groups) seems to be different from what it is for females. In many species, males are often peripheralized or dispersed from the natal group (Dittus, 1975; Drickamer & Vessey, 1973; Sade, 1980; Packer, 1973, whereas female dispersion from the natal group is rare (Dittus, 1975; Packer, 1975). Moreover, the integration of females into a group seems, by existing accounts, to be less difficult than the integration of a new male (Packer, 1978). In some species, such as hamadryas baboons (Kummer, 1968), females may actually be “kidnapped” into groups. Since reproductive success in socially living mammals is usually dependent on membership in a mixed-sex group, group integration becomes a problem central to the overall fitness of a male. Again an exception to this general pattern can be found in a canid species. In wolf packs, dispersion from the natal group can occur in both males and females (e.g., Mech, 1970). In addition, the integration into a pack appears to be no less problematic for females than it is for males. Females can be peripheralized by other females (e.g., Rabb, Ginsburg, & Andrews, 1962). This is no doubt related to the intense reproductive competition and suppression among adult female wolves (Rabb et a / . , 1967). Again, it is interesting to note that in this species there are no sex differences in play-fighting. The hypothesis that emerges here is that sex differences in play-fighting may be related to sex differences in both the dispersion from the natal group and the integration into either the natal group or another unit.y While the comparative data on species in which there are no sex differences in group integration are limited, there are other data that address the issue of a relationship between playfighting and group integration. Simonds (1977) has reported that in bonnet monkeys young males typically join play groups where they experience substantial contact with other subadult males as well as with the dominant males in the group. In these troops the integration of subadult males into the existing dominance hierarchy begins from the time the males join the play group. Thus, by the time the males are sexually mature they are already recognized and treated as 9There is a somewhat of a tautology involved in distinguishing these two factors since the difficulty of integrating into the natal group may be due to pressure on an animal to disperse from that group.

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members of the social structure of the group. Simonds reports that in one bonnet troop (the “Moyar River” troop) this pattern of male-male contact is absent. Interestingly, in this troop young males leave the group. Although this may be an isolated observation, it serves to underscore the importance of male-male interaction. The importance of social contact with dominant males for subadult males is further emphasized by the recent findings of Harcourt and Stewart (1981) on gorillas. They found that some young males emigrated and others remained in their natal group. Their data suggest that the males remaining in the group are those that as juveniles had very close contact with the dominant male, and they go on to suggest that this close relationship may predispose the young male to remain in the group. Comparative data also suggest a relationship between early social interactions and later integration into a group. Altmann (1963) found that elk (Cer.vi4s cunuclerisis nelsoni) young played with other calves, yearlings, and cows, whereas moose (Alces ulces strussi) young rarely engaged in social play. At about 3 to 4 weeks of age, elk young are integrated into the herd. Moose calves, in contrast, gain only limited integration. Bekoff (1977) has observed that social play in canids appears to be related to the social structure of the species. Thus, in the red fox (Vulpes,fulvu; a solitary-living species), social play is less frequent than in the semisolitary coyote. In turn, social play is less frequent in coyotes than in the highly social wolf. The data presented here suggest that sex differences in social play are related to sex differences in both the degree of difficulty in integrating into a social structure and in achieving status within that structure. Although these data argue for a relationship between play-fighting and dominance-related behavior, the nature of this relationship remains obscurc. One feature of the contact derived from play-fighting, however, may simply be to familiarize the participants with one another (cf. Bekoff, 1978). The significance of this can best be appreciated by considering the response of the animals in a group to an unfamiliar conspecific. In this situation the dominant animals in the group usually behave aggressively toward the intruder (Barnett, 1958; Bernstein, 1964; among others). However, in most cases this is only so for male intruders. In the Norway rat, for instance, female intruders are normally accepted into the group (Barnett, 1958). Thus, the cost of not being familiar to the members of a group may be greater for males (which, of course, refers to one original claim about sex differences in group integration). One feature of dominance hierarchies is that they tend to occur within, and not between, sexes. Although there are examples of cross-sex dominance, in most cases the status of an animal within a particular group is dependent on its relations with others of the same sex. Thus, if play-fighting is a behavior that is related to dominance activity, then we might expect animals to play-fight more often with peers of the same sex than with peers of the opposite sex. Indeed, such

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same-sex, play-partner preferences have been reported in several species. In children (Clark e t a / ., 1969), bonnet monkeys (Simonds, 1974), rhesus monkeys (Ruppenthal, Harlow, Eisele, Harlow, & Suomi, 1974; Suomi, 1977), olive baboons (Owens, 1975a), and Norway rats (Meaney & Stewart, 1981a), juvenile males initiate and become involved in play-fights more often with males than with females.'O In contrast, there is evidence to suggest that females do not exhibit play-partner preferences either for males or for other females (Meaney & Stewart, 1981a; Ruppenthal el ul., 1974; Owens, 1975a). These findings suggest that play-fighting may be related to dominance-behavior in males more than in females. In females, soical contact with same-sex peers may be gained through grooming networks (see Simonds, 1977) rather than through play-fighting. In this context it is interesting that social grooming has been reported to occur more often in juvenile females than in juvenile males (e.g., Meaney & Stewart, 1981a; Simonds, 1974, 1977). C.

SEXDIFFERENCES IN

THE

RESPONSETO SOCIAL DEPRIVATION

Another, perhaps, more general, context in which to consider the question of sex differences in social play is that of the rather basic function of play addressed at the beginning of this section, that of enhancing the social contact an animal experiences. This function of play has been analyzed in social deprivation studies with rhesus monkeys. Sackett (1974) has shown that the effects of socially isolated rearing on the eventual social development of males are far more pronounced than on that of females. Taken together, the findings outlined below suggest that social contact may be more important in the social development of males than in that of females. While the sexual behavior of male and female rhesus monkeys reared in isolation is deficient compared to that of controls, females are less affected than are males. Sackett (1974) reports that, in repeated testing, 30% of socially isolated females eventually exhibited species- and gender-typical copulatory behavior, and 20% of the sessions resulted in the insemination of the female. In contrast, not one of the socially isolated males copulated. In tests of affiliative behavior with feral monkeys, both male and female isolates were found to display extreme social fear and to be hyperaggressive, Again, however, the male isolates were significantly more antisocial than were the female isolates (Pratt, cited in Sackett, 1974). This pattern of results was also observed in tests for exploratory behavior and for autoaggression. Finally, it is interesting to note the results of a study examining the survival 'OThis play-partner preference of males for other males is probably not simply due to a preference for a partner of the same size or strength. In Norway rat pups, males and females do not differ in body size until after puberty. Play-partner preferences, however, are observed well before puberty.

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ability of differentially reared male and female monkeys under free-ranging conditions (Sackett, 1974). These results are interesting not only within the present context but also in relation to the arguments made in the preceding section. Of the four female isolates that were released, two survived. One female joined a small group and remained an accepted group member despite exhibiting many of the behavioral anomalies associated with isolated rearing (e.g., selfclasping, rocking, stereotyped locomotor activities). All five of the socially reared females survived. Two of the three socially reared males survived, one actually becoming a dominant male within a native group. None of the three isolation-reared males survived, and it is implied that they were attacked by resident males. First, it is noteworthy that a greater proportion of females, and in particular isolation-reared females, survived than did males. The results from laboratory studies certainly suggest that the social skills of the female isolates are, by comparison, better than those of male isolates. These results, however, are also consistent with the notion that the integration of males into existing social groups is more difficult than is that of females. The thrust of the studies presented by Sackett (1974) is simply that males are more affected by the absence of social contact than are females. Thus, sex differences in the frequency of play-fighting, certainly a contact form of play, may be related to the relatively greater importance for social contact in the social development of males compared to females." In turn, recall that the argument presented in the preceding section stressed the importance of early social contact in males based on what we speculated to be a more arduous integration process than that for females. D.

POSSIBILITY OF IMMEDIATE CONSEQUENCE OF SO C I A L PLA Y

As mentioned earlier one of the features that is presumed to be basic to social play is that it is of little immediate value. Several researchers (e.g., Fagen, 1981) have stressed that social play may involve a cost for the participants (e.g., high energy expenditure, risk of injury, greater visibility to predators). But is social play really of no immediate value? The argument presented above, as well as that of Bekoff (1976, 1978), have stressed the acculturation value of social play both for males and for females: that social play serves to increase the social interactions that familiarize the young with other members of the group. Dittus (1979) has reported that among toque monkeys, during a period of drought, there was an exceptionally high mortality rate among juveniles. This high mortality appears to "The sex-dependent response to social deprivation does not appear to be restricted to early stages of life. In Norway rats, adult animals deprived of social contact even for relatively short periods exhibit an increased tendency to seek out contact with conspecifics. This effect is much greater in males than in females (Meaney & Stewart, 1979).

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have been due to the fact that the juveniles were excluded from the feeding sites. Yamada (1963) has shown that among Japanese macaques adults are more tolerant of juveniles at feeding sites if they are familiar with them. These findings suggest a possible immediate function for the social interactions of juveniles. This possibility merits further investigation, especially with primates where the juvenile period is prolonged and where the juvenile's survival may depend upon its integration into the group.

1V. CONCLUSION In many mammalian species the socialization process for males is d from that for females. In addition to the contact with their mother, young males interact most frequently with other males, whereas young females interact more often with infants and other females. These social interactions serve the acculturation and, to a lesser extent, the motor-learning functions defined earlier. Sex differences in social play contribute to the socialization process by enhancing the appropriate forms of social interactions for each sex. These sex differences in social play emerge, in part, from the influence of hormonal events during the perinatal period. The critical feature of this hormonal action seems to be on the development of the neural systems that later regulate social play. Sex differences in adult-infant interactions also contribute to differences between the social play of males and females. The nature of these interactions is a function of both the behavior of the adult and that of the infant. One question that remains, however, concerns the sex difference in the topography of the preferred forms of social play. It is understandable that in several species females engage in play-mothering since this behavior probably serves a motor-learning function. But why do young females play-fight less and groom more among themselves and adults than do males if the function of both activities is simply to enhance social interaction'? One plausible answer might lie in differences in the preference for different activities. Goldberg and Lewis (1969) have shown that 1-year-old girls prefer fine motor activities while boys spend more time in gross motor activities. Studies with nursery school children have reported similar findings (Clark et a l . , 1969). Thus, the fine motor activities of social grooming may be more intrinsically rewarding to females, while the reverse may be true for play-fighting. As suggested by Goy (1970), sex differences in juvenile behavior might be due to sex differences in the neural substrates that underlie the endogenous reward mechanisms. Considered in this way, play-fighting for young males might not simply be an opportunity to interact with other males, but it might also be the occasion for a good time. There is some support for this notion. Certainly there is evidence that play-

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fighting is rewarding. Mason, Hollis, and Sharpe (1962) found that young chimpanzees preferred a handler that would play-fight with them to one that simply held them. Humphreys and Einon ( 198 1) have shown that juvenile rats prefer the companionship of a playful partner to that of a social, but nonplayful partner. Thus, the act of play-fighting itself appears to be rewarding. One interesting ramification here is that sex differences in the preferred forms of early activity that are of developmental significance might lead to sex differences in adult social skills. The studies reviewed in this article also suggest an understandably high degree of concordance between the social activities of young animals and the experiences from which they benefit most. Thus, for example, among those species in which there are sex differences in dominance-related behavior, males engage most in those forms of social play that provide for the type of social interactions from which they are most likely to benefit (e.g., interactions with males). The processes involved in such social development may be seen as being somewhat analogous to those involved in the development of the visual system. In kittens the time between 7 and 9 weeks of age is a critical period for the development of binocular vision. Monocular or binocular deprivation even for brief periods (4 to 7 days) during this time has an irreversible effect on the visual system. Barrett and Bateson (1978) found that the visual exploration of objects by kittens is greatest during this time when normal visual development is dependent on environmental input. Timney, Emerson, and Dodwell (1979) found that kittens raised in the dark would bar-press to gain visual stimulation and began to do so during the period between 7 and 9 weeks of age. Thus, the period at which visual stimulation was most rewarding corresponded to the period when, in terms ofthe development of the visual cortex, it was most influential. As in the case of social development, animals seem to seek out the forms of experience from which they benefit (in a developmental sense). This close relationship between a preferred activity and its developmental consequence may be considered as a developmental strategy in the evolutionary sense. The term strategy describes the fact that an animal engages in those activities that best contribute to its development. An animal that does so would have an advantage over animals that engage more often in activities that are less relevant to their adult roles. Through an evolutionary feedback system the behavior of the young of a species would come to be typified by those forms of activity most likely to contribute to development. At a motivational level this strategy may be expressed in subtle differences in the neural mechanisms underlying reward and which in turn determines which activities are preferred. In this sense social development is, in part, self-regulated. Sex differences in social play may be seen as differences in the developmental strategies that have evolved to conform to the sex roles typical of the species. Where large sex differences in the social roles of the adults exist, there would be

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sex differences in developmental strategies. These developmental strategies are expressed as sex differences in preferred activities which appear to be a function of perinatal hormones. Likewise, the behavior of the mother should conform to the developmental strategies of her offspring. That is, the behavior of the infant caretakers should serve to promote those activities in their young that provide for the developmentally most relevant forms of experience. As seen earlier this appears to be the case. In this sense, the role of the mother and related adults in promoting sex differences in social play is understandable. Acknowledgments The preparation of this manuscript was supported by Natural Sciences and Engineering Research Council of Canada Grants (E0300) to MJM, (A0156) to JS, and by National Institute of Child Health and Development (HD12620) and National Science Foundation (BNS-8201448) to WWB.

References Abbot, D. H. (1978). Hormones and behavior during puberty in the marmoset. Reccnr Adv. Primatol. 1, 497-500. Aldis, 0. (1975). Playfighting. New York: Academic Press. Altmann, M. (1963). Naturalistic studies of maternal care in moose and elk. In H. Rheingold (Ed.), Maternal behavior in mamnials (pp. 233-253). New York: Wiley. Altmann, S . A. (1967). The structure of primate social communication. In S. A. Altmann (Ed.), Communication among primates (pp. 325-362). Chicago: Univ. of Chicago Press. Anderson, J . W. (1972). On the psychological attachment of infants to their mothers. J . Biosocial Sci. 10, 554-558. Angermeir, W. F., Phelps, J. B., Murray, D., & Howanstine, J . (1968). Dominance in monkeys: Sex differences. Psychonorn. Sci. 12, 344. Balazs, R., & Cotterrell, M. (1972). Effect of hormonal state on cell number and functional maturation of the brain. Nature (London) 236, 348-350. Baldwin, J. D. (1969). The ontogeny of social behavior of squirrel monkeys (Saimiri Scirrreus) in a seminatural environment. Folia Primatol. 11, 35-79. Baldwin, J . D., & Baldwin, J. J. (1974). Exploration and social play in squirrel monkey (Saimiri). Am. Zool. 14, 303-314. Bardin, C. W., & Catterall, J. F. (1981). Testosterone: A major determinant of extragenital sexual dimorphism. Science 211, 1285-1294. Barnett, S. A. (1958). An analysis of social behaviour in wild rats. Proc. Zool. Soc. London 130, 107- 152. Barnett, S . A. (1975). The rat: A stud.y in behavior. Chicago: Univ. of Chicago Press. Barrett, P. T., & Bateson, P. P. G. (1978). Development of play in cats. Behaviour 66, 106- 120. Baum, M. J. (1972). Precocious mating in male rats following treatment with androgen or estrogen. J . Comp. Physinl. Psychol. 78, 356-367. Baum, M. J. (1979). Differentiation of coital behavior in mammals: A comparative analysis. Neurosci. Biobehav. Rev. 3, 265-284. Beach, F. A. (1956). Characteristics of masculine sex drive. In M. R. Jones (Ed.), Nebraska symposium on motivation (pp. 1-31). Lincoln, Nebraska: Univ. of Nebraska Press.

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49

Beatty. W. W. (1979). Gonadal hormones and sex differences in nonreproductive behaviors in rodents: Organizational and activational influences. Horm. Behav. 12, I 12- 163. Beatty, W. W., Dodge, A. M., Traylor, K . L., Donegan, J. C.. & Godding, P. R. (1982). Septa1 lesions increase play-fighting in juvenile rats. Physiol. Behuv. 28, 649-652. Beatty. W. W., Dodge, A. M., Traylor, K . L., & Meaney, M . J . ( 198 I ). Temporal boundary of the sensitive period for hormonal organization of social play in juvenile rats. Physiol. Behav. 26, 24 1-243. Beeman, E. A. (1947). The effect of male hormone on aggressive behavior in mice. Physiol. Zoo/. 20, 373-405. Bekoff, M. (1974). Social play and play-soliciting by infant canids. Am. Zoo/. 14, 323-341. Bekoff. M. (1976). The social deprivation paradigm: Who’s being deprived of what? Dev. Psychob i d . 9, 499-500. Bekoff. M. (1977). Socialization in mammals, with an emphasis on non-primates. In S. ChevalierSkolnikoff & F. E. Poirier (Eds.), Primate bio-social development (pp. 603-636). New York: Garland. Bekoff, M. (1978). Social play: Structure, function, and the evolution of cooperative social behavior. In G . M. Brughardt & M. Bekoff (Eds.), The developmenr ofbehuvior (pp. 367-384). New York: Garland. Bell, R. Q. (1971). Stimulus control of parent or caretaker behavior of offspring. Dev. Psychol. 4, 63-72. Bell, R . W.. & Costello, N. (1964). Three teats for sex differences in tactile sensitivity in the new born. B i d . Neonar. 7, 335-347. Berman, P. W. (1980). Are women more responsive than men to the young’?A review of developmental and situational variables. Psychol. Bull. 88, 668-695. Bernstein, I. S. (1964). Role of the dominant male rhesus monkey in response to external challenges to the group. J . Comp. Physiol. Psychol. 57, 404-406. Bemstein, 1. S. (1967). A field study of the pigtail monkey. Primates 8, 217-228. Bemstein, I . S . (1968). The lutong of kuola selangor. Behuviour 32, 1-16. Bertrand, M . (1969). The behaviorul repertoire o f t h e stionp/ail macaque. New York: Karger. Birke, L. 1. A.. & Sadler, D. (1983). Progestin-induced changes in play behavior of the prepubertal rat. Physiol. Behav. 30, 341-347. Blurton-Jones, N. (1976). Rough-and-tumble play among nursery school children. In J . S . Bruner, A. Jolly, & K. Sylva (Eds.), PIuy (pp. 352-363). New York: Penguin. Blurton-Jones, N. G . , and Konner, M. J. (1973). Sex differences in behaviour of London and Bushman children. In R. P. Michael & J . H. Crook (Eds.). Compurutive ecologyund behaviour of’primates (pp. 689-750). New York: Academic Press. Bolwig, N . (1959). A study of the behavior of the chacma baboon, Pupio urisinus. Behaviorrr 14, 136- 163. Braggio. J. T., Nadler, R. D., Lance, J., & Miseyko. D. (1978). Sex differences in apes and children. Recent Adv. Primutol. I , 529-532. Brain, P. F.. & Nowell, N. W. (1969). Some behavioral and endocrine relationships in adult male, laboratory mice subjected to open-field and aggression tests. Physiol. Behav. 4, 945-947. Bramblett, C. A . (1973). Social organization as an expression of role behavior among old world monkeys. Primates 14, 101-1 12. Bramblett. C. A. (1978). Sex differences in the acquisition of play among juvenile vervet monkeys. In E. 0. Smith (Ed.), Sociul play in primates (pp. 33-48). New York: Academic Press. Breuggenian, J. A. (1964). Parental care in a groups of free-ranging rhesus monkeys (Macucu mulatta). Foliu Primutol. 2, 93- 110. Bridges, R. S . , Zarrow, M . X . . & Dcncnberg. R. H. (1973). The role of neonatal androgen in the

50

MICHAEL J . MEANEY ET A L .

expression of hormonal induced maternal responsiveness in the adult rat. Horm. Eehuv. 4, 315322. Burton, F. D. (1972). The integration of biology and behavior in the socialization of Mucucu sylvana of Gibraltar. In F. E. Poirier (Ed.), Primate socializarion (pp. 29-62). New York: Random House. Caggiula, A. R., Shaw, D. H., Antelman, S . M., & Edwards, D. J. (1976). Interactive effects of brain catecholamines and variations in sexual and nonsexual arousal on copulatory behavior of male rats. Brain Res. 111, 321-336. Calhoun, J . B., (1962). The ecology and.wciology UftheNorwuy rut. Bethesda, MD: U . S . Dept. of Health, Education and Welfare. Chalmers, N. R. (1980). The ontogeny of play in feral olive baboons (Papio anuhis).Anim. Eehav. 28, 570-585. Chamove, A,, Harlow, H. F., & Mitchell, G. (1967). Sex differences in the infant-directed behavior of preadolescent rhesus monkeys. Child Dev. 38, 329-335. Cheney, D. L. (1978). Interactions of male and female baboons with adult females. Anim. Eehtrv. 26, 389-408. Cidlowski, J. A . (1982). Glucocorticoids stimulate ribonucleic acid degradation in isolated rat thymic lymphocytes in virro. Endocrinology 111, 184- 190. Clark, A. H., Wyon, S . M., & Richards, M. P. M. (1969). Free-play in nursery school children. J. Child Psycho/. Psychiar. 10, 205-216. Clark, C. B. (1977). A preliminary report on weaning among chimpanzees of the Gombe National Park, Tanzania. In S . Chevalier-Skolnikoff & F. E. Poirier (Eds.), Primute bio-social development (pp. 235-260). New York: Garland. Cotterrell, M., Balazs, R., & Johnson, A. L. (1972). Effects of corticosteroids on the biochemical maturation of rat brain: Postnatal cell formation. J. Neurochem. 19, 2 I5 1-2167. Dahlherg, E., Snochowski, M., & Gustafsson, J.-A. (1981). Regulation of the androgen and glucocorticoid receptors in rat and mouse skeletal mouse cytosol. Endocrinulogy 108, 143I 1440. Davies, J . A,, & Kemble, E. D. (1983). Social play behaviors and insect predation in northern grasshopper mice (Onychomys leucoguster). Eehuv. Proc. 8, 197-204. DeVore, I . T. (1963). Mother-infant relations in baboons. In H. Rheingold (Ed.), Maternal Behavior in mammals (pp. 305-335). New York: Wiley. Dittus, W. P. J. (1975). Population dynamics of the Togue monkey, Mucacu simica. In R. H. Tuttle (Ed.), S O C ~ O C . C O /and O ~ ~psychology V primates (pp. 125- 151). The Hague: Mouton. Dodge, A. M. (1981). An invcstigation of the effects of ventromedial hypothalamic and medial preoptic area lesions on play-fighting in juvenile rats. Unpublished MA thesis, North Dakota State University. Dolhinow, P. (1971). At play in the fields. Nat. Hisr. 80, 66-71. Dolhinow, P. J . , & Bishop, N. (1970). The developmcnt of motor skills and social relationships among primates through play. In J. P. Hill (Ed.), Minnesotu symposia on childpsychology Vol. IV, pp. 141-198). Minneapolis: Univ. of Minnesota Press. Draper, P. (1973). Crowding among hunter-gatherers: The !Kung. Science 182, 301-303. Drickamer, L. C., & Vessey, S. H. (1973). Group changing in free-ranging male rhesus monkeys. Primates 14, 359-368. Dyer, R. G . , MacLeod, N. K., & Ellendorff, F. (1976). Electrophysiological evidence for sexual dimorphism and synaptic convergence in the preoptic anterior hypothalamic areas of the rat. Proc. R . Soc. London Ser. E 193, 421-440. Ehrhardt, A. A,, & Baker, S . W. (1974). Fetal androgens, human CNS differentiation, and behavior sex differences. In R. C. Friedman, R. M. Richart, & R . L. Vande Wiele (Eds.). SexdifSererices in behavior (pp. 53-76). Ncw York: Wiley.

SOCIAL PLAY

51

Ehrhardt, A. A , , & Money, J . ( 1967). Progestin-induced hermaphroditism: IQ and psychosexual identity in a study of ten girls. J . Ser Res. 3, 83- 100. Ehrhardt, A. A,, Epstein, R., & Money, J. (1968). Fetal androgens and female gender identity in the early treated adrenogenital syndrome. Johns Hopkins Med. J. 122, 160- 167. Eleftheriou, B. E., & Sprott. R. L. (1975a). Hormonul correlaies of heliuvior, V d . I : A l;fi~.spun view. New York: Plenum. Eleftheriou, B. E., & Sprott. R. L. (197%). Homionul correlutes qfbehiivior. Vol 2: An o r p k w n i c view. New York: Plenum. Ember, C. (1973). Female task assignment and the social behavior of boys. Ethos 1, 424-439. Erwin, J . , Anderson, B., & Bunger, D. (1975). Nursing behavior of infant pigtail monkeys (Macacu nemestrina): Preferences for nipples. Percept. Motor Skills 40, 592-594. Estrada. A. (1978). Social relations in a free-ranging troop of Muciicu urcroides. Recenr Advu. Primufol. I , 55-58. Fagen. R. (1981). Animal P l q Behavior. London and New York: Oxford Univ. Press. Fagot, B. 1. (1974). Sex differences in toddlers' behavior and parental reaction. Dev. Psycho/. 10, 554-558. Fox, T. 0.. Vito, C. C., & Wieland, S . J . (1978). Estrogen and androgen receptor proteins in embryonic and neonatal brain: Hypotheses for roles in sexual differentiation of behavior. Am. Zoo/. 18, 525-537. Freedman, D. G. ( 1974). Human iifuncy: An evolrttioriar~p":~l~eetirv. New York: Halstead. Freeman, H. E., & Alcock, J . (1973). Play behaviour of a mixed group of juvenile gorillas and orangutans. In/. Z o o Yeurh. 13, 189-194. Gartlan, J. S . (1968). Structure and function in primate society. Foliu Priinutol. 8, 89-120. Gentry. R. L. (1974). The development of social behavior through play in the stellar sea lion. Am. Zoo/. 14, 391-403. George, F. W., & Ojeda S. R. (1982). Changes in aromatase activity in the rat brain during embryonic, neonatal, and infantile development. Endocrinology I I I , 522-529. Gerall, H. D., Ward, I . L., & Gerall, A. A. (1967). Disruption of the male rat's sexual behaviour induced by social isolation. Ariim. Behav. 15, 54-58. Goldberg. S..& Lewis, M. (1969). Play behavior in the year-old infant: Early sex differences. Child Dev. 40, 21-31. Goldfoot, D. A,, & Wallen. K. (1978). Development of gender role behaviors in heterosexual and isosexual groups of infant rhesus monkeys. Recent Adv. Prirnarol. 1, 155- 160. Goldman, L., & Swanson, H. H. (1975). Developmental changes in pre-adult behavior in confined colonies of golden hamsters. Dev. PsycAoDiol. 8, 137- 150. Gorski, R . A. (1973). Perinatal effects of sex steroids on brain development and function. Prog. Bruin Res. 39, 149- 162. Gorski. R. A , , Gordon, J . H., Shyrne, .I.E., & Southam. A . M. (1978). Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Bruin Res. 148, 333346. Goy, R. W. (1970). Early hormonal influences on the development of sexual and sex-related behavior. In F. 0 . Schmitt (Ed.), The neurosciences: Second study program (pp. 196-206). New York: Rockefeller Univ. Press. Goy. R. W. (1978). Development of play and mounting behavior in female rhesus virilized prenatally with esters of testosterone or dihydrotestosterone. Recent A&. Prirnutol. I , 449-462. Goy. R . W . , & Goldfoot, D. A. (1974).Experiential and hormonal factors influencing development of sexual behavior in the male rhesus monkey. In F. 0. Schmitt (Ed.), The ~ I ~ U ~ O S C Third ~~IICPS: study program ( p p ~571-582). New York: Rockefeller Univ. Press. Goy. R. W., Kemnitz, J . W., Slimp, J . C., Irving, S. M., & Neff, D. A . (lY79).friwpric lesions in pri~puhertulrnule rtie.sus und developrrwnt of testiculur endocrine f i t r m i o n arid behtivior. Pre-

52

MICHAEL J . MEANEY ET A L .

sented at the 11th annual meeting of the Eastern Conference on Reproductive Behavior, New Orleans, LA. Goy, R. W., & McEwen, B. S . (1980). Sexual diflerentiation of the brain. Cambridge. MA: MIT Press. Goy, R. W., & Phoenix, C. H. (1971). The effects of testosterone propionate administered before birth on the development of behavior in genetic female rhesus monkeys. In C. Sawyer & R. Gorski (Eds.), Steroid hormones and brain function (pp. 193-202). Berkeley: Univ. of California Press. Harper, L. V . (1971). The young as a source of stimuli controlling caretaker behavior. Dev. Psyc-hol. 4, 73-88. Harcourt, A. H., & Stewart, K. J . (1981). Gorilla male relationship: Can differences during immaturity lead to contrasting reproductive tactics in adulthood. Adult Behav. 29, 206-210. Hard, E., & Larsson, K. (1968). Dependence of adult mating behavior in male rats on the presence of littermates in infancy. Brain Behav. Evol. 1, 405-419. Harlow, H. F. (1965). Sexual behavior in rhesus monkeys. In F. A. Beach (Ed.), Sex and behavior. (pp, 234-265). New York: Wiley. Harlow, H. F. (1969). Age-mate or peer affectional system. Adv. Study Behuv. 2, 333-383. Harlow, H. F., & Harlow (1970). Harlow, H. F., & Lauersdorf, H. E. (1974). Sex differences in passion and play. Perspecr. B i d . Med. 17, 348-60. Hinde, R. A. (1971). Development of social behavior. In A. M. Schrier & F. Stolhitz (Eds.), Behavior of nonhuman primates (Vol. 3 , pp. 1-68). New York: Academic Press. Hinde, R. A. (1974). Biological basis of human social behaviour. New York: McGrdw-Hill. Hinde, R. A., & Spencer-Booth, Y. (1967). The behavior of socially living rhesus monkeys in their first two and a half years. Anim. Behav. 15, 169-196. Hoof, I. A. R. A. M., van (1972). A comparative approach to the phylogeny of laughter and smiling. In R. A. Hinde (Ed.), Non-verbal communication (pp. 209-2371, New York: Cambridge Univ. Press. Hrdy, S. B. (1976). Care and exploitation of nonhuman primate infants by conspecifics other than the mother. Adv. Study Behav. 6 , 101-158. Hrdy, S. B. (1977). The Langurs of Abu. Cambridge, MA: Harvard Univ. Press. Hrdy, S. B., & Hrdy, D. B. (1977). Hierarchical relations among female Hanuinan langurs (Primates: Colobinue. Presbytis ente/lus). Science 193, 913-915. Humphreys, A. P., & Einon, D. F. (1981). Play as a reinforcer for maze-learning in juvenile rats. Anim. Behav. 29, 259-270. Itani, J . (1959). Paternal care in the wild Japanese monkey, Macacufuscutu fuscuta. Primates 2,6193. Janne, 0 . .Kontula, K . , Vihko, R . , Feil, P. D., & Bardin, C. W. (1978). Progesterone receptor and regulation of progestin action in mammalian tissues. Med. Biol. 56, 225-248. Jay, P. (1963). Mother-infant relation in langurs. In H. Rheingold (Ed.), Murernal behavior in mammals (pp. 282-304). New York: Wiley. Jensen, G. D. (1966). Sex differences in developmental trends of mother-infant monkey behavior ( M . nemestrina). Primates 7 , 403. Jensen, G . D., Bobbitt, R. A,, & Gordon, B. N. (1967). The development of maternal independence in mother-infant pigtailed monkeys, Macuca nemesrrina. In S. A. Altmann (Ed.), Social communication among primates (pp. 43-54). Chicago: Univ. of Chicago Press. Jolly, A. (1972). The evolution ofprimate behavior. New York: Macmillan. Joslyn, W. D. (1973). Androgen-induced social dominance in infant female rhesus monkeys. J . Child Psychol. Psychiat. 14, 137- 145.

SOCIAL PLAY

53

Kawai, M. (1958). On the rank system in a natural group of Japanese monkeys: 1. Basic and dependent rank. Primates I , I 11-150. Kotelchuck. M. (1976). The infant's relationship to the father: Experimental evidence. In M. E. Lamb (Ed.), The role of the father in child development. New York: Wiley. Kummer, H. (1968). Social organizarion of hamudryus buboons: A ,field study. Chicago: Univ. of Chicago Press. Lahiri, R . K . , & Southwick, C. H. (1966). Parental care inMacam slvvuna. FoliaPrimurol. 4 , 257264. Lamb, M. E. (1977). Father-infant and mother-infant interaction in the first year of life. Child Dev. 48, 167-181. Lancaster, J. B. (1971 ). Play-mothering: The relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopifhecus uethiops). Folia Primarol. 15, I61- 182. Lawick-Goodall, J . , van (1968). The behaviour of free-living chimpanzees in the Gonibe Stream area. Anim. Behav. Monogr. 1, 161-311. Lazar, J . W., & Beckhorn, G . C. (1974). Social play or the development of social behaviour in ferrets (Mustela putorious). Am. Zool. 14, 405-414. Lee, P. C., & Oliver. J. 1. (1979). Competition, dominance and the acquisition of rank in juvenile yellow baboons (Papio cytiocephalus). Anim. Behav. 27, 576-585. Leedy, M. G., Vela, E. A,, Popolow, H. B., & Gerall, A. A. (1980). Effects of prepubertal medial preoptic area lesions on male sexual behavior. Physiol. Behav. 24, 341 -346. Lehrman, D. S. (1953). A critique of Konrad Lorenz's theory of instinctive behavior. Q. Rev. Biol. 28, 337-363. Leshner, A. 1. (1975). A model of hormones and agonistic behavior. Physiol. Behav. 15, 225-235. Levine, J . , Fishman, C., & Kagan, J. (1967). Social class and sex as determinants of maternal behavior. Am. J . Orthnpsychiat. 37, 397. Ley, R. G . , & Koepke, J. E. (1982). Attachment behavior outdoors: Naturalistic observations of sex and age differences in the separation behavior of young children. Infant Behav. DPV.5 , 195201.

Lieberburg, 1.. MacLusky. N., & McEwen, B. S . (1980). Androgen receptors in perinatal rat brain. Brain Res. 196, 125-138. Lieberburg, I., MacLusky, N. J . , Roy, E. J . , & McEwen, B. S. (1978). Sex steroid receptors in the perinatal rat brain. Am. Zoo/. 18, 539-544. Loizos, C. (1967). Play behaviour in higher primates: A review. In D. Morris (Ed.). Primate erhologv (pp. 176-218). London: Wiedenfield & Nicolson. Lore, R., & Flannelly, W. (1977). Rat societies. Sci. Am. 236, 106-118. Loy, I . (1975). The descent of dominance in Mac.acut Insights into the structure of human societies. In R. N. Tuttle (Ed.), Socioecology andpsychologv ofprimates (pp, 153- 180). Paris: Mouton. MacRoberts, M. H. (1970). The social organization of the Barbary apes on Gilbraltar. Am. J . Phvs. Anthropol. 33, 83-99. Martini. L. (1978). Role of the metabolism of steroid hormones in the brain in sex differentiation and sexual maturation. In G. Dorner & M. Kawakarni (Eds.), Hormones and brain developmenf (pp. 3- 12). Amsterdam: Elsevier. Mason, W. A. (1961). The effects of social restriction on the behavior of rhesus monkeys: 111 dominance tests. J. Comp. Physiol. Psychol. 54, 694-699. Mason, W. A . (1965). The social development of monkeys and apes. In I. Devore (Ed.), Primare behavior: Field srudies of monkeys arid apes (pp. 514-543). New York: Holt. Mason, W. A., Hollis, J . H.. & Sharpe, L. G . (1962). Differential rehponses of chimpanzees to social stimulation, J. Comnp. Phvsiol. Psychol. 55, 1105-1 110. Mayer, A. D., Freeman, N . C. G . , & Rosenblatt, J. S . (1979). Ontogeny of maternal behaviour:

54

MICHAEL J . MEANEY ET AL.

Factors underlying changes in responsiveness from thirty to ninety days. Uev. Psychobiol. 12, 425-439. Mayer, A. D., & Rosenblatt, J . S . (1979a). Ontogeny of maternal behaviour in the laboratory rat: Early origins in eighteen- to twenty-seven day old young. Dev. Psychobiol. 12, 407-424. Mayer, A. D., & Rosenblatt, J . S . (1979b). Hormonal influences during the ontogeny of female maternal behaviour in juvenile rats. J . Comp. Physiol. Psychol. 93, 879-898. Mayer, M., & Rosen, F. (1975). Interaction of anabolic steroids with glucocorticoid receptor sites in rat muscle cytosol. Am. J . Physiol. 229, 1381-1386. McClintock, M. K., & Adler, N. T. (1978). The role of the female during copulation in wild and domestic Norway rats (Rattus norvegicus). Behaviour 61, 67-96. McEwen B . S . (1977). Glucocorticoid receptors in neuroendocrine tissues. In V. H. T. James (Ed.), Endocrinology (Vol. 1). Amsterdam: Exerpta Medica. McEwen, B. S . , Lieberburg, I . , Chaptal, C., & Krey, L. C. (1977). Aromatization: Important for sexual differentiation of the neonatal rat brain. Horm. Behav. 9, 249-263. McGinnis, M. Y., Davis, P. G., Meaney, M. J . , Singer, M . , & McEwen, B. S . (1983). In vitro measurement of cytosol and cell nuclear androgen receptors in male rat brain and pituitary. Brain Res. 215, 75-82. Meaney, M. J . , Dodge. A. M., & Beatty, W. W. (1981). Sex dependent effects of amygdaloid lesions on the social play of prepubertal rats. Physiol. Behav. 26, 467-472. Meaney, M. J., & McEwen, B. S. (1984). Androgen implants into the amygdala during the neonutal period masculinize the play-fighting qfjemale rat pups. (Submitted) Meaney, M. J., McGinnis, M. Y., Aitken, D., & McEwen, B . S . (1984). Sexdiferences in nuclear androgen-receptor concentrations during the neonatal period in the rat brain. (Submitted) Meaney, M. J . , McGinnis, M. Y., & McEwen, B . S . (1982). The sexual differentiation of social play in Norway rat pups is mediated by the androgen receptor system. Soc. Neurosci. Abstr. 8, 611. Meaney, M. J . , Sapolsky, R. M., & McEwen, B . S . (1985). The development of the glucocorticoid receptor system. I : Ontogeny and autoregulation. Dev. Brain Res. (in press). Meaney, M. J., & Stewart, J. (1979). Environmental factors influencing the affiliative behavior of male and female rats (Raftusnorvegicus). Anim. Learn. Behav. 7 , 397-405. Meaney, M. J . , & Stewart, J . (1981a). A descriptive study of social development in the rat Rattus norvegicus. Anirn. Behav. 29, 34-45. Meaney, M. J., & Stewart, J . (1981b). Neonatal androgens influence the social play of prepubescent male and female rats. Horm. Behav. 15, 197-213. Meaney, M. J . , & Stewart, J . (1983). The influence of exogenous testosterone and corticosterone on the social behavior of prepubertal male rats. Bull. Psychonom. SOC. 21, 232-234. Meaney, M. I . . Stewart, J . , & Beatty, W. W. (1982). The effects of neonatal glucocorticoids on the social play of Juvenile rats. Horm. Behav. 16, 475-491. Meaney, M. J . , Stewart, J., Losos, E., & Ervin, F. ( 1 9 8 4 ~ )Infunt . carrying bv nulliparous, fernule vervet monkeys (Cercopirhecus aethiops). (Submitted) Meaney, M. J . , Stewart, J., Poulin, P., & McEwen, B . S. (1983). Sexual differentiation of social play in rat pups is mediated by the neonatal androgen-receptor system. Neuroendocrinolo~.~ 37, 85-90. Mech, L. D. (1970). The wolf? The eco1og.y and behaviour ofan endangered species. New York: Natural History Press. Milch, K. H., & Missakian-Quinn, L. E. (1977). Longitrmdinul studv of social play in peer-reared children. Paper presented at the annual meeting of the Animal Behavior Society, University Park, Pennsylvania. Miller, R. E., Caul. W. F., & Mirsky. I . A. (1967). Communication of affects between feral and socially isolated monkeys. J . Personal. Soc. Psycho/. 7 , 23 1-239.

SOCIAL PLAY

55

Mitchell, G . D. (1968). Attachment differences in male and female infant monkeys. ChildDev. 39, 61 1-620. Mitchell, G . (1969). Paternalistic behavior in primates. Psychol. Bull. 71, 399-417. Mitchell, G . (1972). Looking behaviour in the rhesus monkey. J . Phenom. Psychol. 3, 53-67. Mitchell, G. ( 1979). Behavioral sex direrences in nonhuman primutes. Princeton, NJ: Van Nostrand Reinhold. Mitchell, G . D., Ruppenthal, G . C . , Raymond, E. J . , & Harlow, H. F. (1966). Long-term effects of multiparous and primiparous monkey mother rearing. Child Dev. 37, 781-791. Mohnot, S. M. ( 1978). Peripheralisation of weaned male juveniles in Presbvris entellus. Recenr Adv. Primatol. I , 87-92. Money, J., Ehrhardt, A. A , , & Masica, D. N. (1968). Fetal feminization induced by androgen insensitivity in the testicular feminizing syndrome: Effect on marriage and maternalism. Johns Hopkins Med. J . 123, 105- 114. Moore, C. L. (1981). An olfactory basis for maternal discrimination of sex of offspring in rats (Rattus norvegicus). Anim. Behav. 29, 383-386. Moore, C. L., & Morelli, G . L. (1979). Mother rats interact differently with male and female offspring. J . Comp. Phvsiol. Psychol. 93, 677-684. Moss. H. (1967). Sex, age and state as determinants of mother-infant interaction. Merrill-Palmer Q . 13, 19-36. Moss, H. (1974). Early sex differences and mother-infant interaction. In R. M. Richart & R. L. Van de Wiele (Eds.), Sex di@rences in behuvior (pp. 149-164). New York: Wiley. Munroe, R . L., & Munme, R. H. (1971). Effect ofenvironmental experience of spatial ability in an East African society. J . Soc. Psychol. 83, 15-22. Nadler, R. D., & Braggio, J . T. (1974). Sex and species differences in captive-reared juvenile chimpanzees and orangutans. J. Hum. Evol. 3, 541-550. Naess, D.,Haug. E., Attrramadal, A , , AaKvaag. A , , Hansson, V., & French, F. (1976). Androgen receptors in the anterior pituitary and central nervous system of the androgen “insensitive” (Tfni) rat: Correlation between receptor binding and effects of androgens on gonadotropin secretion. Endocrinology 99, 1295- 1303. Nerlove, S. B., Munroe, R. H., & Munroe, R. L. (1971). Effect of environmental experience on spatial ability: A replication. J . Soc. Psychol. 84, 3-10. Nicolson. N. A. (1977). A comparison of early behavioral development in wild and captive chimpanzees. In S. Chevalier-Skilnikoff & F. E. Poirier (Eds.), Primure bi(~-sociddevelopment (pp. 529-562). New York: Garland. Nishizuka, M., & Arai, Y. (1981). Sexual dimorphism in synaptic organization in the aniygdala and its dependence on neonatal hormonal environment. Bruin Res. 212, 31-38. Olioff, M., & Stewart, J. (1978). Sex differences in the play behavior of preubescent rats. Physiol. Behuv. 20, 113-115. Owens, N. W. (l975a). Social play behaviour in free-living baboons, Papio anubis. Anim. Behuv. 23, 387-408. Owens, N. W. (1975b). A comparison of aggressive play and aggression in free-living baboons, Papio unubis. Anim. Behav. 23, 575-165. Packer, C. (1975). Male transfer in olive baboons. Nulure (London) 255, 219-220. Packer, C. (1977). Reciprocal altruism in Papio anuhis. Naritre (London) 265, 441-443. Packer, C. (1978). Behavior affecting immigration of male baboons at Gombe National Park. Recent Adv. Primatol. 1, 75-78. Parke, R. D., & Suomi, S . J. (1981). Adult male infant relationships: Human and nonhuman primate evidence. In K. Immelman, G . W. Barlow. L. Petrinovitch, & M. Main (Eds.), Behaviorul devc,lopmerzr (pp. 700-725). New York: Cambridge Univ. Press.

56

MICHAEL J . MEANEY ET AL.

Payne, A. P., & Swanson, H. H. (1972). The effcct of sex hormones on the aggressive behavior of the female golden hamster (Mesocricerus aratus watcrhousc). Anim. Brhuv. 20, 782-787. Phoenix, C. H., Goy, R. W., Gerall, A. A , , & Young, W. C. (1959). Organizational action of prenatally administered testosterone propionate on the tissues mediating behavior in the female guinea pig. Enducrinologv 65, 369-382. Poirier, F. E. (1972). Nilgiri langur behavior and social organization. In F. W. Voget & R . L. Stephenson (Eds.), For the chief: Essuys in honor of Luther S . Cressman (pp. 119-134). Eugene, Oregon: Univ. of Orcgon Anthropology Papers. Poole. T. B. (1966). Aggressive play in polecats. Symp. 2001.Sue. London 18, 23-44. Poole, T. B., & Fish, J . (1976). An investigation of individual, age, and sexual diffcrences in the play of Rattus norvegicus (Murnmaliu: Rodenria). Pruc. Zool. Soc. London 179, 249-260. Pusey. A. (1978). Age changes in the mother-offspring association of wild chimpanzees. Recent Adv. Primutol. I , 119-124. Rabb, G. B., Ginsburg, B. E., & Andrews, S . (1962). Comparative studies of Canid behavior, IV. Mating behavior in relation to social structure in wolves. Am. Zool. 2, 440. Rabb, C. B., Woolpy, J . H., & Ginsburg, B. E. (1967). Social relationships in a group of captive wolves. Am. Zool. 7, 305-31 I . Raleigh, M. J . , Flannery, I. W., & Ervin, F. R. (1979). Sex differences in behavior among juvenile vervet monkeys (Cercopithecus aethicips sabncus). Behav. Neural Biol. 26, 455-465. Rebelsky, F., & Hanks, C. (1971). Father’s verbal interactions with infants in the first three months of life. Child Dev. 42, 63-68. Redican, W. K. (1976). Adult male-infant interactions in non-human primates. In M. E. Lamb (Ed.), The role of the father in child development. New York: Wiley. Redican, W. K., & Mitchell, G. (1974). Play between adult male and female rhesus monkeys. Am. ZOO^. 14, 295-302. Resko, J . A . , Feder, H. H., &Goy, R. W. (1968). Androgen concentrations in plasma and tcstes of developing rats. J . Endrocinol. 40, 485-49 I . Rose, R. M., Gordon, T. P., & Bernstein, 1. S. (1972). Plasma testosterone levels in male rhesus: Influences of social and sexual stimuli. Science 178, 643-645. Rosenblum, L. A. (1974). Sex differences in mother-infant attachment in monkeys. In R. C. Friedman, R . M. Richart, & R. L. Van de Wiele (Eds.), Sexdiflerences in behavior New York: Wiley. Rosenblum, L. A . (1974). Sex differences, environmental complexity, and mother-infant relations. Arch. Sex Behuv. 3, 117-128. Rossi, A. S. (1977). A biosocial perspective on parenting. Duedalus 106, 1-31. Rowell, T. E. (1966). Hierarchy in the organization of a captive baboon group. Anim. Behav. 14, 430-443. Rowell, T. E., Din, N. A,, & Omar, A. (1968). The social development of baboons in their first three months. J . Zool. 155, 461-483. Ruppenthal, G. C., Harlow, M. K . , Eisele, C. D., Harlow, H. F., & Suomi, S. J . (1974). Development of peer interactions of monkeys reared in a nuclear family environment. Child Dev. 45, 670-682. Ryon, C. J . (1979). Aspects of dominance behavior in groups of sibling coyoteired wolf hybrids. Behav. Neural Biol. 24, 69-78. Sachs, B. D., & Harris, V. S. (1978). Sex differences and developmental changes in selected juvenile activities (play) of domestic lambs. Anim. Behav. 26, 678-684. Sackett, G. P. (1974). Sex differences in rhesus monkeys following varied rearing experiences. In R. C. Friedman, R. M. Riehart, & R. L. Van de Wiele (Eds.), Sex differences in behavior (pp. 99112). New York: Wiley. Sade, D. S . (1967). Determinants of dominance in a group of free-ranging rhesus monkeys. In S. A.

SOCIAL PLAY

57

Altmann (Ed.), Social conimrrnicution among primates (pp. 99-1 14). Chicago: Univ. of Chicago Press. Sade, D. S. (1967). Determinants of dominance in a group of free-ranging rhesus monkeys. In S . A. Altmann (Ed.). Social communication among primutes (pp. 99-1 14). Chicago: Univ. of Chicago Press. Sade, D. S . (1980). Population biology of free-ranging rhesus monkeys on Cayo Santiago, Puerto Rico. In M. N. Cohen, R. S. Malpass, & H. G. Klein (Eds.), Biosociul mechunisms of’ populution regulation (pp. 171-188). New Haven, Conn.: Yale Univ. Press. Sasson, S., & Mayer, M. (1981). Antiglucocorticoid activity of androgens in rat thymus lymphocytes. Endocrinologv 108, 760-766. Schaller, G. B. (1972). The Serengeti lion: A stud,v of predutor-prev relations. Chicago: Univ. of Chicago Press. Scott, J. P., & Fuller, J. L. (1965). Genetics and soc.ial behavior ofthe dog. Chicago: Univ. of Chicago Press. Seay, B. M., Schlottman, R . S., & Gandolfo, R. (1972). Early social interaction in two monkey species. .I. Genet. Psychol. 87, 37-43. Seyfarth, R. M., Cheney, D. L., & Hinde, R. A. (1978). Some principles relating social interactions and social structure among primates. Recent Adv. Primutol. 1, 39-54. Shapiro, B. H., Goldman. A. S . , Bongiovanni, A . M., & Marino, J. M. (1976). Neonatal progesterone and feminine sexual development. Nature (London)264, 795-796. Simonds, P. E. (1974). Sex differences in bonnet macaque networks and social structure. Arch. Sex Behuv. 3, 151-165. Simonds, P. E. (1977). Peers, parents and primates: The developing network of attachments. In T. Alloway, P. Pliner & L. Krames (Eds.), Attachment behavior: Advances in the studv of communication and aflect (Vol. 3, pp. 145-176). New York: Plenum. Staudt, J . , & Dorner, G. (1976). Structural changes in the medial and central amygdala of the male rat following neonatal castration and androgen treatment. Endokrinologie 67, 296-300. Struhsaker, T. (1967). Social structure among vervet monkeys, Cercopirhecus aethoips. Behaviour 29, 83-121. Suomi, S. J. (1977). Development of attachment and other social behaviors in rhesus monkeys. In T. Alloway, P. Pliner & L. Krames (Eds.), Aftachmerrt behavior: Advances in the study of communication and aflect (Vol. 3, pp. 197-224). New York: Plenum. Suomi, S . J., & Harlow, H . F. (1976). Monkeys without play. In J . S . Bruner, A. Jolly, & K. Sylva (Eds.), Play (pp. 490-495). New York: Penguin. Symons, D. (1974). Aggressive play and communication in rhesus monkeys (Macacu mulatfa).Am. 2001. 14, 317-322. Symons, D. (1978). Pluv and aggression: A s1ud.v of rhesus monkeys. New York: Columbia Univ. Press. Tasch, R. J . (1952). The role of the father in the family. J . Exp. Educ. 20, 319-361. Taylor, G. T. (1980). Fighting in juvenile rats and the ontogeny of agonistic behavior. J . Comp. Physiol. P.y.ycho1. 94, 953-961. Thoman. E. B., Leiderman, P. H., & Olson, J. P. (1972). Neonate-mother interaction during breast feeding. Dev. Psychol. 6 , 110- 118. Thor, D. H., & Holloway, W. R. (1983). Play-solicitation behavior in juvenile male and female rats. Anim. Learn. Behuv. 11, 173-178. Timney, B. N., Emerson, V. F., & Dodwell, P. S. (1979). Development of visual stimulus-seeking in kittens. Q . J . Exp. Psycho/. 31, 63-81. Toran-Allerand, C. D. (1976). Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: Implications for sexual differentiation. Bruin Res. 106, 407-4 12.

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Traylor, K . L. ( 1982). Social interactions a r n o n ~cuptiw ,cvlves (Cariis lupus). Unpublished MA thesis, North Dakota State University. Vito, C. C., Wieland, S. J., & Fox, T. P. (1979). Androgen receptors exist throughout the ‘critical period’ of brain sexual differentiation. Nature (London) 282, 308-3 10. Weichsel, M. E. (1974). Glucocorticoid effect upon thymidine kinase in the developing cerebellum. Pediatr. Res. 8, 843-847. Weisbard, C., & Goy, R. W. (1976). Effects of parturition and group composition on competitive drinking order in stumptail macaques (Mucaca arctoidrs). Folia Prirnurol. 25, 95-121. Weisz, I., & Ward, I . L. (1979). Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses. and neonatal offspring. Endocrinology 106, 306-3 16. White, L. E., & Hinde, R . A . (1975). Some factors influencing mother-infant relations in rhesus monkeys. Anirn. Brhav. 23, 527-542. Whiting, B . , and Edwards, C. P. (1973). A cross-cultural analysis of sex differences in the behavior of children aged three to eleven. J . Soc. Psvchol. 91, 171-188. Whiting, B. B., & Whiting, J . W. M. (1974). Childrcw q f s i x culrures: A psvchoculturul unalysis. Cambridge, MA: Harvard Univ. Press. Wolff, P. H. (1966). The causes, controls. and organization of behavior in the neonate. Psycho/. Issues 5 , Monogr. 17. Wolfheim, J. H . (1977). Sex differences in behavior in a group of captive juvenile talapoin monkeys (Miopirhrcus takapoiti). Brhavinur 63, 1 10- 128. Yaniada, M. (1963). A study of blood relationships in the natural society of the Japanese monkey. Primates 4, 43-65.

ADVANCES IN THE STUDY OF BEHAVIOR. VOL I S

On the Functions of Play and Its Role in Behavioral Development PAULMARTINAND T. M . CARO SUB-DEPARTMENT OF ANIMAL BEHAVIOUR UNIVERSITY OF CAMBRIDGE CAMBRIDGE, ENGLAND

I.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Defining P l a y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Existing Evidence Concerning the Functions of Play . . . . . . . . . . . . . . . . . . . A. Experimental Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B . Correlational Studies.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Optimal Design Studies . . . . . . . . . . . . . . . . . . . ......... D. Human Play . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .......................... IV. Play May Have No Major Benefits A. The Costs and Benefits of P l a y . . . . . . . . . . . . . . . . . . . . . . . . . . . . B . The Lability of Play . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Adult Play . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Theoretical Problems in Detecting the Benefits of Play . . . . . . . . . . . . . . . . . A. Short-Term versus Long-Term Effects of P l a y . . . . . . . . . . . . . . . . . . . . B . Equifinality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Nonequivalence.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Nonspecificity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. Threshold Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F. Interactions between Developmental Determinants. . . . . VI. Methodological Issucs . . . . . . . . . . . . .................... A. Confounding Variables. . . . . . . . . . . . . . . . . . . . . . . . . . . B. Choosing Outcome Variables. . . . . . ...................... VII. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ............................................. 11.

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INTRODUCTION

The biological functions and evolutionary origins of animal play behavior are issues which generate considerable debate, yet both remain shrouded in uncertainty (for recent general reviews, see Bekoff & Byers, 1981; Fagen, 1981; Smith, 1982). In this respect play is not unique among behavioral research topics. Play does, however, merit particular attention for at least two reasons. 59

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First, play is predominantly a characteristic of young, developing animals rather than of adults and is widely believed to have an important role in the assembly of adult behavior. Thus, play may be of particular relevance to understanding some of the processes of mammalian behavioral development. Second, play holds a particular fascination for those interested in the biological functions of behavior patterns, that is, in answering the question, “What is it for?” Quite simply, the functions of play behavior are not known. Biologists generally assume that for a behavior pattern to have evolved and be maintained by natural selection, it must have biological benefits which, on average, outweigh its costs. Speculation as to the possible function’ of play behavior has been wide-ranging and inventive. One review (Baldwin & Baldwin, 1977) lists 30 functions that have variously been ascribed to play. Although there exists a wealth of descriptive information about play, there have, unfortunately, been very few direct empirical tests of any functional hypothesis. Furthermore, as we shall argue here, the experiments that have been carried out have generally failed to support any of the hypotheses. Thus, the contributions which play presumably makes to an individual’s survival and reproduction remain at present the subject of guesswork and speculation. It is our goal to review the limited empirical evidence concerning the functions of play and to suggest some possible reasons, both theoretical and methodologi‘Some confusion surrounds the termfunction as it is variously used by biologists and psychologists (Hinde, 1975, 1982; Clutton-Brock, 1981; Lewin, 1982). By function, we mean the particular consequences of a behavior pattern which currently increase the individual’s chances of survival and reproduction in the natural environment and upon which natural selection acts to maintain that behavior pattern. Not all consequences of a behavior pattern constitute functions sensu srricto. For example, one consequence of incubating an egg is that the egg shell becomes warm and expands slightly, but it would be misleading to regard this as afunction of incubation (Tinbergen, cited by Hinde, 1982, p.102). It is often extremely difficult to distinguish between a function (sensu stricto) and an incidental benefit of a behavior pattern. The distinction frequently relies on little more than plausibility. Thus, in this article we generally refer to the benefits or beneficial effects of play, although the implication is that beneficial effects of major importance, and for which play has the appropriate structural characteristics or “design features,” are likely to constitute its functions (sensu stricro). Since selection may act on more than one consequence of a behavior pattern and all behavior patterns have multiple consequences. A separate point is that selection may currently be acting on different consequences from those for which the behavior pattern was originally selected. In other words, its function(s) may have changed during the course of evolutionary history. Could and Vrba (1982) have proposed the term exuptation (in contradistinction to adaptation) for any phenotypic character which did not originally evolve through natural selection for its current role, but which has subsequently been “co-opted” and now helps to maximize inclusive fitness in a new manner. As Could and Vrba point out, it is crucial that we distinguish the current utility (function) of a phenotypic character from its historical genesis (evolution) (see also Lewin, 1982; Caro, 1984). Thus, for example, play behavior in the higher primates might originally have evolved because of one set of beneficial effects-say , the physical exercise effect-but is currently maintained by selection for a different set of benefits-say, the acquisition of complex social or cognitive skills. Benefits of play in this article refer only to current utility and not to historical origin.

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cal, why evidence in support of functional hypotheses has not been forthcoming. In addition, we shall describe certain assumptions about play which pervade the biological literature, for example, that early play experience is crucial for normal development and that play is a very “costly” activity and so must have major benefits. We shall argue that these assumptions are mostly without empirical support and reflect an underlying (and usually unstated) view of behavioral development that is highly questionable. First, though, we shall address the question of what is actually meant by the term play. Confusion about the definition of play reflects an even greater confusion in the way play is thought about. As such, the issue of definition needs to be tackled. Criticisms of current explanations of play are presented here in a constructive spirit, in the hope that they will provoke further enquiry and not in an attempt to relegate play to the status of a wastebasket category or to treat it as a functionless epiphenomenon. Play remains a biological enigma which demands closer scrutiny.

11.

DEFINING PLAY

Attempting to define play-once a popular pastime engendering much heated debate-has become unfashionable, despite a marked failure to reach any consensus. Many biologists, including Lorenz (1956), Hinde (1970, 1974), and E. 0. Wilson (1975), have repeatedly pointed to the immense problems surrounding the notion of play. Yet most contemporary workers shun the issue of definition, taking the pragmatic line that it is possible to study play empirically without a satisfactory definition (e.g., Gentry, 1974; Byers, 1977; Chalmers, 1980). There is certainly some sense in the attitude that semantic quibbling alone will not advance our understanding of behavior, and the present authors agree with Kenneth Craik’s (1943) assertion that “the final road to progress will lie not in the search for analytical exactitude in verbal definition but in the self-validatory procedure of experiment and hypothesis. Nonetheless, confusion over the meaning of the term play is so profound that the problem should not be dismissed merely because semantic issues are unfashionable. A definition is, after all, a distillation of current understanding, so an inability to define play must cast considerable doubt on the degree to which it is understood. Because of this, we shall briefly describe some of the problems surrounding the definition of play and propose a definition which we believe reflects current understanding. Failing to define play has often led to its being applied in such a broad sense as to be meaningless. The word play is frequently used, with no further clarification, as a blanket term to describe a wide range of juvenile behavior, as though its meaning were self-evident. Indeed, the term is sometimes used so loosely that ”

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it would appear as though play is the on/y thing that young mammals do. As such, it is hardly surprising that play has become the sine qua non of mammalian behavioral development as far as some writers are concerned and that statements to the effect that play is essential for normal development abound in the literature.2 Clearly, if play is to have any practical use as a behavioral category, its meaning must be restricted to something more specific than “all juvenile behavior.” One factor contributing to the emphasis on the importance of play has undoubtedly been the widespread tendency to confound play-in some restricted sense-with other forms of early experience. Certain general properties of play behavior are widely recognized, for example, the use of motor patterns from several serious functional contexts; exaggeration and repetition of motor acts; and the reordering of behavioral sequences (Loizos, 1967; Hinde, 1970; Fagen, 1981; Bekoff, 1984). In addition, many other criteria-functional, structural, and motivational-have variously been used to typify play: for example, play is “fun”; play occurs only when all basic needs are satisfied and the animal is “relaxed”; sequences of motor acts are incomplete and fragmented; role reversal and self-handicapping occur; and specific “play signals” are present (Loizos, 1967; Bekoff, 1976b; Bekoff & Byers, 1981; see Fagen, 1981, Ch. 2). However, no single characteristic from this list is either necessary or sufficient to define play, so play is polythetically defined. That is, a large proportion of these characteristic properties may be shared by various examples of play, but no single property defines the class “play” (Sokal, 1974). Furthermore, it is uncertain whether play actually has these proposed characteristic properties in many cases. In their study of coyotes, for example, Hill and Bekoff (1977) found that motor acts were actually less exaggerated (in terms of duration) and more stereotyped when performed during social play than during serious agonistic encounters. Henry and Herrero (1974) similarly found little evidence for exaggeration of movements in the social play of bear cubs. There is, however, considerable evidence that play is a spontaneous and rewarding activity with its own motivation and that it does not result merely from the absence of motivation to perform other behavior patterns (e.g., Humphreys & Einon, 1981; Martin & Bateson, 1985; Rasa, 1984). 2We shall give only two examples, referring to the importance of play in human development. Fagen (1981, p. viii) quotes the following statement from the First National Conference on the Vital Role of Play in Learning, Development, and Survival, held in Washington, DC in 1979: “Play is vital to the healthy development of all so-called higher animals. Play is a biological imperative. Play heals, naturally and as a tool in psychotherapy with children. Play for your life: the stakes are survival.” A less lurid example is the following passage from a British government document. cited by Smith (1982): “The realisation that play is essential to development has slowly but surely permeated our educational system and cultural heritage.” Both passages, though overstatements given the paucity of our current knowledge about play, do represent a widely held opinion about the importance of play, for which biological research is often cited as support.

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Most definitions of play can themselves be classified as either functional or structural in nature: the former being concerned with the consequences of play, the latter with its physical form and appearance (Fagen, 1974). Definitions based specifically on function are not possible at present because the functions of play are not known. Play is not a general class of behavior that can readily be defined by some obvious consequence in the way that, for example, aggression, communication, mating, or feeding behavior can be distinguished. Equally, as Bekoff and Byers (198 1) and others have pointed out, definitions of play based solely on its structure are invariably weak because of the immense diversity of motor patterns that are commonly classified as play in various species (see also Bekoff, 1984). Even when discussion is restricted to a single species, a purely structural definition is inadequate if (as is generally the case) it fails to distinguish playful motor patterns from the same motor patterns performed seriously (that is, with their normal functional consequences). This is a distinction which observers can, in practice, usually recognize. Many empirical papers that describe play in a particular species simply list a variety of structurally defined motor patterns under the rubric play but give no explanation as to why these particular motor patterns were called play in the first place (e.g., West, 1974; Gard & Meier, 1977; Guyot, Bennett, & Cross, 1980; Bateson, Martin, & Young, 1981; Davies & Kemble, 1983). In some cases, playful and serious behavior can be given the same structural definitions. For example, children’s rough-and-tumble play draws on the same repertoire of motor patterns as serious aggressive fighting-yet the two can readily be distinguished in young children (Humphreys & Smith, 1984). In an account of social and predatory behavior in cats, Car0 ( 1979) defined several motor patterns in terms of their structure and referred to these as predatory behavior when they were directed in an apparently serious manner at prey. When directed at other cats, though, the same motor patterns were called play, without further explanation. In their study of coyotes, Vincent and Bekoff (1978) also used the same structural definitions for prey-killing actions which occurred both during play and during agonistic interactions. Schaller (1972, p. 165) similarly comments that the predatory behavior and the play of lions are indistinguishable in terms of the motor patterns involved. The point here is that predatory behavior is readily distinguished by its obvious consequences-catching and killing prey-even when these are not explicitly stated. No such obvious consequences distinguish play, however. In fact, the unstated hallmark of play in these examples (and, we suspect, in most other cases) is its very luck of obvious consequences. In other words, the motor patterns were called play because they did not result in the usual consequences of biting injuriously or killing. It is rare for play to be defined explicitly in terms of its consequences or lack of consequences. Some empirical papers include an admission that the standard

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structural definitions are not in themselves wholly adequate. For example, Barrett and Bateson (1978) defined several categories of play behavior in terms of the structure of the constituent motor acts, using the criteria suggested by Loizos (1967), but they added that “to a large extent we had to rely on contextual cues.” An exception to this rule was Biben’s (1979) criterion for distinguishing when cats were playing with prey. Behavior was classified as play when prey was actively approached or manipulated, but not injured. Play was, therefore, explicitly contrasted with the same motor patterns performed seriously (predation) and defined by its lack of functional consequences. Finally, some definitions of play, whether functional or structural, can be dismissed immediately because they are recursive, that is, the thing to be defined (play) is itself used in the definition. Some definitions of play, regrettably, boil down to little more than statements that “play is playful behavior.” Despite these problems with defining play, humans clearly can and do recognize when an animal is playing. Moreover, there is usually a reasonably high level of agreement between different observers about when play is occurring (e.g., Caro, Roper, Young, & Dank, 1979; Guyot et al., 1980; Rasa, 1984; see Fagen, 1981, p. 5 1). It would obviously be foolish to deny the existence of play simply because it cannot be defined. Yet what is it that enables an observer to be confident that an animal is playing? It cannot be just the structural characteristics of the motor acts because the same motor patterns may also be called “serious” behavior. Rather, the distinguishing feature of play seems to be the subjective sense on the part of the observer that the behavior lacks any obvious purpose or immediate benefit (see Schlosberg, 1947; Hinde, 1970; Symons, 1978; Bekoff & Byers, 1981; Smith, 1982). Perhaps one reason why the most obvious characteristic of play-its apparent lack of purpose-is often ignored is that it appears to generate a paradox. On the one hand, motor patterns are called play because they appear to have no obvious purpose or immediate benefits. On the other hand, biologists assume that animals do not do something unless (on average) the overall benefits of this behavior exceed its costs. Hence, there is a superficial contradiction between the notion that play has no obvious benefits (otherwise it would not be called play) and the evolutionary logic which requires that play must have benefits which exceed its costs. This apparent paradox is made to seem more compelling if it is also assumed that the costs of play (and therefore its benefits) must be very large-an assumption that is widespread, but, as we shall argue later, probably wrong. One way of reconciling these apparently contradictory statements is to assert that play does have benefits but that these are delayed in ontogeny and accrue to the adult. The notion of delayed benefits is central to all functional theories which see play as a form of training and may explain their popularity. Yet the contradiction between the axiom that play has benefits which exceed its costs and the notion that play has no obvious benefits vanishes if two points are recognized. First,

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play may not have large costs and so may have only small benefits. Second, the notion that play has no obvious benefits involves a subjective interpretation on the part of the observer; in other words, the emphasis should be on the word obvious rather than on the word no. Our suggestion is, then, that play has a variety of benefits-some or all of which might be immediate-but that these benefits may be small and so not easily detectable. Thus, play appears to an observer to be without any obvious benefits or purpose, in specific contrast to “serious” behavior, whose consequences are obvious. This view is incorporated in the following definition, which is a modified version of the definition proposed by Bekoff and Byers ( 198I): Play is all locomotor activity performed postnatally that uppeurs to an observer to have no obvious immediate benefits for the player, in which motor patterns resembling those used in serious functional contexts may be used in modified forms. The motor acts constituting play have some or all of the following structural features: exaggeration of movements, repetition of motor acts, and fragmentation or disordering of sequences of motor acts. Social play refers to play directed at conspecifics; object play refers to play directed at inanimate objects: locomotor play refers to apparently spontaneous movements which carry the individual about its environment; and predatory play refers to play directed toward living or dead prey.

A final point concerns the possible heterogeneity of the category “play.” It seems increasingly likely that in many cases play will prove to be heterogeneous in terms of its evolution, function, development, and proximate causation. Thus, it may be misleading to refer to play as though it were a single, unitary phenomenon. Play may have more than one function in a particular species, for example, and different aspects of play (such as social, object, and locomotor play) may have separate motivations, different developmental courses, and different evolutionary origins. For example, Barrett and Bateson (1978) found that the play of domestic kittens changes markedly around the end of weaning, when social play starts to decline and object play increases sharply. Correlations between different measures of play also break down at the end of the weaning period. Moreover, some aspects of social play, such as pawing and biting, become increasingly associated with predatory behavior in older kittens, whereas other aspects, such as arching and chasing, become dissociated from predatory measures (Caro, 1981 ) . One suggestion here is that play becomes differentiated at around the end of weaning, with different aspects of play coming under the control of different types of serious behavior such as predation and intraspecific aggression. It is widely reported that rough-and-tumble social play in humans and other species becomes increasingly difficult to distinguish from genuine aggression later in ontogeny (e.g., Aldis, 1975; Caro, 1981; Humphreys & Smith, 1984; Martin, 1984a). Cluster analysis indicates that in rhesus macaques, social play is actually

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composed of at least five temporally distinct types of behavior (Smith & Fraser, 1978). Chalmers (1980) has also suggested that the play of olive baboons can be dissociated into at least two distinct components, each with its own underlying control mechanisms. In conclusion, although empirical evidence for the heterogeneity of play at various levels (function, evolution, causation, and development) is limited, the issue is certainly worth considering.

EVIDENCE CONCERNING THEFUNCTIONS OF PLAY 111. EXISTING Many different hypotheses have been advanced concerning the biological functions of play in different species, including the provision of physical exercise (Brownlee, 1954; Fagen, 1976), various aspects of socialization and the acquisition of social skills (Dolhinow & Bishop, 1970; Poirier & Smith, 1974), and even the learning of mothering skills (Lancaster, 1971). Bekoff and Byers (1981) have distilled the many hypotheses into three main classes: play as motor training, play as socialization, and play as cognitive or sensorimotor training. All have in common the notion that, as a result of playing when young, the individual is better able to perform some form of serious behavior later in ontogeny. In essence, play is seen as a specific developmental determinant (Bateson, 1976a) of adult behavior. For example, it is commonly held that the principal function of play in young carnivores is to develop adult predatory abilities (e.g., Egan, 1976; Leyhausen, 1979; Moelk, 1979; see Martin, 1984a). This can be tested empirically by investigating the relations between early play experience and the relevant serious behavior patterns (in this case, predatory skills) later in ontogeny. We shall refer to the serious behavior patterns, of which play is thought to be a developmental determinant, as the “outcome variables” in any test of a functional hypothesis. Three major lines of approach have been taken in empirical studies of play (see Byers, 1977; Chalmers & Locke-Haydon, 1984): ( I ) experimental manipulation of early play experience; for example, to give fewer or more opportunities for particular types of play; (2) searching for correlations between play and other forms of behavior, exploiting natural variation within populations; and (3) using the indirect “argument from design” approach, in which the observed structure of play is matched against the requirements of its hypothesized function (“Can it do the job?”). We shall refer to these three approaches as experimental, correlational, and optimal design studies. Clearly, evidence from experimental studies is generally more compelling than that from correlational or optimal design studies. We shall also distinguish between two levels of evidence:(l) studies in which a particular hypothesis was explicitly stated and where the evidence could have refuted the hypothesis (the criterion of falsifiability); and (2) studies in which indirect or circumstantial evidence that is relevant to a particular hypoth-

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esis is obtained but cannot conclusively refute the hypothesis or enable the investigators to choose between alternative hypotheses. Most evidence in the current play literature is, unfortunately, in the second category, although we shall concentrate here on the first. A.

EXPERIMENTAL STUDIES

Possibly the earliest experimental test of a play hypothesis was that of Thomas and Schaller (1954), who used the “Kaspar Hauser” isolation-rearing technique with domestic cats. The hypothesis was that play in cats serves as practice for prey-catching motor patterns. Kittens were raised from birth under conditions of both social isolation and visual deprivation (they were either fitted with translucent goggles or raised in a visually barren enclosure). The deprived cats therefore lacked, among many other things, the opportunities for both social play and visually guided object play throughout their early development. The Kaspar Hauser cats and their normally reared siblings were compared, when 1 1 weeks old, on the basis of their ability to exhibit the species-typical prey-catching movements, as elicited by a moving dummy mouse. Thomas and Schaller reported that the isolation-reared cats exhibited the typical prey-catching movements-fixating; lying in wait; jumping at, biting, and clasping the dummy-in the same way as their normally reared siblings. However, the account was without detail and no quantitative evidence was provided in support of this statement. Clearly, an anecdotal report based on a crude deprivation experiment must be treated with considerable caution. It is likely that the Kaspar Hauser cats would, if tested, have exhibited numerous subtle differences in behavior, and it remains uncertain whether they could have used the typical prey-catching movements in the correct context and sequence and with the same degree of skill as normally reared cats. We can, however, conclude that play experience during the first I 1 weeks of life is not necessury for the development of at least the basic prey-catching movements in cats. In an unpublished study, Hopf (1972, cited by Baldwin & Baldwin, 1974) also reported that social play is not essential for “normal development” in squirrel monkeys. Infants raised in laboratory environments without peers showed “no marked differences” from animals raised with peers. These results are in line with a general finding that most of the basic motor patterns forming an animal’s behavioral repertoire can develop normally in social isolates (Marler, 1975). Play may not be necessary for the rudiments of normal behavior to develop, but it might nonetheless improve those skills which are already developing. Such is the tenor of most modern functional theories of play. The issue of whether object play experience quantitatively improves adult predatory skills in domestic cats has been addressed in one experimental study (Caro, 1980a). Eleven kittens between 4 and I2 weeks after birth were repeatedly given the opportunity to play

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with toys. Kittens were given a total of 34 exposures to the toys, each lasting 30 or 40 min. These object-playing (OP) kittens were reared with their mothers and littermates and so had unlimited opportunities for social play. Eight control ( C ) kittens were also reared with their mothers and littermates but never received any opportunities for object play with toys. All the kittens were individually tested, when they were 6 months old, on their ability to catch and kill four different types of live prey. A fine-grained analysis of the cats’ predatory behavior was used: 13 different categories of predatory motor patterns (Caro, 1979) were recorded, from which 25 different frequency and latency measures were derived. Car0 compared the OP kittens with the controls on each of the 25 predatory measures for each of the four prey types. Of the 100 comparisons made between the OP and C kittens, only five were significantly different, that is, no more than would be expected by chance. Moreover, these few differences were not clustered in any meaningful way and were not consistent across prey type. Object play did not appear to make any quantitative difference to the development of adult predation. Caro (1980a) has discussed some of the many possible reasons why no relation was found between prey-catching behavior and play in this experiment (see also Martin, 1984a). For example, both groups had opportunities for social play and this may have compensated for the lack of object play; both groups had opportunities for locomotor play; the control cats may have had some object play experience with wood shavings or other unintended toys in their home pen; kittens may need only a minimal amount of object play experience to become competent predators and the controls may already have attained this level; the tests used to assess prey-catching skills may not have been sufficiently sensitive or demanding; inappropriate measures of predatory skill may have been used; the OP kittens may have received too little object play experience or the wrong type of toys for any improvement in their predatory skills to have occurred. However, the most reasonable interpretation of Caro’s results is that playing with objects when young does not significantly affect a cat’s ability to catch and dispatch prey when adult. The third experimental study we shall describe (Einon, Morgan, & Kibbler, 1978) did find evidence for some differences between animals whose previous play opportunities had differed. However, its results are somewhat difficult to interpret for our present purpose since the study was not aimed at testing a particular functional hypothesis about play. Rats raised in social isolation subsequently behave differently in many respects compared with those raised socially (e.g., Einon & Morgan, 1977). In open-field tests of behavior, for example, their locomotor activity and rate of object contact are slower to habituate. Partial isolate (PI) rats, which are allowed 1 hour of social contact per day, are intermediate in their behavior between socially reared rats and those raised in complete isolation. Einon et al. (1978)

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used drugged social play-partners, which had been injected with chlorpromazine or amphetamine, in order to manipulate the quality of social play experienced by PI rats. When subsequently tested in the open field, PI rats which had interacted with drugged rats behaved more like complete isolates than those which had played with undrugged partners. In other words, the qualiry of social interaction was important as far as later differences in behavior were concerned. Of course, the drugged partners were presumably different in many respects, as Einon et a1. point out, so more than just social play experience was altered for the experimental rats. Nonetheless, this study does offer strong (though not conclusive) evidence for some relations between early social play experience and later behavior. Unfortunately, the use of open-field outcome measures makes it difficult to relate these results to most conventional hypotheses about the functions of play, except the behavioral flexibility hypothesis (Einon et al., 1978; Fagen, 1982; see Section V1,B).

B.

CORRELATIONAL STUDIES

The possible connection between play and behavioral skills has also been investigated in three correlational studies (Vincent & Bekoff, 1978; Davies & Kemble, 1983; Chalmers & Locke-Haydon, 19841, all of which failed to find any strong relation between the two. In a study of coyotes, Vincent and Bekoff (1978) recorded the frequency of social play patterns directed toward littermates by each of the four pups from a single litter. Play was observed between 20 and 34 days after birth. Shortly after this (35-45 days after birth), the predatory ability of each pup was assessed by giving it ten 10-min trials, during each of which a live adult mouse was presented. Predatory success was measured as the percentage of trials in which the prey was killed. Vincent and Bekoff found no correlation between the frequency of play behavior and subsequent predatory success: the pup which had played most was not the most successful predator. Although consistent with Caro’s (1980a) findings, the results of this study are far from conclusive for a number of reasons. The sample size (four pups) was very small, and significant correlations might well have emerged if more animals had been studied. Clearly, it is wrong to place much weight on a negative finding unless the test was adequate to find an effect. Second, a correlational approach was used which exploited natural variation in the independent variable (play), so there is a possibility that other factors might also have been involved. Third, the outcome variable (percentage success in killing prey) was a relatively crude measure of predatory skill and was unlikely to have picked up any subtle differences in the pups’ abilities. Fourth, the pups’ predatory skills were tested only a few days after their play had been studied, while they were still young, so the study did not actually assess the relation between play and adult predatory skills. Possible benefits of play may not

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emerge until later in ontogeny. Despite all these criticisms, though, Vincent and Bekoff‘s study did at least indicate that individual differences in play experience had no major effect on the ability of coyote pups to kill prey. Davies and Kemble (1983) performed a similar correlational study with northe m grasshopper mice. Twenty-nine mice from seven different litters were raised in social groups, and various measures of their social play behavior were recorded between 27 and 61 days of age. Following this (at 68-7 1 days), predatory behavior was assessed by presenting the mice with live crickets on eight occasions. The mice were tested as groups (which raises problems of interpretation regarding the independence of their behavior), and individuals’ predatory success was measured as the number of crickets killed. No relation was found between any measure of play behavior and predatory behavior. Most of the criticisms leveled at Vincent and Bekoff‘s (1978) study apply in this case as well. In addition, it would seem that the predatory success of groups, rather than individual mice, was actually being tested. Littermates are known to behave more like one another than like members of another litter (e.g., Barrett & Bateson, 1978, for play in cats), and a more appropriate approach might be to study differences between litters rather than between individuals (Abbey & Howard, 1973). Nonetheless, much the same conclusion may be drawn from this study, namely, that there appeared to be no discernible relation between individual differences in social play experience and predatory success in this species. More recently, Chalmers and Locke-Haydon (1984) have reported the results of a detailed correlational study which analyzed the relations between social play and the development of sensorimotor and social skills in captive infant marmosets. Skills were generally defined as any behavior that helped the infant to gain a desirable resource, location, interaction, or goal (or to avoid an undesirable one). Many specific outcome measures of skill were recorded, including the infant’s ability to take food from others and resist having its own food taken; its success in attempting to climb onto parents and older siblings; and its ability to reach a food reward through a narrow aperture or over a moving obstacle. Skill outcome measures were recorded at 4-week intervals from 6 to 22 weeks of age inclusive, and various play measures were recorded during the intervening periods. The results were analyzed by searching for correlations between skills (or improvements in skills) at one age and the amount of play performed at earlier ages. Most of the many correlations that were calculated did not differ significantly from zero. The authors commented that “a major feature of our results is the absence of correlations between many measures of social play and skills. Some skills were significantly correlated only with nonplay behavior, and only one outcome measure (taking food from the mother) correlated significantly and exclusively with play. Nonetheless, there were some associations between play and certain outcome ”

TABLE I SUMMARY OF EXPERIMENTAL A N D CORRELATIONAL STUDIES(NONHUMAN) DISCUSSED I N THE TEXT ~

~~~~

~

~

~~

~

Sample size"

Type of play

~

Age play measured

Study

Species

Thomas and Schaller

Domestic cat (Felis curus. captive)

10 ( 6 E + 4 C)

Object (t Social)

Caro (1980a)

Domestic cat (Felis cums. captive)

19 ( I 1 OP + 8CI

Object

4- I 2 weeks

Einon CI ul. (1978)

Hooded rat (Rairus nor\,egicu.\; captive females)

30- I05 (total)

Social

23-45 days

Vincent and Bekoff (1978)

Coyote (Canis lununs; captive)

4 ( I litter)

Social

20-34 days

Daviea and Kemble

29 ( 7 litters) Northern grasshopper mouse ( 0ti~chornv.v Ii~uc~o~us~er.: captive) 10 (from 3 Common martamilies) moset (Cull-

Social

27-6 I day\

Social

6-22 weeks

(1954)

~~

Outcome variables

Experimental studies 0- II weeks Predatory behavior (response to moving dummy mouse) Predatory behavior (25 measures of 13 motor patterns; 4 types of prey) Open field (habituation of object contact and locomotion)

~~

~

~~~

Age 0 . V . measured

Hypothesis

I I weeks

Motor training

6 months

Motor training

45- I20 days

Behavioral flexibility

Results

Kaspar Hauser cats showed "normal" predatory movements No difference in predatory behavior between OP and C kittens Quality of social interactions was important

Correlational studies

(1983)

Chalmera and LocheHaydon (1984)

i0it-i.t ,jucchii.\ jucckio ; captive

"E. Experimental. C. control: OP, object-playing

Prey-killing success ( % of 10 x 10-niin trials in which adult mouse killed) Predatory behavior (latency to kill cricket: 8 trials: tested as a group)

Sensorimotor and social skills

35-45 days

Motor training

68-7 I days

Motor training

6-22 weeks

Practice (skill development)

N o correlation between prey-killing success and play frequency No relation between any play measure and predation

Few correlations between play and skill measures: no evidence for delayed benefits

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measures. Specifically, sociai play at 11-13 weeks of age was significantly correlated with performance at 14 weeks, both in a competitive food test with the mother and in negotiating a moving obstacle to obtain food. In discussing these correlations, Chalmers and Locke-Haydon pointed to two plausible alternatives to the most obvious interpretation-that play serves to practice these skills. These are, first, that the skills serve to promote play (rather than vice versa) and, second, that play and skills are functionally unrelated but simply share some common causal mechanisms. A striking feature of these results was that all significant correlations between play and skill measures were restricted to the same age period, from I 1 to 14 weeks after birth. There were no correlations, for example, between play during this period and any skills later in development (at 22 weeks). As the authors concluded, “There is thus little evidence to support the hypothesis that the promotional effects of play on skill development are delayed, at least across the age range used in this study.” On the contrary, the results suggest that any effects which play might have on skills are short term rather than delayed until adulthood as the practice hypothesis suggests.

C. OPTIMAL DESIGNSTUDIES A third, and less direct, approach to investigating functional hypotheses about play is the optimal design approach, that is, to observe whether the form or structure of play is consistent with its proposed function (“Can it do the job’?’’). Byers (1977) employed this method to test the hypothesis that the play of ibex kids serves as practice for the locomotor skills which they presumably need as adults in order to negotiate steeply sloped terrain. The specific prediction tested was that locomotor play patterns should occur mainly on sloped (as opposed to flat) surfaces, when both were available. Observations of ibex kids in a zoo confirmed that some forms of locomotor play did indeed occur more often on sloping terrain, in line with the motor training hypothesis. Taking a similar approach, Symons (1974) discussed the hypothesis that aggressive social play (play-fighting and play-chasing) in rhesus monkeys serves to learn, refine, or practice agonistic communication skills. (The improvement of communication skills has frequently been suggested as a function of play in primates, e.g., Mason, 1965; Jolly, 1972.) Symons noted that nearly all serious agonistic interactions involve gesturing of threat and submission rather than fighting. These agonistic signals are generally absent from aggressive social play in rhesus monkeys, and furthermore, signals used during social play are not used during fighting. In addition, Symons argued, the appropriate responses to agonistic signals are absent during play. In play, for example, one individual does not consistently adopt a submissive role; rather, roles alternate. Symons concluded from this and other circumstantial evidence that aggressive social play in

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rhesus monkeys is an “unpromising candidate” as a means of practicing communications skills, and he cast doubt on the plausibility of the communication hypothesis (but see Section V,B). As with Byers’ (1977) study, evidence of this type can lend more or less support to a particular hypothesis but cannot in itself refute or demonstrate the correctness of an hypothesis. Byers’ (1977) results indicate that locomotor play in ibex kids has some of the structural properties needed to perform a particular function, but they do not demonstrate that play is necessarily performing that function. For example, the exercise hypothesis would also predict that locomotor play should preferentially occur on sloped terrain, since this would provide more opportunities for physical exercise. Optimal design studies can, however, demonstrate that a particular hypothesis is probably not correct. Thus, Symons’ argument-that aggressive social play in rhesus monkeys is unlikely to be involved solely in practicing communication skills-is a compelling one. Similar conclusions can be drawn from Schaller’s (1972, pp. 165-166) observations about the play of lion cubs, which resembles adult hunting behavior. Schaller notes that wrestling (which is the commonest motor pattern in play) is rarely used by adults, whereas stalking (an important component of hunting) is not a prominent feature of play. Another valuable source of circumstantial evidence is the comparison of play and serious behavior, either within species (for example, between sexes or populations) or between species. A good example of intraspecific comparison comes from the work of Baldwin and Baldwin (1973, 1974), who studied the exploratory behavior, play, and social interactions of squirrel monkeys in a variety of natural environments. Baldwin and Baldwin (1974) reported that both the frequency and form of social play varied enormously between different populations of squirrel monkeys, with play accounting for anything from 0 to 3 hr per day of young monkeys’ time. In one population living in Panama, no social play whatsoever was observed during 261 hr of observation over a 10-week period. The monkeys at this site spent 95% of their waking time foraging or traveling, leaving little time for play. Despite this, their social behavior appeared normal, and the troop was cohesive and stable. As the Baldwins (1974, p.314) noted, these observations suggest that “social organization and many normal social behaviors can develop in squirrel monkeys without social play,” although play might improve the competence with which they are performed. Evidence such as this, like the results of laboratory deprivation experiments, demonstrates that an adaptive modicum of competence can develop in the absence of play, but it usually leaves open the possibility that play may subtly improve certain skills. Only through fine-grained experimental studies, such as Caro’s (1980a), can this second possibility be investigated. In a study of two canid species, Biben (1982a) found that interspecific differences in juvenile play could be related to the species’ different treatments of

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prey when adult. Crab-eating foxes hunt individually and engage in extensive solitary object play when young, whereas bush dogs (which hunt cooperatively in social groups) show little object play and share, rather than compete for, objects when young. Similarly, sex differences in play can be compared with sex differences in adult behavior. For example, young male ferrets perform more neck-bites during play and are also more aggressive than females when adult (Biben, 1982b). The existence of such interspecific or intraspecific differences in juvenile play that correspond to differences in adult behavior is certainly consistent with the practice hypothesis of play but by no means constitutes strong evidence in its support (Caro & Alawi, 1985). Various factors might commonly affect both juvenile play and adult behavior even if there is no direct relation between the two. For example, males might be more aggressive than females throughout life for a variety of reasons, irrespective of whether play functions as practice for adult aggression. Equally, some features of social organization (such as social versus solitary living) will be exhibited both in juvenile play and adult behavior whether or not the two are directly related. Animals might simply behave socially throughout life, for example, even if play has no long-term benefits. All of the studies described so far addressed the issue of whether play is a specific developmental determinant of one type of adult behavior (for example, predation or communication skills). A different sort of hypothesis, originally formulated by Brownlee (1954), is that rather than providing training for one particular form of adult behavior, play has a generally beneficial effect by improving the efficiency of skeletal muscles and the cardiopulmonary system. This is the exercise hypothesis of play, which essentially proposes that play enhances an individual’s Darwinian fitness by improving its physical fitness. The exercise hypothesis has been discussed in detail by Fagen (1976), who is a notable and rare proponent of the hypothetico-deductive method in play research. Fagen formulated a list of specific and empirically testable predictions stemming from the exercise hypothesis, one of which has been tested empirically (McDonald, 1977). The maximum physiological training effect of physical exercise occurs when muscles are exercised near to fatigue. Hence, if play serves to exercise muscles then, Fagen argues, bouts of play should last long enough to exercise muscles near to fatigue (but no longer) and the duration of play bouts should follow a nonrandom statistical distribution. To test this prediction, McDonald (1977) recorded the duration of 127 bouts of social play in young California ground squirrels under natural conditions and analyzed their distribution using a log-survivorship technique. The results did not support the exercise hypothesis. Bout durations followed a simple exponential decay model, a finding suggesting that the duration of play bouts was under the control of random events. McDonald’s finding does not, of course, constitute a conclusive falsification of the exercise hypothesis. Only one of its many predictions was tested for

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only one species, and the assumptions behind the test may themselves have been wrong.

D.

HUMANPLAY

The play behavior of children has been studied extensively. Before subsuming evidence from studies of human play into our main argument, however, we should first sound a strong note of caution. Glib generalizations about human nature based on dubious evidence from other species are rightly censured, and the converse should be no less true. There are likely to be profound differences between human play and that of other mammals, in its form, control, development, and consequences. Indeed, the differences between humans and other mammals may often be more informative than the similarities (Hinde, 1974). For example, no obvious parallels exist between the linguistic, fantasy, and sociodramatic play of children and play in other species (Smith, 1983). As a result, most hypotheses about the effects of human play (as opposed to biological functions, senm stricto) are qualitatively different from those applied to play in other species. Notwithstanding these problems, the study of play in humans can and should be related, where possible, to our knowledge of play in other mammals. One commonly espoused hypothesis about play in human infants is that it aids creative thinking and behavioral flexibility (e.g., Piaget, 1962, p. 155; SuttonSmith, 1967). This hypothesis is actually of considerable relevance to animal studies because play is often held to be a source of novel and innovative behavior in nonhuman species (see Fagen, 1981, 1982). Another common hypothesis is that children’s play aids problem solving and, once again, parallels exist with phenomena observed in other species. Numerous experimental studies have tested hypotheses about play in humans, with mixed results (e.g., Pepler & Ross, 1981; Vandenberg, 1981; Cheyne & Rubin, 1983; reviewed by Smith & Simon, 1984), although we shall only outline two representative studies here. Dansky and Silverman (1973, 1975) investigated the notion that object play in children is related to their ability to name novel uses for these objects, or “associative fluency” (a measure of creative or divergent thinking). Thirty nursery school children were individually allowed to play freely with a variety of objects for a 10-min period. Thirty different children were given the same objects for 10 min and told to use them in an imitative manner, copying an adult experimenter. Finally, 30 controls were given a “neutral experience” not involving the objects for 10 min. Immediately following the 10-min period, all children were individually tested on their associative fluency using an alternative uses test, in which the child was asked to name as many nonstandard uses for the objects as possible. The 30 children who had played with the objects immediately prior to testing had higher associative fluency scores (that is, named more

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novel uses for the objects) than children in the other two groups. In this sense, the results supported the idea that playing facilitates creative thinking immediately after the play experience. The experiment did not, however, address the issue of whether play is either necessary or beneficial for the development of creative thinking, and no conclusions can be drawn from it about the long-term effects of early individual differences in children’s play experience. As Dansky and Silverman themselves pointed out, a playful attitude engendered by the 10-min play period may have lowered the threshold for forming unusual associations during the subsequent test, but “no claim has been made regarding any increase or decrease in the actual creative ability of the children in this study.” At most, this experiment indicated that children are more likely to form unusual associations when in a playful mood, although this may, in turn, support the suggestion that play is beneficial in the development of creative thinking abilities. Another study by Sylva (1977; Sylva, Bruner, & Genova, 1976) tested the hypothesis that prior experience playing with the components of a “lure-retrieval” problem would improve a child’s subsequent ability to solve that problem. Children were given different forms of prior experience, both playful and nonplayful, with the components of a mechanical problem, which was to retrieve an object from an out-of-reach container using a tool assembled from available components (sticks and clamps). Children who had played with the sticks and clamps for 10 min prior to being tested showed more goal-directed responses, were less likely to opt out, and were better able to use hints given by an adult than children who had merely observed an adult manipulating the sticks and clamps. Prior play also tended to lead to a different style of problem solving: a “bottom-up’ ’ progression from simpler to more complete partial solutions, rather than trying immediately for a complete solution. However, prior play did not result in more spontaneous solutions to the problem, nor did children who had played solve the problem more rapidly than those who had only observed. Thus, it would be misleading to state that play improved problem-solving ability. Rather, play changed the way in which children solved the problem (see Cheyne, 1982). Subsequent studies of similar design have also failed to find clear-cut evidence for facilitatory effects of object play on children’s problem-solving abilities (e.g., Cheyne & Rubin, 1983). Just as with Dansky and Silverman’s work described earlier, Sylva’s experiment investigated only the immediate effects of a brief period of play and can tell us little about the long-term effects of early play experience on the development of other forms of behavior. Christie (1983) makes a similar point about most studies investigating the effects of “play tutoring” on children’s cognitive abilities, commenting that it is unclear whether “play tutoring truly promotes children’s cognitive development or merely results in inconsequential, short term gains in cognitive performance. The results of many experimental studies of children’s object play are ambigu”

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ous because of uncertainties of experimental design and procedure (Cheyne, 1982; Simon & Smith, 1983; Smith & Simon, 1984). In particular, when alternative-treatment (rather than no-treatment) controls have been used, significant differences have often failed to emerge. In many lure-retrieval tests of problem solving, it was not known whether the children had actually played with the objects. In addition, the effects of observer bias have not always been adequately accounted for. Indeed, when possible observer bias was controlled for, Simon and Smith (1983) were unable to replicate the findings of a previous study (Smith & Dutton, 1979) in which play experience had proved to be markedly superior to training for innovative problem solving. In common with many studies, Simon & Smith (1983) found that, in most respects, the effects of play experience did not differ from those of training directly related to the problem. Similarly, many experimental studies investigating the effects of play tutoring on children’s cognitive and linguistic skills have lacked appropriate controls, with the consequence that some apparent improvements may have resulted from increased contact with adults rather than from any specific effects of play per se (Smith, Dalgleish, & Herzmark, 1981; Christie, 1983). Where control groups have been included, few differences have been found between the effects of play tutoring and straightforward skills tutoring (Smith ef al., 1981; Christie, 1983). For convergent problem solving, certainly, play experience is not significantly more effective than comparable nonplay experiences (such as imitation or observation), although a superiority of play over nonplay has been found for some divergent problem-solving tasks (Smith & Simon, 1984). However, the relevance and importance of some of these tasks (such as the alternative uses test) are questionable, and Smith and Simon (1984) rightly point to the need for “ecologically valid” play experiences and outcome variables in such experiments (see Section VI, B). In conclusion, no consistent evidence has yet emerged to indicate that the effects of play experience on children’s problem-solving or other skills is markedly superior to the effects of other forms of experience, such as direct training (Vandenberg, 1981; Cheyne, 1982; Christie, 1983; Simon & Smith, 1983; Smith & Simon, 1984). The method used in these lure-retrieval, problem-solving studies is, interestingly, a modern variant of Kohler’s ( 1 925) classic “stick-as-rake’’ problem, which was originally used to study insightful problem solving in chimpanzees. Numerous animal studies, both with primates (e.g., chimpanzees: Birch, 1945) and with other species (e.g., polecats: Weiss-Burger, 1981; pigeons: Epstein, Kirshnit, Lanza, & Rubin, 1984) have found that animals are better able to solve a problem or perform a task if they have received prior experience (which may include play) with the elements of that task. Yet even the immediate effects of children’s play are not always beneficial, as illustrated by Hutt’s (1966) study of play and exploration in nursery school children. Hutt found that play could actually impede learning. Children were

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presented with a novel and complex object (a box with a lever that operated a bell, a buzzer, and four counters), whose properties they were allowed to investigate freely. Hutt found that the object was not incorporated into play until the child had discovered all of its salient physical properties. After this, she argued, learning was incidental. Indeed, one boy who started a game with the object after only a brief period of investigation failed completely to discover one of its major properties (the buzzer). Hutt (1966, p.76) concluded that “by being repetitive, play is by definition a highly redundant activity, and can actually prevent learning.” Similarly, in his famous study of play and mechanical problem solving in chimpanzees, Schiller ( 1957) concluded that previous play often impeded rather than facilitated problem solving. Indeed, one chimp failed to use a stick in a food-retrieval problem, even after several hours of fasting, because he was preoccupied by playing with it (Schiller, 1957, p.272). We have summarized the evidence from studies which have directly tested a functional hypothesis of play and have found little solid evidence upon which to base a conclusion about the functions of play. To explain this lack of evidence for any beneficial effects of play, we can appeal to two suggestions, which we shall discuss in turn. The first is that play does not actually have any major longterm benefits but is a facilitative developmental determinant of minor importance. The second is that the beneficial effects of play have not yet been detected for a variety of methodological and theoretical reasons. We certainly do not wish to dismiss this second possibility, and it would clearly be wrong to conclude that an absence of empirical evidence proves an absence of any benefits-particularly when so few experiments have actually been performed. Moreover, these two suggestions are not mutually exclusive. For example, play may have only minor benefits, and these have not yet been detected because of the way in which the experiments were performed.

1V. PLAYMAY HAVEN o MAJORBENEFITS Two lines of circumstantial evidence support the notion that play has relatively small benefits, and a third counters the view that play is an important developmental determinant of adult behavior. The first is the cost-benefit argument, which asserts that, contrary to prevailing dogma, play probably has relatively minor biological costs and may therefore have only minor benefits (as long as these exceed the costs). The second is the lability argument. This asserts that play is extremely sensitive to prevailing conditions and is a low-priority activity which may be suppressed or completely absent under natural conditions, implying that play is unlikely to be essential for normal development. Third, there is the often neglected point that adults of many species also play. We shall consider each of these arguments separately.

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A . THE COSTSAND BENEFITSOF PLAY One of the few generalizations about play which is widely agreed upon is that play is a very “costly” activity. It is frequently asserted that play consumes large amounts of an animal’s time and energy and may involve risk of injury, so it must be highly beneficial. Fagen (198 1, p.3 1 I ) , for example, speculates at one point about the likely consequences of a young animal devoting “95 or perhaps even 99% of its daily caloric expenditure (excluding thermoregulatory and digestive metabolism) to play.” Hinde (1974, p. 227) succinctly summarizes the view of the overwhelming majority when he writes that “play consumes so much time and energy that it must be of crucial adaptive importance in development.” (Further examples appear elsewhere.3) Certainly, in order for a behavior pattern to be maintained by natural selection it must have beneficial consequences which, on average, exceed its costs. Therefore, the axiom that play is very costly necessarily implies that play must have large benefits, otherwise animals simply would not be selected to play. Unfortunately, there is no convincing evidence that the absolute time and energy costs of play are in fact great. Indeed, the results of some recent work (Martin, 1982, 1984b) suggest quite the contrary. The terms energy and costly are used inconsistently and with a wide variety of different meanings in the behavioral literature (see Hinde, 1960; Burghardt, 1984), and it is often unclear what is actually meant by statements such as ‘‘play is energetically costly” (Martin, 1984b). One suggestion has been to define the energy cost of play (ECP) as the net daily energy expenditure (in excess of resting metabolism) that is due to play. expressed as a percentage of the total daily energy budget (Martin, ‘There is no need to search far in the biological literature on play to find play described as “costly,” or to encounter a clear implication that play involves a substantial expenditure of time and/or energy (e.g., Beach. 1945; Berlyne. 1966: Loizos, 1966, 1967: Dolhinow & Bishop, 1970, 1972; Bekoff, 1972, 1976b; Farentinos, 1971; Hinde, 1974, p. 227: Poirier & Smith, 1974; Symons, 1974; Poole & Fish, 1975; White, 1977: Berger. 1980; Immelmann, 1980, p. 101: Bateson & Young, 1981; Bekoff& Byers. 1981, p. 315: Byers. 1981: Fagen, 1981, pp. 272. 311, 312, 314; Suonii, 1982). Numerous authors have developed this supposition about the costliness of play into an informal cost-benefit analysis which seenis to have become one of the central tenets of play research: Play has large costs and must, therefore. have large benefits (e.g.. Dolhinow & Bishop, 1970, p. 192: Farentinos, 1971: Hinde, 1974. p. 227: Poirier & Smith, 1974, p. 277; Symons. 1974. p.317; Poole & Fish. 1975: Bekoff& Byers, 1981, p.325; Fagen, 1981, pp.19.482; Smith, 1982). For example. Symons (1974. p.317) argues. “Since immature animals of many species spend so much time and energy playing, play must be adaptive.” We do not wish to imply that previous writers have been uncritical. Some have recognized that the costliness of play is only an assumption. For example, Fagen (1981, p.24) write,, “Time, energy. growth. and survivorship costs of play are generally recognized, if not rigorously demonstrated in all cases,” and later (p.313) he points out that, at the time of writing, “direct measurement of caloric expenditure in play remains to be performed.” Similarly. Bekoff and Byers (1981) make it clear that the costliness of play is only an assumption rather than an empirically dcrnonstrated fact.

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1982). This is numerically equal to the net percentage reduction in the mean daily rate of energy expenditure that would result from resting instead of playing, given that all other activities remained unaltered. Using this definition, Martin (1982) initially estimated the energy cost of play for most mammals to be of the order of 2.5%, with an upper limit of 15%. The substantial cost of growth (typically around 30% of total energy intake) is excluded from the total energy expenditure in this formulation of ECP, which therefore tends to underestimate the relative energy expenditure on play. One possible objection to using ECP as an index of energy cost is that other, patently beneficial activities (such as copulation) probably also have a small energy cost relative to total expenditure. However, energy cost is not by itself used to justify the view that, say, copulating is biologically beneficial, whereas for play it often is. Similar logic applies to the use of time as a measure of importance. Clearly, some manifestly beneficial activities do not consume a great deal of time. Again, though, play is different in so far as assumptions about its costs are often the only arguments used to support the view that play is highly beneficial. In an attempt to question the consensus view about the costliness of play, Martin (1984b) measured the amount of time and energy that young domestic cats devote to play, using a variety of empirical methods. Both time-lapse photography and time-sampling observations were used to estimate the proportion of total time spent in social or object play by sibling-pairs of kittens living with their mothers in their own large indoor pen. Food was available ad libitum, a variety of toys were provided, and the animals were undisturbed. Under these ideal conditions, kittens were found to spend on average 9% of total time (per 24 hr) playing. In a separate set of measurements, indirect (oxygen consumption) calorimetry was used to record kittens’ metabolic rates when resting and playing. The likely upper limit of play metabolic rate was also independently estimated, using a published numerical model of metabolism. The amount of energy expended on play (in excess of resting expenditure) was found to account for about 4%, and at most 9%, of total daily energy expenditure (Martin, 1984b). If anything, these are overestimates of ECP since the large costs of growth were excluded from total expenditure and, second, the upper limit of ECP was estimated on the unrealistic assumption that play consisted entirely of running. These empirical results confirmed earlier speculation by Blaxter (1962, p. 108) and Martin (1982) that play accounts for only a small proportion (less than 10%) of total daily energy expenditure in most mammals. The time budget results were also consistent with Fagen’s (1981, p.273) conclusion that play accounts for 110% of total time in most species that have so far been studied. Thus, Martin’s (1984b) results show that play accounts for less than 10% of a kitten’s total time and involves an additional energy expenditure (over and above the minimum that would occur anyway) that is about 4%, and certainly less than lo%, of its total daily output. Moreover, in this experiment the subjects were

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well-fed, disease-free, and predator-free juveniles of a domesticated species noted for its playfulness, living with their mothers in spacious, heated rooms containing a variety of toys-all optimal conditions for eliciting play according to the available evidence (see Fagen, 1981, p.361; and Section IV, B). It is likely that the time and energy expenditure on play would generally be lower in other species and in domestic kittens living under less favorable conditions. Juvenile mammals spend little or no time engaging in adult activities such as mating, hunting, or defending territory and are probably less constrained by time and energy considerations than adults of the same species. Thus, the numerically small expenditures on play of time and energy are likely to be of limited importance in terms of the juvenile’s eventual survival and reproduction. Nonetheless, it must be admitted that there is no simple answer to the question of to what extent a particular time or energy cost should be regarded as costly. A third potential effect of play is a survivorship cost, resulting from an increase in the risk of injury, predation, or separation from the parent (Fagen, 1981, p.275; Bekoff & Byers, 1981). There have been many anecdotal accounts of animals falling or in some other way exposing themselves to risks when playing (e.g., Byers, 1977; reviewed by Fagen, 1981, Table 5-2). So far, though, the survivorship cost of play has not been quantitatively defined, estimated, or measured, and its possible magnitude and biological significance remain unknown. Clearly, though, an absence of empirical data does not entitle us to infer an absence of cost. The survivorship cost of play is certainly an issue that warrants much more research. As R . Fagen (personal communication) correctly points out, “If play were as interesting to certain field biologists as infanticide, we would have plenty of information about survivorship costs of play-and this information would be just as hotly contested. To summarize, an animal which plays does not necessarily incur large time or energy costs. Under most circumstances play probably accounts for less than 10% of total time and involves an additional energy expenditure which is less than 10% of total output. Unless it is found that play per se frequently results in injury or death, it is reasonable to conclude that its immediate biological costs may not be large. If so, then play need only have minor biological benefits in order to be maintained by natural selection. The only requirement in evolutionary terms is that the benefits should, on average, exceed the costs. Thus, there are no grounds for ussuming that play is of major adaptive importance solely on the basis of its costs. We hasten to add that of course it does not necessarily follow that because play has small costs it must have small benefits. The logic of any such cost-benefit argument is not reversible, and there remains a logical possibility that play has small costs but large benefits. However, given the evidence summarized in Section 111, we can find no compelling reason to suppose that play does necessarily have large benefits. At present, therefore, it is reasonable to propose that play may have relatively ”

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minor (and therefore not easily detectable) benefits, which nonetheless outweigh its minor biological costs. This suggestion could potentially be refuted empirically in a number of different ways, for example ( I ) by demonstrating that animals uniquely acquire valuable skills or experience from play; (2) by showing that play is a significant cause of death or injury under natural conditions; (3) by demonstrating that young animals play at the expense of a reduction in their growth rate; or (4) by showing that play directly prevents other manifestly beneficial activities. If play has only minor benefits, animals would be predicted not to play when, for example, this necessitated reducing their food intake-an expectation which is largely born out by existing evidence (e.g., Chavez, Martinez, & Yaschine, 1975; Baldwin & Baldwin, 1976; Miiller-Schwarze, Stagge, & Miiller-Schwarze, 1982; see Section IV, B). It must be stressed that assessing the true biological significance of the time, energy, and survivorship costs of play is not a straightforward matter. It is difficult to translate proximate costs (such as time, energy, and risk of injury) into ultimate costs (their consequences for lifetime reproductive success). The importance of proximate costs will certainly depend upon environmental conditions. For example, an additional daily energy requirement of, say, 4% might be inconsequential when excess food is available but might be of critical importance when an animal is already starving. Yet starving animals generally do not playand it is this closely related issue which we deal with in Section IV, B. Finally, we wish to emphasize that these arguments about the costs of play are put forward to generate further debate, not to stifle it. The hope is that, rather than using dubious notions about the costliness of play to support assumptions about its benefits, direct evidence for these proposed benefits will instead be sought empirically. B.

OF PLAY THE LABILITY

Another reason for suggesting that play may not be of crucial adaptive importance is its absence in many species of mammal and its extreme sensitivity to prevailing conditions in those species which do play. Play is highly variable in its distribution, both interspecifically and intraspecifically. In his masterly review, Fagen ( 198 1, Ch. 3) has comprehensively documented the phylogenetic distribution of play, demonstrating that play (as commonly defined) seems to be present in many-but not all- mammals and some birds but is completely absent from other taxonomic groups such as the reptiles and insects (see also Burghardt, 1984). Furthermore, there are often substantial differences in both the amount and nature of play between taxonomically closely related species (Smith, 1982). For example, rats engage in social play, but social play is rarely, if ever, observed in mice (Poole & Fish, 1975; Einon, Humphreys, Chivers, Field, &

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Naylor, 1981). It seems implausible that play should be of vital importance in the ontogeny of some species but not in other, closely related species. A second and more important point is that play is also very variable within those species which do play. A well-known feature of play is that animals will play only when they are “relaxed” and free from threats, discomfort, hunger, danger, and illness (e.g., Hutt, 1966; Bekoff, 1972; Schaller, 1972, p.165; Fagen, 1981, p.361; Suomi, Kraemer, Baysinger, & DeLizio, 1981). Indeed, many writers have held the view that play is a sensitive indicator of an animals’s general state of physical and mental well-being, and Fagen (1981, p.361) notes that, in the experience of many veterinarians and pediatricians, a reduction in the amount of play “is the first and most obvious sign of illness in an animal that may otherwise appear very healthy” (see also Suomi et al., 1981). An illustration of the intraspecific lability of play is provided by the field observations of Baldwin and Baldwin (1973, 1974), discussed earlier. Some wild populations of squirrel monkeys were found to exhibit extensive social play, whereas in other groups play was rare or completely absent. A subsequent laboratory experiment with squirrel monkeys showed that if food was made difficult and time-consuming to obtain, social play rapidly dropped to about 1% of its former level (Baldwin & Baldwin, 1976). As in the field studies, “no pathological or dysfunctional consequences were observed in any of the circumstances when play was reduced to zero or near zero.” Numerous field studies of other species have also found sharp reductions in play associated with changes in the abundance or quality of food (e.g., rhesus monkeys: Loy, 1970: lions: Schaller, 1972, p.165; vervet monkeys: Lee, 1983; children: Chavez et al., 1975; see Fagen, 1981, p.370). Another example of the lability of play comes from Berger’s (1979, 1980) study of populations of bighorn sheep inhabiting different natural environments. Major differences in the quantity and quality of play behavior were found between the different study populations. For example, playful interactions were drastically curtailed in sheep inhabiting a desert environment and play was at least nine times more frequent in a northern study population. Changes in the ease of food availability can also lead to a large reduction in the incidence of play. For example, Muller-Schwarze et al. (1982) studied the locomotor play of five white-tailed deer fawns when their food was changed from milk to grass. The fawns were initially bottle-fed with milk but could also graze in their enclosure. When their milk supply was subsequently reduced to twothirds of the previous ad libitum intake, the fawns increased their grazing by 62% and almost exactly compensated for the loss of calories from milk. Their total energy intake remained at 99% of the ad libiturn level. This change in food source led to a reduction in their general locomotor activity of about 9%, but their play fell by 35%. Such a disproportionately large reduction in play, result-

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ing from a minor ( 1 %) reduction in total calorific intake, points both to the sensitivity of play and to its low priority relative to other forms of activity. Surprisingly, though, Muller-Schwarze et a f . concluded from these results that “the persistence of play . . . points to the importance of play.” Play may also be curtailed for a variety of other reasons, such as overcrowding (Leyhausen, 1979), inclement weather (Rasa, 1971; Card & Meier, 19771, and the presence of a human observer (Sugiyama, 1965; see Fagen, 1981, pp.302, 361, 370). Play may also vary intraspecifically for reasons other than short-term changes in environmental conditions. Young voles born in the spring and early summer play extensively, whereas those born in the autumn seldom, if ever, play (Wilson, 1973). Similarly, there are often marked individual differences in play, for example, in the locomotor play of domestic kittens and their mothers (Martin & Bateson, 1985) and in the play of yellow-bellied marmots (Nowicki & Armitage, 1979). In conclusion, play is absent from the behavioral repertoire of some species, and, more importantly, the incidence of play is extremely variable within those species which do play. Play may be suppressed by a variety of factors which occur relatively often in natural environments, yet we know of no evidence that its absence has any major effects. Play appears to be an activity of low priority, since it is dropped in preference to virtually all other forms of activity. We know of no instances in the literature, for example, where animals have been found to continue playing yet have curtailed their foraging or other aspects of social behavior as a result of minor food shortages. Play may be less prominent than is often assumed in many wild populations of mammals. In passing, it should be said that the lability of play might also point to its having very large costs, since the most costly activities (as well as the least important) might also be dropped temporarily during conditions of stress. Nevertheless, we tend to discount this alternative explanation for the lability of play because independent empirical evidence (see Section IV, A) suggests that play has low time and energy costs. Furthermore, it is not immediately obvious why play should be far more costly in some species than in other, closely related species. In summary, the interspecific and intraspecific variability of play suggest that it is unlikely to be a crucial ingredient of normal behavioral development. A more plausible view is that play is a facilitatory developmental determinant whose benefits outweigh its costs in some favorable environments but not in others.

C . ADULTPLAY Adults of many species also play, both socially and with objects (see Fagen, 1981; Smith, 1982), and it is clearly mistaken to assume that play is solely the province of juveniles. The existence of adult play is another piece of circumstan-

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tial evidence against practice hypotheses because skilled serious behavior patterns are already present in the repertoire of adults. Of course, the same behavior can have different functions at different stages of ontogeny-as, for example, shown by the differences between filial and sexual imprinting in birds (Bateson, 1979)-and the functions of play in adulthood might be different from those earlier in ontogeny. Adult play might maintain specific behavior patterns rather than facilitate their development, for example. Whatever the case, it seems likely that adult play is selected for because of its immediate benefits. As such, it is not unreasonable to suggest that the play of juveniles might also have immediate benefits.

V.

THEORETICAL PROBLEMS I N DETECTING THE BENEFITSOF PLAY

The benefits of play, though manifold according to prevailing theories, are not obvious in practice and, as we have seen, have so far evaded most attempts to elucidate their nature. In the first half of this article, we proposed that one reason why no major benefits of play have yet been uncovered might be that there are none; the minor costs and lability of play point toward its having a relatively small role in behavioral development. Nonetheless, there are several other factors which might also contribute to difficulties in uncovering the benefits of play. Discussion of these factors raises theoretical issues about behavioral development, such as when in ontogeny the benefits of play manifest themselves, as well as some methodological points. These issues are addressed here in order to generate suggestions for future empirical research. A.

VERSUS LONG-TERM EFFECTSOF PLAY SHORT-TERM

Most theories about the functions of play assert that play has immediate costs and delayed benefits. The young animal, it is argued, plays at the immediate expense of time and energy expenditure but subsequently benefits from, say, improvements in predatory or social skills later in ontogeny (e.g., Groos, 1898; Fagen, 1981, pp. 355, 362; Smith, 1982, p. 149). This conventional view-that play is practice for some form of serious behavior later in ontogeny-is represented in Fig. la. Here, the outcome variable (that is, a measure of the serious behavior purportedly practiced by playing) is shown as a function of age for two hypothetical animals: one which plays during a period early in ontogeny and one which does not play but is otherwise similar. A concrete example can be chosen from Caro’s (1980a) work on the role of object play in the development of predatory skills in domestic cats. Here, the outcome variable would be a measure of adult predatory behavior (say, percentage success in killing prey), and the two

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w

FIG. I . Hypothesized differences in a behavioral outcome variable (a measure of the serious behavior) between playing (dotted line) and nonplaying (continuous line) subjects, as a function of age. (a) Conventional practice model; long-term benefits. (b) Immediate benefits only. (c) Acceleration of normal development; short-term benefits.

curves would represent animals which had and had not received opportunities for object play when young. In fact, Car0 failed to find any such difference between the two groups of cats. Note that in this case the adult behavior pattern is assumed to develop to some extent even in the complete absence of prior play, since most practice theories now postulate that play improves adult skills rather than being absolutely necessary for the development of adult behavior. In its simplest form, then, the conventional practice theory predicts that a quantitative difference between the Play and No Play groups first starts to emerge when the relevant adult behavior pattern has begun to develop (point 3 in Fig. la) and persists to some extent thereafter (e.g., point 4,in adulthood). According to this model, experimental or correlational studies should be able to detect the consequences of differences in early play experience at any stage in ontogeny after the serious adult behavior has developed. The pattern of development shown in Fig. l a would be one way of accounting for the negative results of the correlational studies we described earlier. In these cases, the outcome variables (predatory success or other skills) were measured while the animals were still young (point 2

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in Fig. la). The model does not, however, explain Caro’s (1980a) failure to find any long-term consequences in kittens of not playing since, in his experiment, the outcome variables were actually measured in early adulthood. Yet there are no compelling grounds for assuming that the principal benefits of play must be delayed in ontogeny. Indeed, because of the cumulative effects of mortality, any benefit would have a larger selective advantage the earlier in ontogeny it acted. Thus, it could equally well be proposed that play is adaptive because it has immediate beneficial consequences for the juvenile. This possibility is lent further credence if, as we argued earlier, the benefits of play are neither very large nor important. For example, the experimental studies of children’s play we described found that play has certain immediate beneficial effects on children’s problem-solving abilities and creative thinking. If we suppose (as in fact seems likely) that these differences result from the immediate mood induced by playing, then there need be no long-term benefits for adult problemsolving or creative-thinking abilities. This possibility is represented in Fig. 1 b. Here, differences can be detected only during the same stage in ontogeny when differential play experience occurs (point I), but not thereafter. Thus, if the principal benefits of play accrue to the juvenile as an immediate consequence of playing, then any experiment which searched for major differences in adult skills might prove fruitless. (Of course, even if most benefits of play do occur immediately. some long-term comequences might be detectable later in ontogeny . The point is, though, that these would not in general be functionally related to the prior play patterns in any obvious or easily predictable way.) In conclusion, it would appear that too little attention has been paid by ethologists to the possibility that play may have immediate benefits (see Bekoff & Byers, 198 1 , for a similar view). A third possibility is that play serves to accelerate the development of adult behavioral capabilities but neither is necessary for their eventual development nor improves their final performance when they have fully developed. This is represented in Fig. lc, which again illustrates the point that behavioral differences resulting from differences in play experience might be detectable only during a restricted phase in ontogeny (e.g., point 3). For example, let us suppose that the principal effect of playing with dead prey or prey-like objects is to reduce young kittens’ fear of live prey and thereby to hasten slightly their first successful prey killing attempt (Martin, 1984a). The idea here is that all kittens would eventually become competent predators, regardless of whether or not they had previously played, but that the onset of successful predation would occur slightly earlier in ontogeny if they had played. Kittens which had played less or not at all would be slightly older when they first successfully dealt with prey but would do this equally competently on average. This speculative suggestion is consistent with current knowledge of how predatory behavior actually develops in domestic cats. For example, individual differences in predatory behavior are most promi-

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nent, not in the final predatory acts themselves, but in the time needed to become a competent predator and in the developmental route leading up to this (Baerendsvan Roon & Baerends, 1979, pp.75-78). The prevalence of the view that play has delayed benefits and is involved in the development of adult behavior raises a broader point about behavioral development. There has long been a tendency to regard juvenile behavior solely in terms of its relation to adult behavior (see Bateson, 1976b; Oppenheim, 1980; Galef, 1981). Sometimes, as in practice theories of play, juvenile behavior is seen specifically as a means of developing adult behavior, or “behavior used in development” as Bateson (1976b) has termed it. Yet natural selection acts at all stages in ontogeny-not just on the adult phenotype-and the developing organism must be adapted at every stage in ontogeny (Hamilton, 1966; Williams, 1966, p.44; Galef, 1981). The juvenile is not a miniature adult, and it can be highly misleading to regard its behavior as no more than an incompetent version of adult behavior. For example, numerous experiments have now established that the suckling of rat pups is in many respects qualitatively distinct from adult feeding (Drewett, 1978; Hall & Williams, 1983). Some aspects of juvenile behavior might specifically be concerned with problems that are unique to that stage in ontogeny and have no direct role in the development of adult behavior. Play could be an example of a “juvenile adaptation” (Oppenheim, 1980), in which case the relation between play and structurally similar forms of adult behavior would be unpredictable and difficult to establish. Of course, we are not suggesting that no attempts should be made to analyze the long-term consequences of play. The point is that efforts should also be directed toward investigating its consequences for the juvenile. B.

EQUIFINALITY

Another reason why individual differences in play apparently have few major consequences later in ontogeny might be that development is well buffered against such variation in early experience. This point is encapsulated in the system theory concept of equifinality, which asserts that in an open system (such as a living organism) the same steady state in development can be reached from different initial conditions and in different ways (Bertalanffy, 1968, p.40; Bateson, 1976b). Thus, the same state in behavioral development-say, the attainment of adult predatory skills-could be achieved via a variety of different developmental histories. In other words, different developmental routes involving different amounts and types of play, or perhaps none at all, might converge on the same developmental end point, and playing when young might be only one way of achieving predatory competence. Thus, an alternative to the suggestion that play has no major benefits is that play does have important benefits under some circumstances, but these benefits can also be obtained in other ways.

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Once again, we may illustrate this point using Caro’s work on the developmental determinants of predatory behavior in domestic cats. Adult predation is influenced by numerous factors which act early in ontogeny, such as manipulation of prey when young (Caro, 1980b), the presence and behavior of the mother during exposure to prey (Caro, 1980a), and the possible effects of competition between siblings during exposure to prey (Caro, 1980~).In addition, experience with prey when adult also enhances adult predatory skills (Caro, 1980a). These findings are illustrated in Fig. 2 . The point here is that a given set of adult behavior patterns, in this case predatory behavior, has multiple developmental determinants, and variation in one of these (play, for example) might be compensated for by variation in another. This type of buffering would clearly be adaptive, in so far as it would allow competence to develop despite environmental variation during ontogeny. Car0 (1980a) found no differences between the adult predatory skills of cats which had and had not received opportunities to play with objects when young. One explanation of this is simply that object play is not involved in the development of predation. An alternative explanation, suggested by the idea of equifinality, is that early differences in play opportunities were compensated for by other factors, such as increased attention to the mother’s prey handling. Similarly, predators living in a natural environment would be able to improve their predatory skills by increased experience of prey when adult. The development of predation could be buffered against normal variation in opportunities for play when young, in which case related differences in adult behavior would not emerge as a result of many experimental manipulations. Initial differences in kittens’ predatory skills do in fact tend to disappear later in ontogeny, as individuals who are poor predators when young catch up as adults (Baerendsvan Roon & Baerends, 1979, p.77; Caro, 1979). The notion of equifinality has also proved useful in studies of child development where it has become clear, for example, that there is more than one way to acquire language and that early traumatic experiences do not necessarily have immutable, long-term effects (Clarke & Clarke, 1976; Dunn, 1976; Kagan, 1978). It would be surprising-given the variability of play and its apparent sensitivity to variation in environmental conditions-if the development of vital adult behavioral capabilities were to depend critically on playing during early ontogeny . Some theoretical support for the notion of equifinality in relation to play is provided by Fagen’s computer models, in which the development of play was analyzed in cost-benefit terms as a life-history strategy (Fagen, 1977; 1981, Ch.6). Some of the general predictions of Fagen’s models were that (1) not all species will exhibit play; (2) within a species, play is an optimal strategy in some environments but not in others; and (3) within a particular environment, play may not be a unique optimal strategy, that is, play may evolve in some subpopulations but not in others inhabiting the same environment. The evolution of

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multiple optimal strategies, some not involving play at all, was a common feature of Fagen’s models and emphasized that play is often not a unique optimal strategy (Fagen, 1981, p.375).

C. NONEQUIVALENCE Another assumption in most functional theories of play is that play must be practice for structurally similar behavior patterns. For example, the play of kittens is frequently held to be practice for adult predatory behavior because the motor acts used in the two contexts look somewhat similar (e.g., Egan, 1976). However, two behavior patterns can have similar structures yet serve different functions, and vice versa. For instance, suckling and lapping milk have the same consequences for rat pups (Hall & Williams, 1983). Functional similarities cannot simply be inferred from structural similarities between two behavior patterns, particularly when (as in the case of play and adult predation) they occur at different stages in ontogeny. Structural similarity between object play and adult predatory patterns does constitute a reason for hypothesizing that the two are functionally related but is not in itself a sufficient reason for assuming this relationship (see also Car0 & Alawi, 1985). This line of reasoning raises the disheartening possibility that play could be a developmental determinant of adult behavior patterns which look entirely different. If, for example, the social play of primates has a socializing function, then the detailed form of playful motor patterns would, to a large extent, be irrelevant. This argument seems particularly compelling in the case of children’s play, where the important factor may be just that the children engage in activities with their peers. The precise form of those activities may, within certain limits, be of no great importance. In the case of motor training theories of play, though, it is reasonable to hope that play will resemble in form the adult behavior it is purported to practice. If not, it is difficult to know which adult behavior patterns should be chosen as the outcome variable in an experimental study.

D. NONSPECIFICITY All practice or motor training theories of play postulate that play is a developmental determinant which has specific effects on a particular type of serious adult behavior. Many developmental deterniinants of behavior have general effects, however (Bateson, 1976a, 1981). For example, simple exposure to patterned light during early development can affect many aspects of chicks’ behavior, including the rate at which they learn about visual targets, their readiness to approach an imprinting stimulus, and their accuracy of pecking at seeds (Bateson, 1976a). The possibility that play may exert general rather than specific

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effects on adult behavior is embodied in one functional theory of play, the exercise hypothesis. The exercise hypothesis postulates that the principal benefits of play result from physiological training effects which improve the overall efficiency and stamina of skeletal muscles and the cardiopulmonary system (Brownlee, 1954; Fagen, 1976; Fagen & George, 1977). If play does act mainly to improve general physical fitness, then early play activity would exert a broad range of nonspecific effects on many types of adult behavior rather than specifically improving one particular type of adult skill. The summed effects of many small improvements in the efficiency with which all motor acts were performed would constitute a significant selective advantage, even though the effect on any one adult behavior pattern might be suble and difficult to detect experimentally. Once again this theoretical possibility, if true, would have disheartening consequences for practical research because it implies a need to search for subtle differences in behavior across a broad range of behavior patterns rather than dramatic changes in a single outcome variable. At the very least, the possibility that play has beneficial physical training effects suggests that experiments should be fine grained and use multiple, sensitive measures. A single, relatively crude outcome variable, such as percentage success in killing prey, is unlikely to pick up subtle differences in the speed or efficiency with which the prey-killing motor acts are performed.

E. THRESHOLD EFFECTS Another theoretical possibility is that some threshold amount of play experience may be necessary before any changes in adult behavior occur. If so, one explanation for failing to find an effect of differences in early play experience could be that none of the animals had played enough for this threshold to be exceeded. In Caro’s (1980a) study, for example, the kittens which were allowed to play with objects might not have played enough for any improvement in predatory skills to have occurred-a so-called floor effect. Conversely, play can probably improve adult skills only by a finite amount, and once an animal has received a certain amount of play experience, adult skills may cease to be improved any further-a ceiling effect. In Caro’s experiment it is possible (though unlikely) that the control animals received sufficient opportunities for object play (for example, with wood shavings from their litter trays) that they attained the maximum possible improvement in predatory skills, thereby obscuring any difference relative to the object-playing kittens. Clearly, in any such experiment it is necessary to manipulate play experience to a sufficient extent that differences in outcome variables can emerge.

F. INTERACTIONS

BETWEEN

DEVELOPMENTAL DETERMINANTS

In so far as there are any valid generalizations about behavioral ontogeny, one is that the development of all behavior is influenced by many factors (Bateson,

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1981). For example, the predatory behavior of adult cats is influenced by a variety of factors which operate earlier in ontogeny (Fig. 2), although object play does not seem to be one of these (Caro, 1980a). As a general principle, developmental determinants cannot be assumed to operate independently of one another, and it has become clear that they often interact in important ways (Bateson, 1976a). To take an example from human development, a longitudinal study (Werner, Bierman, & French, 1971) found that the effects of severe perinatal stress on later measures of children’s physical and psychological well-being depended greatly on social and economic factors (see Dunn, 1976). In the case of Caro’s (1980a) cats, it could be that object play early in ontogeny exerts a beneficial effect on adult predatory skills only when it occurs in conjunction with some other form of early experience, for example, manipulation of dead prey or observing the mother deal with prey (Caro, 1980a,b). It certainly seems plausible that playing with objects might improve adult predation only if kittens concurrently achieve a certain degree of competence or familiarity with prey items. Bruner (1973) has postulated a similar set of interactions between “mastery play” and other factors involved in the development of skilled manipulative actions in human infants. Specifically, Bruner suggests that a child’s ability to copy adult behavior and incorporate it into play (whereby manipulative skills can be developed) depends on the child initially having a certain degree of competence at the task in question. In addition, Bruner argues, the child’s ability to develop skilled action through play will undoubtedly be affected by a variety of social factors such as maternal encouragement and other aspects of the home environment.

VI.

METHODOLOGICAL ISSUES

It should be apparent from our survey that few general statements about the functions of play can currently be supported by any solid empirical evidence. Very little is actually known about either the biological costs and benefits of play or its role in development. In particular, the following questions can currently be answered only tentatively and incompletely: (1) What are the benefits of play? (2) Does play have one or more beneficial effects-in other words, is play a developmental determinant with specific or general effects on behavior? (3) Are the beneficial effects of play immediate or are they delayed in ontogeny, accruing mostly to the adult’? (4) What are the biological costs of play and how important are they relative to other forms of activity’? In particular, does play incur significant survivorship costs’? ( 5 ) Is play a homogeneous set of behavior patterns in terms of its proximate causation, development, and function, or are several unrelated types of behavior being mistakenly lumped together‘? Clearly, there is a pressing need for these and other questions to be addressed empirically. In the hope that such experimental work will be carried out, we offer some

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methodological suggestions which stem directly from the views advanced in this article.

A. CONFOUNDING VARIABLES To answer questions about the functions of play it will, of course, be necessary to perform experiments in which various aspects of early play experience are manipulated and the consequences for other forms of behavior are assessed. Crude deprivation experiments, in which animals are deprived of all opportunities for play, suffer considerably from the problem of confounding variables. Any procedure which deprives a young mammal of all opportunities for, say, social play will inevitably alter many other potentially important factors as well, including all other forms of social experience, motor activity, sensory stimulation, stress, and (probably) nutrition and temperature (see Bekoff, 1976a). Thus, if differences are found between play-deprived and normally reared animals, this alone does not constitute evidence for the importance of play per se. In Bekoff‘s (1976a) phraseology, it is difficult to know “who is being deprived of what” in such a deprivation study. Nonetheless, the deprivation procedure should not be dismissed out of hand, since this method is in principle capable of providing useful i n f ~ r m a t i o n In . ~ particular, a series of selective deprivation experiments, each focusing on a different aspect of playful experience, could be very informative. A subtle approach is needed, in which specific components of play experience are manipulated and a variety of other behavior patterns (the outcome variables) are measured quantitatively. A number of different experimental techniques appear promising, including ( 1) selective enrichment or selective deprivation of opportunities for particular types of play (e.g., Caro, 1980a); (2) the use of drugs such as chlorpromazine and amphetamine to modify the behavior of social play partners (Einon et al., 1978); (3) the use of objects with different physical properties in studies of object play, for example, comparing the consequences of playing with toys which are predictable versus unpredictable, hazardous versus safe, preylike versus nonpreylike, fast-moving versus slow, complex versus simple, or passive versus reactive; and (4) altering the rearing environment so as 4Specifically. a deprivation experiment can demonstrate that a particular type of early experience (such as play) is nor necessary for some other form of behavior (such as predation) to develop (Lorenz, 1965, p.107). However, it is important not to confuse outcome (which is measured) with process (which is not). A deprivation experiment cannot show that an early experience is not involvcd in development under normal circumstances, since the deprived animal might have been forced to develop in a different way. In other words, there may be more than one developmental route leading to the same end point (see Section V , B). As Bateson (1981) points out, to contend that an early experience is not involved in development when it is available “would be like arguing that travellers who are forced to use bicycles because of a fuel shortage do not need petrol to run their cars.”

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to vary the opportunities for particular types of locomotor play, for example, manipulating the ease with which running, climbing, or balancing on narrow surfaces is possible. Valuable information can also come from comparisons of natural populations of a species which live in different habitats (e.g., Baldwin & Baldwin, 1974, for squirrel monkeys; Berger, 1979, 1980, for bighorn sheep). Even in the most refined and carefully controlled experiment, however, some confounding variables are likely to be present. For example, in the study by Einon er al. (1978) described earlier, drugs were used to modify the behavior of rats’ social play partners, and the drugged rats presumably differed from normal social companions in many ways besides just playing differently. Hence, as the authors point out, it is incorrect to conclude from this one experiment that the lack of social play per s e affected the subsequent behavior of the experimental rats. Play cannot easily be isolated from other forms of experience, so no single experiment is likely by itself to settle a functional question conclusively. Rather, several related experiments will generally be needed, each experiment controlling for certain factors, excluding certain competing possibilities, and narrowing the range of possible explanations. In this sense, research on the functions of play is akin to work on the neural basis of memory, where detailed understanding has begun to emerge only as a result of performing a systematic series of experiments (see Horn, 1981). B.

CHOOSING OUTCOMEVARIABLES

Investigating the functions of play requires first choosing the serious behavior patterns of which play is supposed to be a developmental determinant, that is, choosing the correct outcome variables. The view of play proposed in this article suggests that outcome variables should be (a) multiple; (b) sensitive; and (c) clearly related to the hypothesized biological benefits. The need for multiple outcome variables arises because current functional hypotheses are not sufficiently specific to make precise predictions about the detailed effects of play on subsequent behavior. Several components of the serious behavior must therefore be rneasured in order to assess the role of play in its development. For example, to test the hypothesis that kittens’ object play functions as training for adult predatory behavior would require measuring several components of predation. since there are at present no n priori grounds for deciding precisely which aspects of predation may be affected by play. The need for multiple outcome measures is even more obvious in tests of the exercise hypothesis, since this predicts that play exerts beneficial effects on the performance of many motor patterns. Indeed, the more general the effects of play are predicted to be (or the vaguer the hypothesis) the more outcome variables are necessary. The need for sensitive and subtle outcome measures arises because play is,

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according to the arguments presented here, unlikely to be of major importance in behavioral development and may have only minor benefits. If play subtly affects the efficiency with which an act is performed or facilitates its development, rather than determining whether or not the act is performed at all, then behavioral analysis of the subsequent acts must be detailed. Crude outcome variables, such as the percentage of prey killed, are unlikely to uncover small differences between animals with different histories of play experience. A more fruitful strategy would be to search for subtle differences in, say, the efficiency with which components of predatory behavior were performed, or in the accuracy and speed of predatory motor patterns. Finally, changes in the quality or ordering of behavior patterns will not be revealed by simple frequency or latency measures-a consideration that is all the more relevant if another of play’s hypothesized functions is as a source of innovative behavior (Fagen, 1981, 1982). A third requirement is that outcome variables should be functionally relevant, that is, direct and easily interpretable measures of the hypothesized biological benefits. Any functional hypothesis makes certain predictions about the biological benefits of play, and it is these benefits which should be assessed as directly as possible. In theory, the function of any behavior pattern ought ultimately to be measured in terms of its contribution to the individual’s inclusive fitness or, more tangibly, to its lifetime reproductive success (Grafen, 1982). In experimental situations, lifetime reproductive success will usually be impossible to measure, but assessing an adaptation in terms of its proximate beneficial consequences will sometimes be a reasonable approximation (see Clutton-Brock, 1983). Some otherwise informative experiments have used outcome measures that were not directly relevant to any functional hypothesis, as, for example, in the elegant work by Einon and colleagues described earlier. These experiments showed that social isolation can produce long-term behavioral changes in rats, some of which can partially be annulled by brief periods of social contact later in development. Unfortunately, the consequences of isolation were assessed in terms of openfield measures such as habituation of object contact and locomotor activity. However, differences in open-field behavior cannot readily be interpreted in terms of biological benefits or deficits. It is far from obvious, for example, why an increase in “timidity” (as measured by slower habituation of open-field activity and object contact, or slower emergence into an unfamiliar environment) should necessarily be regarded as a behavioral deficit. Indeed, Daly (1973) has convincingly argued the converse: any small rodent which fearlessly enters a brightly lit and novel arena is, arguably, acting rnakadaptively. Thus, it is not possible to conclude from these experiments that play has particular adaptive consequences. Measures of open-field behavior, although pertinent to questions of motivation and emotionality, are difficult to assess in terms of biological function and, accordingly, are unsuitable outcome variables for the present pur-

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pose (see Hinde, 1970, p.535, and, especially, Daly, 1973, for criticisms of open-field measures and their frequent misinterpretation).

VII.

SUMMARY

Play is widely assumed to be a costly juvenile activity, crucially involved in the development of adult behavioral skills and exerting major beneficial effects on serious behavior later in ontogeny. However, a review of the limited evidence reveals no strong empirical support for this view. At present, there is no direct evidence that play has any important benefits, with the possible exception of some immediate effects on children’s behavior. One explanation for this is that play does not have major benefits but is instead a facilitative developmental determinant of minor importance. In support of this view is evidence that play has only minor time and energy costs and so need have only minor benefits to be maintained by natural selection. In addition, play is highly variable and labile, both interspecifically and intraspecifically, and is very sensitive to prevailing conditions. Because play is curtailed or absent under many naturally occurring conditions, it seems unlikely that it is essential for normal development. Adults of many species also play. We see no compelling reason to assume that the principal benefits of play, whatever they may be, are delayed in ontogeny and accrue only to the adult as improved skills. This widespread assumption, embodied in all practice theories, reflects a misleading view of ontogeny in which all juvenile behavior is seen as a preparation for adulthood. On the contrary, play may be adaptive because of its immediate or short-term benefits to the juvenile and may have no consistent, important, or predictable long-term consequences. At the very least, more attention should be paid to the consequences of play for the juvenile. Other possible reasons why no benefits of play have yet been detected are also discussed. Behavioral development may be well buffered against variation in play experience (equifinality); the effects of play may be nonspecific; the benefits of play may be manifested in structurally dissimilar forms of adult behavior; and the benefits may only be realized through interaction with other variables or if particular thresholds are attained. Current definitions of play are inadequate and reflect a deep conceptual muddle. In practice, the essence of the current concept of play seems to be a subjective interpretation on the part of the observer that the behavior has no obvious immediate benefits. A general definition of play is proposed which explicitly incorporates this notion. Methodological issues are also discussed, including the problem of confounding variables and the need for multiple, sensitive, and functionally relevant outcome measures in future experiments. If, as we suggest, play is a marginal activity, performed only as long as its benefits outweigh its costs, then play may be a

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useful and sensitive index of other aspects of behavioral development. These arguments are presented in the hope that they will provoke further enquiry. Play remains a biological enigma and deserves the serious attention of anyone seeking to understand the development and functions of behavior.

Acknowledgments The first draft of this article was written while PM was a Harkness Fellow at Stanford University and while TMC held a Royal Society scientific investigations grant. We are very grateful to the following people for kindly reading and commenting on the manuscript: Patrick Bateson, Marc Bekoff, Gordon Burghardt, Robert Fagen, Robert Hinde, Harriet Sants, and Peter Smith.

References Abbey, H., & Howard, E. (1973). Statistical procedures in developmental studies on species with multiple offspring. Dev. Psyclzobiol. 6, 329-335. Aldis, 0. (1975). “Play Fighting.” New York: Academic Press. Baerends-van Roon, J. M., & Baerends, G. P. (1979). The morphogenesis of’the behuvior ofthe domestic cut. Amsterdam: North-Holland Publ. Baldwin, J . D., & Baldwin. J. I. (1973). The role of play in social organization: Comparative observations of squirrel monkeys (Suimiri). Primates 14, 369-38 I . Baldwin, J . D., & Baldwin, J . I . (1974). Exploration and social play in squirrel monkeys (Suimiri). Am. Zoo/. 14, 303-315. Baldwin, J. D., & Baldwin, J . I . (1976). Effects of food ecology o n social play: A laboratory simulation. Z. Tierp.rvchul. 40, I - 14. Baldwin, J . D., & Baldwin, J. 1. (1977). The role of learning phenomena in the ontogeny of exploration and play. In S. Chevalier-Skolnikoff & F. E. Poirier (Eds. ), Prirnute hio-sociul developmen/ (pp.343-406). New York: Garland. Barrett, P., & Bateson. P. (1978). The development of play in cats. Behuviour 66, 106-120. Bateson, P. P. G. (1976a). Spec ity and the origins of behavior. Adv. Stucfv Behav. 6, 1-20. Bateson, P. P. G . (l976b). Rules and reciprocity in behavioural development. In P. P. G. Bateson & R. A. Hinde (Eds.), Growing points in ethnlogv. (pp.401-421). London and New York: Cambridge Univ. Press. Bateson, P. P. G. (1979). How do sensitive periods arise and what are they for’?Anim. Behuv. 27, 470-486. Bateson, P. (1981). Ontogeny. In D. McFarland (Ed.), The Oxford conipunion t o unifnul behuviour (pp.414-426). London and New York: Oxford Univ. Press. Bateson, P., Martin, P., & Young, M. (1981). Effects of interrupting cat mothers’ I bromocriptine on the subsequent play of their kittens. Physiol. Belruv. 27, 841-845. Bateson, P., & Young. M. (1981). Separation from the mother and the development of play in cats. Anbn. Behuv. 29, 173-180. Beach, F. A . (1945). Current concepts of play in animals. Am Nut. 79, 523-541. Bekoff. M. (1972). The development of social interaction, play and metacommunication in mammals: An ethological perspective. Q . Rev. B i d . 47, 412-434. Bekoff. M. (1976a). The social deprivation paradigm: Who’s being deprived of what? Dev. Psvchoh i d . 9. 499-500.

PLAY IN BEHAVIORAL DEVELOPMENT

99

Bekoff, M. (1976b). Animal play: Probrems and perspectives. In P. P. G . Bateson & P. H. Klopfer (Eds.), Perspectives in ethology (Vol. 2, pp. 165-188). New York: Plenum. Bekoff. M. (1984). Social play behavior. BioScience 34, 228-233. Bekoff, M., & Byers, J. A. (1981). A critical reanalysis of the ontogeny and phylogeny of mammalian social and locomotor play: An ethological hornet's nest. In K . Immelmann, G . W. Barlow, L. Petrinovich, & M. Main (Eds.), Behavioral development (pp.296-337). London and New York: Cambridge Univ. Press. Berger. I. (1979). Social ontogeny and behavioural diversity: Consequences for Bighorn Sheep Ovis canadensis inhabiting desert and mountain environments. J . Zool. 188, 25 1-266. Berger. J. (1980). The ecology, structure and functions of social play in Bighorn Sheep (Ovis ranadensis). J . Zoo/. 192, 531-542. Berlyne, D. E. (1966). Curiosity and exploration. Science 153, 25-33. Bertalanffy, L., von (1968). General system theorv. New York: Braziller. Biben, M. (1979). Predation and predatory play behaviour of domestic cats. Anim. Behav. 27, 8194. Biben, M. (1982a). Object play and social treatment of prey in bush dogs and crab-eating foxes. Behaviour 79, 201-21 1 . Biben, M. (1982b). Sex differences in the play of young ferrets. B i d . Behav. 7, 303-308. Birch, H. G. (1945). The relationship of previous experience to insightful problem-solving. J . Comp. Psvchol. 38, 367-383. Blaxter. K . L. (1962). The energv metabolism of ruminants. London: Hutchinson. Brownlee, A. (1954). Play in domestic cattle in Britain: An analysis of its nature. Br. Vet. J . 110, 46-68. Bruner, J. S. (1973). Organization of early skilled action. Child Dev. 44, 1-1 I . Burghdrdt, G . M. (1984). On the origins of play. In P. K. Smith (Ed.), Plav in animals and humans (pp. 5-41). Oxford: Blackwell. Byers, J. A . (1977). Terrain preferences in the play behavior of Siberian ibex kids (Capra ibex sibirica). Z . Tierps.vchol. 45, 199-209. Byers, J . (1981). The significance of play. (Review of Animalplay behavior by R. Fagen, 1981). Science 212, 1493-1494. Caro, T. M. (1979). Relations between kitten behaviour and adult predation. Z . Tierpsvchol. 51, 158- 168. Caro, T. M. (1980a). Effects of the mother, object play, and adult experience on predation in cats. Behav. Neural B i d . 29, 29-5 I . Caro, T. M. (1980b). The effects of experience on the predatory patterns of cats. Behav. NeuralBiol. 29, 1-28. Caro, T. M. (1980~).Predatory behaviour in domestic cat mothers. Behavioiw 74, 128-148. Caro, T. M. (1981). Predatory behaviour and social play in kittens. Behaviour 76, 1-24. Caro, T. M. (1984). Intersexual selection and cooption. J . Theor. Biol. (in press). Caro, T. M., & Alawi, R. M. (1985). Comparative aspects of behavioural development in two species of free-living hyrax. Behavioirr (in press). Caro, T. M., Roper, R., Young, M., & Dank, G . R. (1979). Inter-observer reliability. Behavioitr 69, 303-315. Chalmers, N . R. (1980). The ontogeny of play in feral olive baboons (Papio anubis). Anim. Behav. 28, 570-585. Chalmers, N. R., & Locke-Haydon, J . (1984). Correlations among measures of playfulness and skillfulness in captive common marmosets (Callithrix jacchus jacchrrs). Dev. Psvchabiol. 17, 19 1-208. Chavez, A , , Martinez, C., & Yaschine, T. (1975). Nutrition, behavioral development, and motherchild interaction in young rural children. Fed. Proc. Fed. Am. Soc. Exp. B i d . 34, 1574-1582.

100

PAUL MARTIN AND T. M . C A R 0

Cheyne. I. A. (1982). Object play and problem-solving: Methodological problems and conceptual promise, In D. J . Pepler & K. H. Rubin (Eds.), The play of children: Current theory and research. Basel: Karger. Cheyne, J . A . , & Rubin, K. H. (1983). Playful precursors of problem solving in preschoolers. Dev. Ps.vchol. 19, 577-584. Christie, J . F. (1983). The effects of play tutoring on young children’s cognitive performance. J . Educ. Res. 76, 326-330. Clarke, A. M., & Clarke, A. D. B. (1976). Early experience: Myth and evidence. London: Open Books. Clutton-Brock, T. II. (1981). Function. In D. McFarland (Ed.), The Oxford companion to animal behaviour (pp.220-223). London and New York: Oxford Univ. Press. Clutton-Brock, T. H. (1983). Selection in relation to sex. In D. S . Bendall (Ed.), Evolution,from molecules to men (pp.457-481). London and New York: Cambridge Univ. Press. Craik, K . J . W. (1943). The nature ofexplanation. London and New York: Cambridge Univ. Press. Daly, M. (1973). Early stimulation of rodents: A critical review of present interpretations. Br. J . P,yychol. 64, 435-460. Dansky, J. L., & Silverman, 1. W. (1973). Effects of play on associative fluency in preschool-aged children. Dev. Psycho/. 9, 38-43. Dansky, J. L., & Silverman, I . W. (1975). Play: A general facilitator of associative fluency. Dev. Psycho/. 11, 104. Davies, V. A,, & Kemble, E. D. (1983). Social play behaviours and insect predation in northern grasshopper mice. (Onychomvs leucogastrrj Eehav. Proc. 8, 197-204. Dolhinow, P. J . , & Bishop, N. H . (1970). The development of motor skills and social relationships among primates through play. Minnesotu Symp. Child Psvchol. 4, 141- 198. Dolhinow, P. J . , & Bishop, N. (1972). The development of motor skills and social relationships among primates through play. In P. Dolhinow (Ed.), Primate patterns (pp.312-337). New York: Holt. Drewett, R. F. (1978). The development of motivational systems. Prog. Brain Res. 48, 407-417. Dunn, J . (1976). How far do early differences in mother-child relations affect later development? In P. P. G. Bateson & R. A . Hinde (Eds.). Growingpoints iti ethology (pp.481-496). London and New York: Cambridge Univ. Press. Egan, J . (1976). Object-play in cats. In J. S . Bruner, A. Jolly, & K . Sylva (Eds.), Play-its role in development and evolution (pp. 161- 165). New York: Basic Books. Einon, D. F., Humphreys, A. P., Chivers, S . M., Field, S . , & Naylor, V. (1981). Isolation has permanent effects upon the behavior of the rat, but not the mouse, gerbil, or guinea pig. Dev. Psychobiol. 14, 343-355. Einon, D. F., & Morgan, M. J . (1977). A critical period for social isolation in the rat. Dev. Psychobiol. 10, 123- 132. Einon, D. F., Morgan, M. J . , & Kihbler, C. C. (1978). Brief periods of socialization and later behavior in the rat. Dev. Psychobiol. 11, 213-225. Epstein, R., Kirshnit, C. E., Lanza, R. P., and Rubin? L. C. (1984). ‘Insight’ in the pigeon: Antecedents and determinants of an intelligent performance. Nature (London) 308, 6 1-62. Fagen, R. (1974). Selective and evolutionary aspects of animal play. Am. Nut. 108, 850-858. Fagen, R. M. (1976). Exercise, play and physical training in animals. In P. P. G. Bateson & P. H. Klopfer (Eds.), Perspectives in elhology (Vo1.2, pp. 189-219). New York: Plenum. Fagen, R. (1977). Selection for optimal age-dependent schedules of play behavior. Am. Nut. 111, 395-4 14. Fagen, R . (1981). Animal play behavior. London and New York: Oxford Univ. Press. Fagen, R. (1982). Evolutionary issues in development of behavioral flexibility. In P. P. G . Bateson & P. H. Klopfer, (Eds.), Perspectives in ethology (Vol. 5, pp.365-383). Kew York: Plenum.

PLAY IN BEHAVIORAL DEVELOPMENT

101

Fagen, R . M., & George, T . K. (1977). Play behavior and exercise in young ponies (Eyuus caballus L.). Behav. Ecol. Sociobiol. 2, 267-269. Farentinos, R. C. (1971 ). Some observations on the play behavior of the Steller sea lion (Eumetopias jubata) Z. Tierpsvchol. 28, 428-438. Galef, B. G . , Jr. (1981). The ecology of weaning: Parasitism and the achievement of independence by altricial mammals. In D. J. Gubernick & P. H. Klopfer (Eds.), Parental care in mammals (pp.211-241). New York: Plenum. Card, G. C . , & Meier, G. W . (1977). Social and contextual factors of play behavior in sub-adult rhesus monkeys. Primates 18, 367-377. Gentry, R. L. (1974). The development of social behavior through play in the Steller sea lion. Am. Zoo/. 14, 391-403. Could. S. J., & Vrba, E. S . (1982). Exaptation-a missing term in the science of form. Paleobiology 8, 4-15. Grafen, A. (1982). How not to measure inclusive fitness. Nature (London)298, 425-426. Groos, K. (1898). The play of’ animals (first published Basel, 1896). New York: Appleton. Guyot. G . W., Bennett, T. L., & Cross, H. A . (1980). The effects of social isolation on the behavior of juvenile domestic cats. Dev. Psychobiol. 13, 3 17-329. Hall, W. G.. & Williams, C. L. (1983). Suckling isn’t feeding, or is it? A search for developmental continuities. Adv. Study Brhav. 13, 219-254. Hamilton. W. D. (1966). The moulding of senescence by natural selection. J . Theor. B i d . 12, 12-45. Henry, J . D., & Herrero. S . M. (1974). Social play in the American Black Bear: Its similarity to canid social play and an examination of its identifying characteristics. Am. Z o o l . 14, 371389. Hill, H. L., & Bekoff, M. (1977). The variability of some motor components of social play and agonistic behaviour in infant Eastern coyotes, Cariis larrans. Anim. Behav. 25, 907-909. Hindc. R . A. (1960). Energy models of motivation. Svmp. Soc. E.xp. Biol. 14, 199-213. Hinde. R. A. (1970). Animal Behaviour (2nd ed.), New York: McGraw-Hill. Hinde. R. A. (1974). Biologicul bases ojhuman social behaviour. New York: McGraw-Hill. Hinde, R. A. (1975). The concept of function. In G. Baerends, C . Beer, & A. Manning (Eds.), Function and evolurion in behaviour (pp.3- 15). Oxford: Clarendon. Hinde, R. A. (1982). Ethology. London and New York: Oxford Univ. Press. Horn, G. (1981). Neural mechanisms of learning: An analysis of imprinting in the domestic chick. Proc. R. Soc. London Ser. B 213, 101-137. Humphreys. A. P.. & Einon, D. F. (1981). Play as a reinforcer for maze-learning in juvenile rats. h i m . Behav. 29, 259-270. Humphreys, A . P., & Smith, P. K. (1984) Rough-and-tumble in preschool and playground. In P. K. Smith (Ed.), Play in animals and humans (pp.241-266). Oxford: Blackwell. Hutt, C. (1966). Exploration and play in children. Symp. Zool. Soc. London 18, 61-81. Immelmann, K. (1980). Introduction to ethology. New York: Plenum. Jolly, A. (1972). Troop continuity and troop spacing in Propithecus \vrreaui and Lemur catfa at Berenty (Madagascar). Folia Primarol. 17, 335-362. Kagan. J . (1978). Continuity and stage in human development. In P. P. G. Bateson & P. H. Klopfer (Eds.). Perspectives in ethology (Vo1.3, pp.67-84). New York: Plenum. Kohler, W. (1925). The tnentalify qfapes. London: Kegan Paul. Lancaster, J . B. (1971). Play mothering: The relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops). Folia Primatol. 15, I61 - 182. Lee, P. C. (1983). Play as a means for developing relationships. In R. A. Hinde (Ed). Primate social relationships (pp.82-89). Oxford: Blackwell Scientific Pub. Lewin. R . (1982). Adaptation can be a problem for evolutionists. Science 216, 1212-1213.

102

PAUL MARTIN AND T . M . C A R 0

Leyhausen, P. (1979). Cat behavior: The predatory and social behavior of domestic and wild cats. (B. A. Tonkin, Trans.) New York: Garland. Loizos, C. (1966). Play in mammals. Symp. Zool. Soc. London 18, 1-9. Loizos, C. (1967). Play behaviour in higher primates: A review. In D. Monis (Ed.), Primate ethology (pp. 176-21 8). London: Weidenfeld & Nicolson. Lorenz, K. (1956). Plays and vacuum activities. In L'insrinct duns le comportement des animaux el de l'homme (pp.633-637). Paris: Masson. [Reprinted in Miiller-Schwarze, 19781 Lorenz, K. (1965) Evolution and modification of behavior. Chicago: Univ. of Chicago Press. Loy, J. (1970). Behavioral responses of free-ranging rhesus monkeys to food shortage. Am. J . Phys. Anthropol. 33, 263-271. Marler, P. (1975). On strategies of behavioural development. In G. Baerends, C. Beer, & A. Manning (Eds), Function and evolution in behaviour (pp.254-275). Oxford: Clarendon. Martin, P. (1982). The energy cost of play: Definition and estimation. Anim. Behav. 30, 294-295. Martin, P. (1984a). The (four) whys and wherefores of play in cats: A review of functional, evolutionary, developmental and causal issues. In P. K. Smith (Ed.), Play in animals and humans (pp.71-94). Oxford: Blackwell. Martin, P. (198413).The time and energy costs of play behaviour in the cat. Z . Tierpsychol. 64, 298312. Martin, P., & Bateson, P. (1985). The ontogeny of locomotor play behaviour in the domestic cat. Anim. Behav. 33 (in press). Mason, W. A. (1965). The social development of monkeys and apes. In I. DeVore (Ed.), Primate behavior (pp.514-543). New York: Holt. McDonald, D. L. (1977). Play and exercise in the California ground squirrel (Spermophilus heecheyi). Anim. Behav. 25, 782-784. Moelk, M. (1979). The development of friendly approach behavior in the cat: A study of kittenmother relations and the cognitive development of the kitten from birth to eight weeks. Adv. Study Behav. 10, 163-224. Miiller-Schwarze, D., Ed. (1978). Evolution of play behavior. Stroudsburg, PA: Dowden, Hutchinson & Ross. Miiller-Schwarze, D., Stagge, B., & Muller-Schwarze. C. (1982). Play behavior: Persistence, decrease and energetic compensation during food shortage in deer fawns. Science 215, 85-87. Nowicki, S., & Armitage, K. 8. (1979). Behavior of juvenile yellow-bellied marmots: Play and social integration. Z . Tierpsychol. 51, 85-105. Oppenheim, R. W . (1980). Metamorphosis and adaptation in the behavior of developing organisms. Dev. Psychobiol. 13, 353-356. Pepler, D. J . , & Ross, H. S . (1981). The effects of play on convergent and divergent problem solving. Child Dev. 52, 1202-1210. Piaget, J . (1962). Play, dreams, and imitation in childhood. New York: Norton. Poirier, F. E., & Smith, E. 0. (1974). Socializing functions of primate play. Am. Zool. 14, 275287. Poole, T., & Fish, J . (1975). An investigation of playful behaviour in Rattus norvegicus and Mus musculus (Mammalia). J . Zoo/. 175, 61-71. Rasa, 0. A. E. (1971). Social interaction and object manipulation in weaned pups of the Northern elephant seal Mirounga angusrirostris. Z . Tierpsychol. 29, 82- 102. Rasa, 0. A. E. (1984). A motivational analysis of object play in juvenile dwarf mongoose (Helogalr undulata rufula). Anim. Behav. 32, 579-589. Schaller, G. B. (1972). The Serengeti lion. Chicago: Univ. of Chicago Press. Schiller, P. H. (1957). Innate motor action as a basis of learning. In C. H. Schiller (Ed.), Instinctive behavior (pp. 264-287). London: Methuen. Schlosberg, H. (1947). The concept of play. Psychol. Rev. 54, 229-231. Simon, T., & Smith, P. K . (1983). The study of play and problem solving in preschool children:

PLAY IN BEHAVIORAL DEVELOPMENT

103

Have experimenter effects been responsible for previous results'? Br. J . Dev. Psvchol. 1, 289297. Smith, E. 0.. & Fraser, M. D. (1978). Social play in Rhesus Macaques (Maraca mulatfu):A cluster analysis. In E. 0. Smith (Ed.), Social pluv in primates (pp.79-I 12). New York: Academic Press. Smith, P. K. (1982). Does play matter'? Functional and evolutionary aspects of animal and human play. Behav. Brain Sci. 5 , 139-184. Smith, P. K. (1983). Differences or deficits'? The significance of pretend and sociodramatic play. Dev. Rev. 3, 6-10. Smith, P. K., Dalgleish, M., & Herzmark, G. (1981). A comparison of the effects of fantasy play tutoring and skills tutoring in nursery classes. Int. J. Behav. Dev. 4, 421-441. Smith, P. K., & Dutton, S. (1979). Play and training in direct and innovative problem solving. Child Dev. 50, 830-836. Smith, P. K . & Simon, T. (1984). Object play, problem-solving and creativity in children. In P. K. Smith (Ed.). Pluv in unimuls und humarrs (pp. 199-216). Oxford: Blackwell. Sokal, R. R. (1974). Classification: Purposes. principles, progress, prospects. Science 185, 1 1151123. Sugiyama, Y. (1965). Behavioral development and social structure in two troops of hanuman langurs (Presbvris enfellus).Primates 6 , 213-247. Suomi, S. J . (1982). Why does play matter'? Brhav. Brain Sci. 5 , 169-170. Suomi, S . J . , Kraemer, G. W., Baysinger, C. M., & DeLizio, R. D. (1981). Inherited and experiential factors associated with individual differences in anxious behavior displayed by rhesus monkeys. In D. F. Klein & J . Rabkin (Eds), Amiefy: New research and changing concepfs (pp. 179-199). New York: Raven. Sutton-Smith, B. (1967). The role of play in cognitive development. Young Child. 22, 361-370. Sylva, K. (1977). Play and learning. In B. Tizard & D. Harvey (Eds.), Biology of plav (pp.59-73). London: Clinics in Dev. Med. No.62, Spastics Intemationa~iHeinemdnnMedical. Sylva, K., Bruner, J . S., & Genova, P. (1976). The role of play in the problem-solving of children 3-5 years old. In J . S. Bruncr, A. Jolly, & K. Sylva (Eds.), Play-its role in development arid evolution (pp.244-257). New York: Basic Books. Symons, D. (1974). Aggressive play and communication in rhesus monkeys (Macaca mulaffa).Am. Zool. 14, 317-322. Symons, D. (1978). Play and aRgression: A studv qfrhesus monkevs. New York: Columbia Univ. Press. Thomas, E., & Schaller, F. (1954). Das Spiel der optisch isolierten Kaspar-Hauser-Katze. Naturwissenschaften 41, 557-558. [Translation in Miiller-Schwarze. 19781 Vandenberg, B. (1981) The role of play in the development of insightful tool-using strategies. Merrill-Palmer Q. 21, 97-1 10. Vincent, L. E., & Bekoff, M. (1978). Quantitativc analyscs of the ontogeny of predatory behaviour in coyotes, Canis latrans. Anim. Behuv. 26, 225-231. Weiss-Burger, M. (1981). Untersuchung zum Einfluss des Erkundungs- und Spielverhaltens auf das Lernen bei Iltisfrettchen (Miislela puforius x M. jirro). Z . Tierpsychol. 55, 33-62. Werner, E. E., Bierman, J . M., & French, F. E. (1971). The children ofKuaii. Honolulu: Univ. of Hawaii. West, M. (1974). Social play in the domestic cat. Am. Zool. 14, 427-436. White, L. (1977). Play in animals. In B. Tizard & D. Harvey (Eds.), Biology ofplay (pp.15-32). London: Clinics in Dev. Med. No. 62, Spastics InternationaliHeinemann Medical. Williams, G. C. (1966). Adapfation and naturul selection. Princeton, NJ: Princeton Univ. Press. Wilson, E. 0. (1975). Sociobiology; The new s w h e s i s . Cambridge, MA: Belknap. Wilson, S. (1973). The development of social behaviour in the vole (Microtus agresfis).Zool. J . Linn. Soc. 52, 45-62.

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ADVANCES IN THE STUDY OF BEIIAVIOR. VOL 1.5

Sensory Factors in the Behavioral Ontogeny of Altricial Birds S.N. KHAYUTIN INSTITUTE OF HIGHER NERVOUS ACTIVITY A N D NEUROPHYSIOLOGY ACADEMY OF SCIENCE OF THE USSR MOSCOW, USSR

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Oganization of Natural Behavior in the Nestling.. . . . . . . . . . . . . . . . . . . . . . A. Feeding Behavior at the Beginning of Nestling Life . . . . . . . . . . . . . . . B. Passive-Defense Behavi .................... C. Feeding Behavior at the eriod . . . . . . . . . . . . . . . ............................................ tic Sensitivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . Auditory Evoked Potentials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Recovery Cycles of Acoustic Evoked Potentials. C. Heterochronous Maturation of Frequency Channels. . . . . . . . . . . . . . . . D. Auditory Sensitivity and Behavior.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1V. Role of Audition in the Organization of Defense Behavior . . . . . . . . . . . . . . V. Ontogeny of Some Visual Mechanisms .................... VI. Complexity of Behavior Organization i Postembryonic Development .................... A. Sensory Organization o i t Nestlings . . . . . . . . . . . B. Sensory Organization of Behavior in Redstart Nestlings . . . . . . . . . . . . C. Sensory Organization of Cuckoo Nestling Behavior in the Redstart Nest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ns . . . . . . . . . . . . . . . . . . . . . 1. 11.

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

I.

10.5 108 108 11.5 116

118 I18 I19

I23 12.5 125 128 134 138 138 140

142 I43 I49

INTRODUCTION

In recent years the organization of behavior in humans and animals has been studied with increasing interest. Behavior as a subject of investigation has received the attention of physiologists, ethologists, zoologists, evolutionists, psychologists, and neurophysiologists. A thorough analysis of behavior enables us to come closer to defining the principles of its organization, development, and

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S . N. KHAYUTIN

phylogenetic and ontogenetic complexity, and to discover some of its basic neurophysiological mechanisms. Despite its long history, this complex behavioral science continues to undergo changes of a general biological nature as well as in some of its details. Nowadays a systems approach makes it possible to investigate individual actions without separating them from a larger behavioral continuum, which includes also the behavioral result and the change from one activity to another. This plays an important role in the analysis of behavioral actions at different levels of organization and complexity. The study of the behavior of adult animals in many ways sets limits to the interpretation of the underlying mechanisms. For example, in such studies the possibility of making definite statements about the role of exogenous and endogenous factors in behavioral organization is limited. Studying the early ontogeny of animals enables us to examine the developing natural behavior in “uncontaminated” form before its development is complicated by an infinite variety of behavioral acts aimed at the satisfying needs. This has been shown by the efforts of many investigators (Coghill, 1929; Kuo, 1932, 1967; Tinbergen, 1953, 1965; Orbeli, 1967; Anokhin, 1964, 1974; Schneirla, 1965, 1966; Volokhov, 1968; Rosenblatt, 1970; Shuleikina, 1971; Gottlieb, 1971). At early ontogenetic stages there are usually no redundant “degrees of freedom,” which are acquired by an individual at later stages of life. Early on, only a limited number of behavioral programs are observed within the strict limits of the reaction norm. Every hour, however, they too are enriched by acquired experience and modified by environmental factors. Another advantage of the ontogenetic approach to the analysis of both behavior and its central neural mechanisms is the simple structural foundation of early behavioral responses. The system of total brain integration, which includes many central structures in adult animals (John & Morgades, 1969; Shvirkov, 1978), is limited in the newborn to only a few selectively mature structures (Anokhin, 1964; Shuleikina, 1971; Gladkovitch, 1979). The basic principles of development of functions are formulated within the concept of systenogenesis (Anokhin, 1964). This theory states that general and specific trends in the ontogeny of functional systems, especially behavioral ones, are determined by the influence of species ecological factors. The behavior itself is considered by the theory as a relationship between the organism and its environment. From this viewpoint the study of behavior must include both the analysis of the environment and of processes inside the organism, as well as an analysis of interaction between the organism and the environment (Shvirkov, 1978). That is why the study of the formation and organization of feeding and defense behavior in early avian ontogeny conducted in the natural habitat of the species is promising for an understanding of the nature of environmental influences on early forms of behavior and their development.

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This approach to early avian postembryonic ontogeny , involving analysis in the natural habitat, is intended to help evaluate the role of ecological factors in the development of the behavior and its dynamics, including that of social behavior. One special characteristic of the avian species selected, namely the pied flycatcher (Ficedula hjpoleuca), great tit (Pcirus major), and the redstart (Phoenicurus phoenicurus), is that each developing chick is surrounded by siblings in the nest. Under such conditions, information about the current state of the other chicks will affect the organizational processes of each individual's behavior. The main goal of this study was, therefore, to analyze the formation of feeding and defense behavior and the conditions eliciting them, as well as their interaction at all stages of nestling life, with features of the species' ecological environment. While analyzing these forms of behavior, we paid special attention to the dynamics of their sensory basis at the successive stages of early postembroyonic development, to the maturation of sensory mechanisms, and the time of onset of their full-scale functioning, i.e., to the intra- and intersensory heterochronics, I enabling adaptation to the ecological environment of the species. The data presented here were collected during the last 10 years in the OkaTerrace Reserve (120 km south of Moscow). The methods used in the study have been described previously (Khayutin & Dmitrieva, 1976a,b, 1978, 1981). Here we shall only note that in order to study the natural behavior of nestlings and adult birds we moved the nest 1-2 days before hatching from the simple nestbox to an experimental one which had no back wall. The experimental box was fixed on the wall of the light-protected experimental chamber which housed a researcher with cameras and tape-recorders. Behavior in the nest could thus be observed and recorded from a distance of 20-50 cm. To create an exact reference system for recording the position of the young and parents during feeding, the nest was divided into 12 sectors corresponding to the numbers on a clock face, with zone 12 situated right under the entrance hole. A further thirteenth zone was the center of the nest. Each of the nestlings bore an individual color mark. Evoked potentials from wulst and field L of awake nestlings were obtained through chronically implanted electrodes. The experiments were conducted in the laboratory but approximated natural conditions as much as possible: the nest was placed in the shielded nest-box with background noise and light levels equal to those in the wild. The nest temperature was automatically maintained constant. EMGs were recorded from the awake nestlings through wire electrodes 'According to P. K. Anokhin's theory of functional systems (Anokhin, 1964, 1974), heterochrony means a selective and accelerated development in the embryogenesis of structures differing in role and location whose functions are integrated. thus providing for the survival of newborn animals. From our point of view. the principle of heterochronic development may also be applied to individual postembryonic ontogeny.

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FIG.1 . Interior of an experimental nest-box with the nest of pied flycatcher. (a) Microphone of the tape recorder; (b) microphone of SPL meter; (c) photoelectric element.

implanted in their neck muscles. All electrophysiological data were obtained from experiments with pied flycatchers. Sounds used for communication between nestlings and adult birds were analyzed with a Kay-Electric 7029A sonagraph.

OF NATURAL BEHAVIOR I N THE NESTLING 11. ORGANIZATION

A.

FEEDINGBEHAVIOR

A T THE

BEGINNING OF NESTLING LIFE

When the nestling behavior of pied flycatchers was studied under natural conditions (in the wild), it was found that at the moment of hatching only one type of behavior had been formed, i.e., begging in response to specific acoustic stimulation. Up to the point when their eyes opened at 5-6 days this behaviorthe rapid lifting of the head with upwardly outstretched neck, beak opening, and vocalization-was elicited by the following succession of stimuli: a tap of feet on the nest-box when the parent bird arrived, a rustle of the nest material caused by the bird’s jumping to the nest edge, and a special food call emitted by it. The latter stimulus was observed in 70-75% of all feedings. Spectral characteristics of the components of this sound sequence (“the sonic complex of feeding”) are

TABLE I PARAMETRES OF SPECIES-SPECIFIC SIGNALS OF Ficedula hypoleuca (F.h. ), Parus major (P.m.),

Signals Sonic complex of feeding

Feet tap on the wall Rustle of nest material Conspecific “food” call

Alarm call

Species song

Auditory sensitivity peaks of nestlings

Species F.h. P.m. P.p. F.h. P.m. P.p. F.h. P.m. P.p. F.h. P.m. P.p. F.h. P.m. P.p. F.h. P.m. P.p. Cuckoo

AND

Phoenicurus phoenicurus (P.P.)

Spectrum (kHz)

Energy maximums (kHz)

Duration of sonic units (msec)

.I-7.0 .I-7.0 .I-7.0 .I-3.5 .I-3.0 .I-3.0 1.5-5.5 1.04.5 .54.5 4.0-6.0 1.5-4.0 2.5-5.5 1.7-5.7 2.5-3.5 2.0-3.7

1.0-3.5 .5-5.0 .5-2.0 .5 .5 I .o 1.5-2.5, 3.0-4.5 1 .O-2.5, 3.0-4.5 .5- 1 .O, 2.5-4.0 4.5-5.5 2.2-3.3 3.0-5.0 2.5-4.0 3.0-3.5 2.5-3.0 1.0-2.5, 4.0-5.0 1.0-2.5, 3.5-4.0 1.5-2.5, 3.0-3.5 .5-1 .O, 2.0-2.5

50 50 50 100 100 100

-

-

75 75 75 25 (click), 125 (whistle) 50 40 (click), 150 (whistle)

May be repeated 5-6 times

25-500

30 sec-dozens of minutes

250-500 25 250-500

-

2.5-3.0 sec 2.5-3.0 sec 2.5-3.0 sec

50-100 -

Duration of the whole signal

Interval between sonic units (msec)

-

-

-

-

-

-

-

-

-

-

-

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presented in Table I and Figs. 2 and 3. The temporal parameters of the complex were as follows: the tap of feet, 25-100 msec; the jump to a particular place (fixed for each bird) on the nest edge, 10-50 msec; the rustling sound, 25-100 msec. Having placed itself in the nest the bird would immediately emit one or several food calls lasting together 25-150 msec. Thus it took the bird about 400 msec to reach its fixed place in the nest and be ready to feed the chicks; this period corresponds to the maximum begging latency for nestlings with an optimum level of feeding motivation. In other words, by the time the bird took its place on the nest edge ready for feeding some of the nestlings were already actively begging. But as a rule only one of them received food, namely the one occupying the zone optimal for reinforcement. The duration of one feeding act was 2 . 8 2 . 3 sec. The timing of the parent bird’s arrival showed that it returned with food every 30- 150 sec during daylight hours. An earlier study (Khayutin & Dmitrieva, 19764 demonstrated that nestlings begging in different nest zones had an unequal probability of reinforcement, this probability depending on the place occupied by the parents during the feeding (Fig. 4). Within each day and during the entire nest period all six to eight nestlings of a brood received statistically equal amounts of food in spite of the unequal probability of reinforcement in the different zones. This equal distribution was due to a special behavioral phenomenon: the circular shift of the young in the nest during the first half of the nesting period. Later this rotation was transformed into moving across the nest along the light gradient that existed in the nest from the very beginning. Having received a portion of food in a certain

Duration (sec)

FIG.2. Contour spectrograms of signals of adult birds affecting the behavior of nestlings. (A) Sonic complex of feeding: (a) foot tapping on the nest-box; (b) rustle of nest material; (c) species-specific food call. To the left of (a), wing noises during the approach of the bird. (B) Species-specific alarm call.

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Frequency (kHz)

FIG. 3. Energy sections of the signals presented in Fig. 2 (along the lines a-a,, b-b,, c-c,, d-d,). Various signals emitted by different pied flycatchers are presented.

zone a nestling would return to it after some time (this interval is constant for each age). As birds in the majority of cases of arrival with food fed only one of the young, it is suggested that the nestling with the highest level of feeding motivation would usually be reinforced. The same phenomenon has been observed in studies of other species, e.g., field sparrow (Spizella pusilla), Best (1977); great tit (Parus major), Khayutin and Dmitrieva (1978), Bengtsson and RydCn (198 l), redstart (Phoenicurus phoenicurus), Khayutin and Dmitrieva (1978); song thrush (Turdus merula), Bengtsson and RydCn (1981). Electromyographic analysis correlated with begging behavior revealed that the EMG in all instances was characterized by no less than two phases of activation

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FIG.4. Probability of the begging success in each zone of the nest. 0 6,Places taken by the parents during feeding; e, entrance hole. The probability is represented by the figures in the upper diagram.

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(Fig. 5). The first phase reflected the begging itself (i.e., adequate posture, beak opening, etc.), while the second phase reflected the movements of the young that followed (i.e., change of position in the nest whether food was received or not). Considering that each arrival of a parent elicited begging in SO-100% of the young, it is suggested that the phenomenon of the circular shift would be a result of the second phase of begging by these very nestlings, whereas the rhythmic and monotonous organization of the rotation is determined by the individual characteristics of the reactions composing it. One of the factors in this is the asynchronous onset and development of begging due to the different levels of feeding motivation of nestlings at any given moment. On days 5-6, the eyes of the nestlings started to open: on the fifth day a narrow slit appeared during begging, on days 7-8 their eyes were fully open during begging but the lids were half closed at other times. The set of stimuli eliciting begging changed accordingly. The species-specific food call was not used any more because begging started in response to the tap of feet on the box when the parent arrived with food, and the short-term change in light intensity caused, as before, by the parent bird’s body closing the entrance hole. A soundless, artifical change of light level also provoked normal begging in 5- to 9-day-old young. When the the parameters of the light stimuli which induce begging were investigated in the field, the following data were obtained: the background luminosity (- 300 lux) dropped to 3-5 lux and remained at that level for about 100-200 msec while the bird was moving through the hole into the box, then returned to its initial level. Thus a

FIG. 5 . Biphasic (A) feeding reaction of a nestling with intermediate level of feeding motivation, and polyphasic (B) reaction of one with a high motivational level. Both reactions were elicited by the food call (upper traces) reproduced from a loudspeaker.

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visual stimulus adequate for begging of 5- to 9-day-old nestlings is a twocomponent luminosity change of 1.5-2.0 log units lasting 100-200 msec, consisting of a decrease followed by an increase. Figure 6 illustrates the change of begging latency during the satiation-hunger cycle in 5- to 9-day-old young. Light flashes of standard intensity and duration (2 log units, 150 msec) were produced according to a schedule derived from field studies and based on the timing of parent arrival with food. It was found that reactions to these visual stimuli also involved two phases and that their latencies changed with the change in the level of feeding motivation. After reinforcement with a standard portion of food the next few responses would be either at a very short latency (80-100 msec) or a more prolonged one (300-400 msec). During the following 5-10 min a nestling did not react to the 8-15 stimuli presented. Then the reactions reappeared, the latency of EMG activation gradually became shorter, until it stabilized at the minimal level. When the latency of begging was approaching its minimal value, the second phase of activation of the repeatedly unreinforced reaction began to separate into fragments and to grow longer; 2-4 subphases, or even more, were observed in the EMG. An average time interval from one period of EMG latency stabilization at the minimal level till the onset of

Ah

Interval after feeding (rnin)

FIG.6. The change in begging latencies (according to EMG analysis) during the satiation-hunger cycle. (a-c) Motivation levels (see text); (0)5-day-old nestling; (0)9-dayold nestlings. Arrows: feeding episodes. Vertical bars on the graphs here and below ?SD. n= 12 nestlings of each age.

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the next one nearly corresponded to the averaged full cycle of the nestling’s movements round the nest. Thus it corresponded to the interval between two feedings of the same chick under natural conditions. The correlation between the behavioral activity of nestlings under natural conditions and the dynamics of EMG activation in the laboratory experiments suggests that the latter adequately reflects the fluctuations of feeding motivation within the satiation-hunger cycle. Moreover, the analysis of EMG activation dynamics reveals three levels of motivation in this cycle: ( I ) the highest level, involving minimal latency of EMG activation [between 80 and I10 msec, mean 106.6k 17.7, the second phase of activation polyphasic (Fig. 6a)l; (2) the intermediate level [EMG activation latency 160-250 msec, mean 204.0k26.3 msec, the second phase monophasic (Fig. 6b)l; (3) the lowest level, at which low level light flashes fail to stimulate begging, so EMG activation is not exhibited (Fig.6~).

B. PASSIVE-DEFENSE BEHAVIOR At the same time as eye opening and the change in the modality of triggering stimulation for begging occurred, the behavioral repertoire of the nestlings became inore complex. From then on a passive-defense reaction appeared in response to an alarm call emitted by the birds outside. This reaction was the cessation of begging and other movements (freezing) during the time the alarm call sounded and terminated 30-60 sec after the signal had stopped. The speciesspecific alarm call of the pied flycatcher consists of one or two types of sounds, clicks, and whistles (Khayutin & Dmitrieva, 1976b; Curio, 1975). In general, these calls occurred as an almost rhythmic succession of sounds. The repetition rate of sounds emitted by one bird was about 2/sec. When both parents simultaneously reacted to danger the repetition rate would increase to almost 4/sec. The parameters of the pied flycatcher’s alarm call are presented in Table I and in Figs. 2 and 3. During the field studies we found that alarm calls abruptly stopped nestling vocalization and blocked begging in response to specific (visual) stimuli. This suggests that the biological role of the passive-defense reaction of tree hole nestlings is to inhibit a vocalization which appears with increasing feeding motivation. The experiments with EMG as an index of the nestlings’ motor activity confirmed this hypothesis. A chick with a high motivation level demonstrated increased motor activity accompanied by a loud constant vocalization with a repetition rate of up to 1.5/sec. The presentation of an alarm call previously recorded in the wild via the speaker immediately caused the flattening of EMG, reflecting the decrease of motor activity and tightening of the muscles that occur during freezing. Vocalization also stopped after the first few seconds of alarm call presentation. When alarm and food calls were presented simultaneously, the

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resultant behavioral effect was found to be the appropriate reaction to one or the other; which of the two reactions occurred depended upon the gradually increasing level of feeding motivation. Signals presented simultaneously to nestlings with intermediate levels of motivation induced the passive-defense reaction. Nestlings with high motivation levels (but within its natural limits) also demonstrated a defense reaction. However, when duration of the alarm call presentation greatly exceeded an average interval between two successive feedings of the same young, food calls began to elicit begging in spite of the alarm call, although this reaction lacked the vocalization component. In the nestlings with the highest motivation level the defense reaction was completely suppressed by the begging response, and the latter exhibited its normal integration. Thus the results of this study point to the close interrelationship between these two reactions and this, in turn, makes possible the suggestion that the passive-defense reaction is incorporated in the tree hole nestling’s behavior repertoire on days 5-6 because of the great increase of vocalization intensity at this stage, and that its principal biological function is to inhibit vocalization. With the formation of these two behavioral integrations (begging and defense) the song of the species, which did not influence nestlings’ prior behavior, began to play an important role. From then on, and until the end of the nesting period, the adult male’s song modulated the level of sensory, motor, and emotional activity of the young, facilitating the transformation of one behavioral pattern into another. It also acted as a signal of safety, as an influence opposite to alarm calling (Khayutin, Grinchenko, & Dmitrieva, 1978).

C. FEEDINGBEHAVIORAT

THE

ENDOF THE NESTLING PERIOD

In spite of both the change in the set of natural stimuli eliciting begging and the incorporation of the passive-defense reaction into the behavioral repertoire of the young up to the eighth day, no change in the zone occupied by parents for a forthcoming feeding, or of the zone where begging was most often reinforced, was observed (see Fig. 4A and B). Between the eighth and thirteenth days after hatching the begging of the nestlings was caused by the closures of the hole by the body of the adult bird. During this stage the young lifted their heads with wide open beaks not vertically upward as before but in the direction of the parent’s head, actively attacking its beak to snatch the food away. Thus the nestlings got to the food before the adult had time to move from the hole and take its place on the nest edge, so that from the ninth day of life nestlings sometimes got food from the parent sitting in the hole. The percentage of such feedings gradually increased, reaching 80% by the twelfth day. The distribution of the zones where nestlings got food changed accordingly. An analysis of this new form of food acquisition behavior revealed that it was organized on the basis of two stimuli: triggering caused by a change in light

ALTRlClAL BIRDS

I17

level, and guidance provided by the moving silhouette of the parent. Specially designed experiments confirmed the different roles of these two stimuli in the organization of the food acquisition response of nestlings at that age. The mere drop in light level appeared to elicit only a weak reaction, ceasing in 1-1.5 sec, whereas the movement of a conelike object imitating the parent’s silhouette provoked the young to turn their heads with their gaze following the stimulus, but without the characteristic begging posture, beak opening, and vocalization. Exactly the same reaction as to the conelike object without a decrease in illumination was observed in response to the arrival of a parent with food when an artificial source of light was introduced into the nest-box, thereby increasing the light level far beyond the limits of the normal level; under such conditions the closure of the hole by the body of the bird resulted in no drop in luminosity at all. During this period (days 8- 13) the circular shift of the nestlings lost its regular character. Their feeding behavior became more and more closely connected with the light gradient in the box. Not only the luminosity change accompanying the arrival of a parent but also the background light level started to play an important role in the feeding behavior of the brood. At this time the feeding motivation cycle appeared to be “tied” to the light gradient constantly present in the box. Naturally, the best lit region of the nest included zones situated directly under the hole; the sides of the nest were less lit, and the most dimly lit zones were those near the rear wall of the box, with a luminosity difference between different areas in the nest possibly as great as 1 log unit. The zones directly under the hole were optimal for food reinforcement during this period; these were the zones with the highest background light level and most marked drop in luminosity resulting from the adult’s arrival. A young with a high motivation level “sought” to occupy those zones while the replete nestlings left them immediately after feeding to move to dimly lit zones. When feeding was interrupted for a long time by natural or artificially created obstacles, all nestlings huddled in the zones with maximal luminosity. Conversely, after frequent feeding (when the parents were compensating for a long natural or artificial break) all nestlings, being satiated, left these zones to huddle in the dimly lit area of the nest. Quite as in the preceding period, the trajectory of each chick depended on other nestlings’ movements in a complicated fashion; nevertheless the active goal-directed component of movement was apparent: when hungry, toward well lit zones, when replete, away from them. So that during this period light became the leading factor in feeding behavior, which naturally loosened the tie between individual movements and the integrated activity of the brood and also destroyed the strict organization of the circular shift. The cycles became shorter and the young often moved along the axis of the nest only toward maximal light intensity. At the last stage of nest life (days 13-15) begging occurred whether the feeding was preceded by the short-term light intensity change or not. At that time only the moving adult could elicit begging and the light change lost its effective-

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N.

KHAYUTIN

ness. Parents fed only from the hole, consequently the zones optimal for reinforcement were situated directly below the hole. Begging could then be artificially induced by moving the conelike object imitative of the parent’s silhouette on every occasion.

D. CONCLUSIONS This study has revealed the principal sensory factors that determine the feeding and defense behavior of nestlings in the natural habitat. It also shows their connection with the feeding motivation level throughout the whole of nestling life. As to the change of the sensory basis of the nestlings’ feeding behavior, four distinct periods may be distinguished during the nestling phase.

I . During the first phase, from hatching until the eyes open (days 0 to 5-6) the feeding reaction is elicited by the complex of wide-band sounds which occur in succession as the parent arrives at the nest. 2. After eye opening (days 5-9), the main stimulus for feeding behavior changes to a passive-defense reaction. During this period a short-term light change with intensity of 1.5-2.0 log units and of duration 100-200 msec appears to be the stimulus for feeding behavior. This permits the hypothesis that during that period (limited to 5 days) only those receptive fields are functioning in the nestling’s visual system that are adequately stimulated by a diffuse change in light level. It is important to note that such receptive fields are actively involved in the organization of goal-directed feeding behavior and, moreover, are sufficient for such organization. The passive-defense reaction is induced by the alarm call, which consists of rhythmically organized signals. 3. During the next period (days 9-13) feeding behavior is modified. The reaction, initially a passive begging, turns into an active food-acquisition response. At the same time the phenomenon of circular shift of nestlings in the nest (the basic mechanism underlying the statistically equal distribution of food) is transformed into the traversing of the nest along the light gradient. Two stimuli of the same modality are now involved in the organization of feeding: a triggering stimulus (diffuse light change) and a guiding one (the silhouette of the moving adult). 4. During the last period of nestling life (days 13-15), the nestlings’ foodacquisition response is induced only by the movements of a parent entering the nest-box. The passive-defense reaction is still provoked by the alarm call.

111.

DEVELOPMENT OF ACOUSTIC SENSITIVITY

It has been established that the principal forms of behavior of altricial nestlings are rather closely connected with species-specific acoustical signaling (Messmer

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& Messmer, 1957; Milyagin, 1957; Royama, 1966; Khayutin & Dmitrieva,

1976b, 1978). For instance, the very first begging after hatching in many species is induced under natural conditions only by the food call emitted by the parents and remains unchanged for the next few days. This form of behavior was called “inborn conditioning” (Anokhin, 1964, 1974). An analysis of such behavior enabled us to state only that the auditory perception of the nestlings is selectively accelerated in the frequency range of species-specific signals during development (Milyagin, 1957; Khayutin & Dmitrieva, 1978; Golubeva, 1980; Tikhonov & Fokin, 1981). However, independent investigations of acoustically guided behavior and of the formation of the avian auditory system by electrophysiological means did not yield enough material about the central mechanisms of inborn conditioning. This part of our research was designed to analyze the dynamics of avian auditory perception during early postembryonic development and to link it to the analysis of the organization and appearance of natural acoustically guided behavior. A.

POTENTIALS AUDITORY EVOKED

It has already been mentioned (Section 11) that two of the principal behavior patterns of nestlings during early life are based on acoustic signaling in the frequency band from , l-7 kHz (see Fig. 2). The study of the range and dynamics of audition in I .5-to 7.5-day old nestlings, by examining the occurrence and characteristics of evoked potentials (EP) in field L (the highest acoustic center of birds; see Leppelsack & Vogt, 1976; Saini & Leppelsack, 1977; Bonke, 1978; Kelly & Nottebohm, 1979), was carried out simultaneously with recordings of behavior. The study was based on the presentation of pure tones with frequencies within the aforementioned range (with steps of .5 kHz) as well as of natural species-specific signals. During the recording of field L EPs in response to pure tones at different sound pressure levels (SPL), three age groups of nestlings were discovered which differed in the range of frequencies for EP generation. 1 , Nestlings 1.5-2.5 Days Old

EPs to pure tone stimulation were recorded only in response to frequencies from .l-4.0 kHz (Fig. 7). The EP consisted of three constant components: PI N , and P, (first positive component, P,; first negative component, N , ; second positive component, P,); their latencies and amplitudes depended on the frequency of the signal and its SPL (Fig. 8). The SPL required for the occurrence of a response had a minimal value in the frequency band .5-2.5 kHz. The EP in response to a food call was characterized by the shortest latency, the minimal threshold SPL required for its occurrence, the inclusion of two additional components following P, and a longer duration than the responses to pure tones. The presentation of pure tone signals at the minimal SPL showed that EP

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FIG.7. Evoked potentials in response to pure tones and the food call (in the center, sonogram of the food call used in the experiment). Each panel: above, EP; below, EMG; left in each pair, EPs to suprathreshold signals (2-5 dB above the response threshold); right, to the signals of behavioral threshold intensity: for the frequencies 1-4.0 kHz and food call. Right column: left, EP in 1.5- to 2.5-day-old nestlings; right, in 3.5-day old nestlings, P,, N , , P2, phases of EP. Downward deflection, positivity.

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Frequency (kHz1

FIG.8. Frequency-threshold auditory curves for nestlings of different ages (A), and spectra of the signals eliciting the behavior (averaged sections of the signals presented in Fig. 3). (B).(A) EP thresholds to tones of different frequencies in 1.5- to 2.5-day-old 2.5-4-day old (0- -O), 4- to 7.5-day-old nestlings (@---a), and behavioral thresholds in 1.5- to 7.5-day old nestlings (0-0). (B) (a) Foot tapping; (b) food call; (c) alarm call.

(o--o),

generation thresholds did not change significantly with the functional state of nestlings. Threshold SPL stayed constant for the responses to stimuli throughout the whole frequency range effective for nestlings of this age under light nembutal anesthesia ( 10- 12 mg/ 100 g given intraperitoneally) or when EPs were recorded during evening and night hours, i.e., after the end of the daylight feeding period. In addition, it was found that the EP generation thresholds averaged for each frequency did not depend upon the current level of nestling feeding motivation. Throughout the whole satiation-hunger cycle (see Section II), lasting about 1825 min for nestlings of this age, the threshold SPL for EP generation remained constant both for each frequency of pure tone and for the food call.

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When the SPL exceeded the threshold, nestlings manifested begging reactions throughout the entire frequency band effective for EP generation. However, the parameters of these reactions (latency and duration, calculated from EMG), and the repeatability of the response to identical signals, depended, as would be expected, on the motivational level, and on the physical characteristics of the stimuli. Here only those reactions will be discussed which occurred when feeding motivation was stabilized at the maximal level (i.e., in response to stimuli presented during daylight hours and 18-30 min after the nestling had received a standard portion of food). Threshold SPL for each frequency to produce begging in such nestlings appeared to exceed the thresholds for EP generation by 13 dB at 1.5 kHz and as much as by 35 dB at .1 kHz. The probability of a reaction occurring to the pure tones of threshold intensity also depended on frequency. When the intensity of stimulation was 2-5 dB above the threshold, the probability of response was about .75-.8 at frequencies of 1.0 and 3.0 kHz. The probability of response to the food call reached .8-.9. Latency of the EMG component of begging averaged for the tonal and species-specific signals (at the same threshold SPL) in the entire experimental group of nestlings of these ages was 109.2+ 12.7 msec. Most short-latency EMG activations started synchronously with the N , peak; in other instances the onset of activation was confined to the N,-P, descending branch, or activation started after the EP was over (see Fig. 7). Thus in 1.5- to 2.5-day-old nestlings, testing throughout this auditory range (. 1-4.0 kHz), defined according to the EP generation index in the highest integrative structures of the auditory system, auditory perception appeared to be closely related to the only form of acoustically guided behavior that appears to be organized at the moment of hatching. However, within this range the sensitivity to different frequencies and the connection with the organization of feeding behavior differed greatly. Considering that EPs to stimuli with frequencies between .5 and 2.5 kHz occurred when the SPL was minimal, and that the difference between the intensities effective to induce begging and EP was smallest in the same range, it seems that the auditory perception of 1.5- to 2.5-day-old nestlings is most completely formed in this range, and that in this range it plays an important role in behavioral organization.

2. Nestlings 2.5-4 Days Old The spectrum of perceived frequencies widened to 6.0 kHz in 2.5- to 4-dayold nestlings. EPs to the tones in the range 4.5-6.0 kHz first appeared by the end of the 3rd day of life. SPLs effective for the occurrence of the threshold EPs to these tones are presented in Fig. 8. Begging in response to the signals of these frequencies was never observed, whichever intensities were used. EPs to thresh-

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old signals with frequencies of .I-4.0 kH7 and to the food call showed no detectable changes from the earlier age. All the main EP characteristics in response to the frequencies inducing begging, and also behavior guided by sound itself, did not change during this period. 3. Nestlings 4-7.5 Days Old EPs were recorded in response to stimulus frequencies up to above 8 kHz. As compared to the preceding age groups the changes in auditory perception characteristics were most marked here. The SPL required for threshold EP generation decreased significantly in the range 2.5-4.0 kHz and the range of high sensitivity was extended to 4.5-5.0 kHz (Fig. 8). EPs to species-specific signals became consistently triphasic. During this period, however, no changes in any of the parameters of acoustic sensitivity in the range of .5-2.5 kHz were observed. Minimal SPL effective for EP generation by tones in this range did not differ from that defined for previous age groups. The pattern of feeding behavior as a whole also did not change, even though during this period the nestlings’ eyes opened and so the modality of triggering stimulation of this behavior changed. As may be inferred from Fig. 8, absolute values of SPL, which were effective throughout the whole frequency range for the organization of alimentary behavior, remained constant in the third period.

B . RECOVERYC Y C L E S

OF A c o u s T l C

EVOKED POTENTIALS

Data about the degree of maturation of the nestling auditory mechanisms which are responsible for analysis of the frequency spectrum of food and alarm calls were obtained from the studies of recovery cycles (recovery of excitability) in structures at the highest integrative level of the auditory system. Nestlings were presented with pairs of tones of equal frequency and intensity separated by different time intervals. It was found that in I .5- to 2.5-day-old nestlings the first signs of response recovery to the second test stimulus were observed after intervals between 500 and 750 msec. Full recovery of EP components to tones corresponding to the energy maxima of food calls occurred after 750- 1250 msec, whereas the recovery of response components near the upper limit of auditory sensitivity, i.e., 3.5-4 kHz had reached only 65575% by this time. In nestlings of the second age group the time of full recovery of response components to frequencies in the food complex range decreased to 350-500 msec and to 500-700 msec in the case of higher frequencies. The first signs of recovery of responses to all frequencies analyzed were seen at intervals of 150 msec (Fig. 9A and B). In nestlings of the third age group the response recovered completely after an interval of 90 to 150 msec (Fig. 9C and D). But the degree of recovery of responses to stimuli separated by a 90 msec interval depended on the frequency

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1 .o

1.5 2.5

3.0 4.0 4.5 5.5

FIG. 9. Averaged EPs in response to paired tones of different frequency (figures on the left in kHz) with the interval 90 (A, C) and 150 (B, D) msec in 3.5- to 4-day-old (A, B) and 6.5- to 7-day-old (C, D) nestlings. Signal duration: 40 msec, black bars below.

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of the stimulus. The amplitude of the second response to a frequency of 1 .O kHz exceeded the amplitude of the conditioning response by 5- 10% while the recovery of response to 5.5 kHz was never more than 45-55%. After 150 msec the response amplitude had recovered almost completely in the high frequency range and with 1 5 2 0 % overshoot for stimuli at low frequencies.

C. HETEROCHRONOUS MATURATION OF FREQUENCY CHANNELS The above analysis of the dynamics of auditory perception, judged by the occurrence of EP to different frequencies during ontogeny, and the analysis of the degree of maturity of nestling central auditory mechanisms, judged by recovery of excitability, showed that different frequency channels responsible for the analysis of species-specific signals linked to the principal nestling behavior patterns developed at different rates. Numerous facts confirm this suggestion. As seen in Fig. 9, EPs to the low-frequency tones consisted of more short-latency low-amplitude waves than the responses to high-frequency tones. Maksimova (1979) proposed that the early response components, which are best seen in the averaged EPs, reflected the activity of modality-specific brainstem structures. The fact that the responses to high frequencies lacked such components may point to the immaturity of the whole complex of central-peripheral elements responsible for the analysis of these frequencies. Moreover, it was found that response latencies in all age groups depended on stimulus frequency. However, this dependence was somewhat paradoxical. In spite of the fact that in all age groups the responses to low-frequency stimuli were similar in many respects (amplitude, set of components, duration of recovery cycles) to the activity of more mature structures, and were more similar to the mature EPs, their latencies exceeded those of responses to high frequencies. Thus the responses to low- and high-frequency stimuli differed in many characteristics of their EPs both in developing and mature animals. All data show that at each stage of development of avian auditory mechanisms the frequency channels responsible for the processing of low and high-frequency signals have achieved different levels of functional maturity: the structures responsible for the processing of low frequency tones are formed with greater speed at all stages. That is why at the moment of hatching nestlings already have sensitivity in the frequency range of “sonic complex of feeding,” and thus the nestlings are capable of normal feeding reactions in the very first days of life. The sensitivity to the adult alarm call forms later: approximately 2 days before defense behavior appears. D.

AUDITORY SENSITIVITY AND BEHAVIOR

The comparision of the nestling’s auditory sensitivity (Fig. 8A and B ) demonstrates that during even the first period (1.5-2.5 days of age) the range of lowest

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thresholds for auditory perception corresponds in general to energy maxima in the sonic complex of feeding, whereas thresholds to sounds within the alarm call frequency range are still difficult to establish. The main characteristics of the EPs to pure tones in the food frequency range remain constant throughout the whole period of ontogeny during which this form of behavior is manifested. However, the characteristics of EPs and their threshold in response to pure tones of the same frequencies as the maxima of the alarm call change significantly during the first 4 days of life. All this leads to the conclusion that the formation of auditory sensitivity in the frequency band of .I-2.5 kHz is complete before hatching but the sensitivity to higher frequencies is still developing even during the first days of postembryonic life, reaching its mature form two days before the onset of the passive-defense behavior based upon these frequencies. As has been established, thresholds of EP generation do not depend upon all the factors influencing the organization of begging i.e., they are not affected by levels of motivation and arousal and the current phase of daily activity. At the same time, behavioral thresholds do depend on these factors. Thus these two indexes must reflect different aspects of auditory perception and its connection with the organization of behavior affected by sounds. The former reflects the level of absolute auditory sensitivity and its age-related characteristics, while the latter shows the fixed connection of auditory perception with the display of inborn conditioning. This assumption makes it possible to explain the fact that behavioral thresholds exceed thresholds of auditory preception defined according to electrophysiological indexes. However, many studies have shown that thresholds of auditory sensitivity in mature animals and humans, when defined with behavioral tests (using conditioned reflexes, reports by subjects, etc), are usually below or equal to those defined on the basis of electrophysiological analysis of activity in different structures of the auditory system (McCondless & Best, 1964; Saunders, Colles, & Gates, 1973; Dallos, Harris, Ozdamar, & Ryan, 1978; Dooling & Walsh, 1976). This phenomenon may be accounted for by the fact that a behavioral reaction may be based on the involvement of very rare lowthreshold elements and the chance of finding them with electrophysiological methods is extremely small (Baru, 1978). Considering this possible explanation we may suppose that the performance of an inborn behavior of vital importance elicited by sensory stimulation requires not only integration of relevant sensory input within brain structures controlling feeding (formed before hatching), but also a powerful modality-specific inflow. Naturally, such an input cannot be provided by the activation of only a very limited number of low-threshold elements. Thus one of the factors that increases the chances of occurrence of inborn, ecologically determined behavior in response to biologically meaningful stimuli is the inclusion of many sensory elements with different threshold characteristics in the integration. Other factors increasing the likelihood of response are the

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match between the physical characteristics of signals and the frequency characteristics of the elements involved. It was noted above that the feeding behavior of nestlings under natural conditions is controlled not by a single sonic signal but by the whole complex, the components of which have different frequency-energetic characteristics. Figure 8 shows that the spectral composition of the sounds as a whole corresponds to the range of the frequencies perceived by nestlings on the very first days of life when only this behavior pattern is present. The overall frequency range of the sound complex is . l-5.0 kHz with the most pronounced components at .5, 2.0, and 4.0 kHz. The best auditory sensitivity of nestlings is in the range .5-2.5 kHz, while the begging is most efficiently induced (as shown by maximal probability of repeated occurrence in response to repeated stimulation and by minimal effective SPL) by .5, 1.5, 2.5, and 3.5 kHz signals. From this finding we can conclude that although the ranges of auditory sensitivity generally coincide with the frequency composition of signals, narrow sensitivity peaks do not match the limited dominant signal bands, and thus there is no strict accordance between them. In the study of altricial nestlings of other species the nonmatching of the ranges of maximal sensitivity with the dominant frequencies of species-specific signals has also been demonstrated (Golubeva, 1980). Comparison of the threshold characteristics of audition in one-day-old nestlings of precocious species with the parameters of species-specific signals meaningful for behavioral organization revealed that at the moment of hatching the development of sensitivity has been completed and its peaks are strictly correlated with the dominant frequencies of the signals (Gottlieb, 1965; Konishi, 1973; Saunders, Gates & Colles, 1974). It may be assumed that the differences in sensitivity of altricial and precocious nestlings are determined by their ecological environment, which appears to be a modulating factor in the development of hearing. The posthatching development of precocious nestlings occurs in an “open” acoustic environment and the acoustic contact between them and their parents is maintained over a significant distance. The “peak to peak” matching of nestlings’ auditory sensitivity to the dominant range of the parental signaling spectrum will greatly increase the certainty of communication in such cases by providing relative insulation from the surrounding noises. Communication of altricial species is founded on another basis. All sounds of the complex need travel only a short distance as the recipient is situated very close (3-10 cm) to the source of a sound which spreads in the limited, closed space. Under such conditions the general correspondence of the auditory sensitivity to the spectrum of signals which are redundant in content, frequency, and intensity, is quite enough to meet the needs of producing a single behavior pattern. In contrast to the complex of food signals, an alarm call emitted by the parents from a considerable distance from the nest reaches the recipient in a rather weakened form. Thus the auditory system of nestlings must possess different qualities to make use of it. Considering the important biological role of this

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signal (Khayutin et ul., 1978) we may suppose that at the time of organization of defense behavior nestlings must have a well-matured mechanism for the recognition of this call against the background of other environmental sounds as well as their own vocalizations. This mechanism has been found to be the accelerated development (maturing 2 days prior to the occurrence of this behavior) of the narrow sensitivity peak around 4.5 kHz which exactly coincides with the dominant frequency of the alarm signal. Additional factors increasing the certainty of perceiving this signal are its long duration and perhaps also its rhythmic structure. It is known that distance communication signals used by mammals have a rather narrow spectrum with clearly marked formant frequencies exactly matching the ranges of maximal auditory sensitivity (Konstantinov & Movchan, 1978). In the case discussed here, however, signals of “close” and ‘‘long-distance’’ action both have wide-band spectra and the identification of the latter is based, to a large degree, on the narrow maximum sensitivity to its dominant frequency. Thus two forms of acoustically guided behavior following one another early in life (i.e., sound-induced feeding and defense behavior) are based on different principles of selectivity by the nestling’s auditory system, although the relevant signal spectra partially overlap. There is no ambiguity of response for two reasons: (1) the onset of defense behavior coincides with the cessation of acoustic signaling during feeding behavior, and (2) 2 days before the onset of defense behavior the auditory sensitivity thresholds (judged by EPs) are rapidly increased for the range of 3.0-4.0 kHz connected with the feeding reaction. As the behavioral thresholds of begging in this range remain unaltered, an increasing gap is formed between the absolute thresolds of auditory sensitivity and behavioral thresholds of the feeding reaction. All this may prove to be due to the accelerated development and accentuation of one of the auditory sensitivity channels relevant to the newly emerging pattern of behavior.

Iv. ROLE OF AUDrTlON IN THE ORGANIZATION OF

DEFENSEBEHAVIOR

It has already been demonstrated (Section 11) that food and defense signals differ not only in frequency but in many other acoustical parameters as well. So we thought it important to define the critical acoustical characteristics of these signals as they elicit these two forms of behavior with different biological roles in altricial nestlings. While investigating the juvenile behavior of precocious birds, Gottlieb (1974, 1979) established that the specificity of the mallard duckling’s (Anus pluryrhynchos) behavioral responses was determined by differences in the frequency modulation pattern of the assembly call whereas response specificity in Carolina wood duck ducklings (Aix sponsu) was determined by the signal repetition rate. Later it was found that the repetition rate was the most important

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acoustic characteristic for newly hatched ducklings to discriminate the assembly calls (inducing vocalization and approach) from the reconnaissance calls which suppress locomotor activity and vocalization. The signal frequency and frequency modulation pattern played secondary roles in the discrimination between these signals (Gottlieb, 1979). Miller (1980) discovered that the reconnaisance signals of wild ducks differed from the assembly calls in their frequency modulation pattern, lower dominant frequency, greater duration of sound elements and much lower repetition rate; 1.4/sec as compared to 3.7/sec. However, only the repetition rate has been discovered to be important for ducklings to discriminate between conspecific assembly calls and reconnaissance calls. The presentation of the latter with a repetition rate of 3.7/sec caused approach and vocalization in ducklings, which were immediately suppressed by the presentation of assembly calls at a lower repetition rate ( I .4/sec). The present investigation was designed to define the critical acoustic parameters of tonal signals that effectively imitate the alarm call. Preliminary experiments were expected to reveal whether pied flycatcher nestlings use a frequency or repetition rate to identify signals of different biological significance (we also considered the possibility that both parameters might provide information). To clear up this question the following test was used: during EMG recording 5 - to 7.5-day-old nestlings were presented with a succession of pure tone signals in the frequency range of the alarm call (5.0, 5 . 5 , 6.0, and 6.5 kHz) with different (but constant in each stimulus series) repetition rates of .2, .4. .6, . 8 , 1.0, 1.2, and 4/sec. The effectiveness of the tones of the alarm call frequency spectrum (5.0-6.5 kHz) appeared independent of the repetition rate only within a limited range. As Fig. 10 clearly demonstrates, the tonal signal matching one of the dominant alarm call frequencies (5.5 kHz) effectively induced defense behavior when repeated .8-4/sec. When the repetition frequency was decreased from . 8 to .2/sec, the general motor activity and vocalization of nestlings increased and almost reached the background level observed without the controlled stimuli. Thus the results of this study testify to the important role of frequency of the tones in the process of alarm call identification by nestlings. Nevertheless, signal repetition rate is also to some extent important for the organization of the defense reaction, since the signals of the alarm call frequency interspersed by too long intervals are only slightly or not at all effective for the maintenance of defense integration. To find additional evidence for the suggestion that signal frequency is the critical acoustic characteristic for eliciting a defense reaction, another experimental series was conducted. As tones of appropriate frequencies (frequency range of the alarm call) with repetition rate of .8-4/sec appeared to be the most effective for the defense, it was decided to use the signals of the same repetition rate but in the frequency range of the food complex and thus investigate their role for the organization of feeding behavior.

S. N. KHAYUTIN

No stimulation

Stimulus repetition frequency (sec-' j

Alarm call

FIG. 10. Level of general movement activity (total time of all EMG activations summed throughout each series) of the nestling (0- -0)and the activity directly related to the rhythmic signal (the time of EMG activations related to the stimulus presentation summed throughout each series) of the alarm call range (0-0) with different repetition. Data collected over 270 sec epoch (20 series each lasting 270 sec, 6 nestlings, 47 series).

After 30-60 sec of background EMG recording during the presentation of rhythmic signals of the alarm or food frequency (in the interval between two successive signals), the frequency was abruptly changed (from food to alarm or vice versa). Under such conditions when the frequency changed from 6.0 to 3.0 kHz with the same repetition rate of 2/sec the level of general motor activity increased rapidly (in 2- 10 sec), vocalization started, and nestlings began to produce feeding reactions. In the opposite situation, when the tonal frequency was changed from 3.0 to 6.0 kHz, begging stopped during the very first seconds and a minimal level of motor activity was maintained until the signal was terminated (Fig. 11). Thus the results of this experiment confirmed that tonal frequency of signals is the main factor for differentiation between the two kinds of signals which elicited behavior patterns of different biological function. Signal repetition rate does not play such a role, but it is reasonable to suppose that it is important for the tonic maintainance of either behavior pattern. It seemed likely that an investigation of the dynamics of recovery cycles in brain structures at the highest integrative level of the avian auditory system (field L) in response to tones of different frequencies would yield further information

131

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1

A

2

C

1'

2'

WLI.

.L.

ll*L.

50 pV ._I

1 rec

FIG. 1 1 . EMG of three nestlings (A, B, C) after a sudden change in the rhythmic tone frequency, repetition rate being constant. (A, B, C) ( I ) EMG; ( 2 ) timing of stimuli (3 kHz, downward deflection); (6 kHz, upward deflection). Lower traces on (C), direct continuation of the upper ones; vertical double bars divide thrce fragments of one series.

on the role of signal repetition rate in the organization of defense behavior. Changes in the amplitude of the main EP phases in response to test stimuli of various frequencies were considered in the previous section (see Fig. 9). Here we shall only discuss the dynamics of amplitude recovery of two phases of testing averaged EP to tones of 5.0, 5.5, and 6.0 kHz with different interstimulus intervals (Fig. 12). It may be seen that in all instances the time to the first complete recovery of N , is never more than 250 msec. The secondary complete recovery of the same wave is completed only by 2.5 sec. At the same time P, amplitude also recovers completely. As both components recover completely by 2.5 sec it would be natural to expect the repetition rate of .4/sec (with the tonal frequency of the alarm call) to be most effective for maintenance of the defense reaction. However, as Fig. 10 shows, this repetition rate of tones within the alarm call range is absolutely ineffective for the defense response. It must be remembered also that the optimal repetition rate of the signals in the natural alarm call is between 2 and 4/sec, that alarm calls with repetition rates lower than 1.5/sec are never observed in the wild, and that the experimental presentation of signals in the alarm call frequency range with repetition rates below .8/sec never results in the defense reaction. Therefore we have to assume that the complete subnormality period,

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%

i

120.

A

?*,

I t

80

-

-!il

I

6

E+ Em .-C .-

40-

i . , 90150 250 350

500

750

2500

Interstimulus interval (msec)

I

5

B

n

Interstimulus interval (msec) FIG. 12. Dynamics of the recovery cycles of N, amplitude (A) and P, amplitude (B) of the test response to 5.0 kHz (0-O), 5.5 kHz (0- -O),and 6.0 kHz

(o--o).

separating the secondary and primary complete recovery of N , of the test EP, impedes the organization of tonic activation necessary for the maintenance of defense integration. We found earlier that the differentiation of conspecific signals leading to two different forms of behavior in altricial nestlings was based solely on differences

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in their tonal frequencies. At the same time, the signal repetition rate in both calls also played an important but different role in the organization of the different forms of behavior. We also found that feeding and defense behavior require different levels of motor activation. As we have shown (Section It), the basis for tonic activation of feeding behavior is the constantly increasing feeding motivation in the intervals between feedings. Pretriggering integration (in terms of Anokhin, 1974), built on this foundation, is developed to form the feeding reaction under the influence of the “sonic complex of feeding.” Thus, this auditory complex acts as a triggering stimulus for feeding behavior and also maintains the reaction during the short time required to receive food (1-5 sec). The defense reaction, unlike the feeding one, is both started and maintained only under the influence of a rhythmically repeated alarm call. In this case rhythmic signals both create the pretriggering integration and maintain the behavior (sometimes during a period of many minutes). This occurs only if the signals follow each other at the intervals required for the maintenance of the defense state. Here a question arises: which interval between successive signals is optimal for maintenance of the defense response’?As demonstrated above, the effectiveness of rhythmic tones in the alarm call frequency range decreased with a repetition rate decrease from .8 to .2/sec. In other words, an interval between successive signals of 1250 msec is the greatest at which the response will be maintained. As Fig, 12 shows, the effective interstimulus interval cannot be less than 125 msec or the excitability of auditory structures will be suppressed by the preceding stimulus. Thus only an interval between 125 and 1250 msec will be effective. The same figure demonstrates that during this period the amplitude of the test response recovers completely, then decreases to 70%, whereupon a secondary increase to 80% follows. Consequently, a 70-80% recovery in the level of N , and 50-80% recovery level of P, of the test response are the minimum ones required to create and maintain a defense response. An interval of 250-500 msec, which corresponds to the optimal repetition rate of an alarm call (42/sec), occupies the central area leaving aside the zones of initial response recovery and of the succeeding recovery of N and the beginning of the zone of P, response recovery. It may be supposed, however, that the artificial signal imitating the alarm call with a repetition rate corresponding to the beginning of the P, recovery zone (125-250 msec), i.e., 8-4/sec, must be most effective in eliciting and maintaining the defense response. Only further research can indicate whether the repetition rate of 8-5/sec is more effective than the optimal repetition rate in the conspecific alarm call. If that is the case, then the ethologists’ concept (Tinbergen, 1953; Hinde, 1970) of “supernormal” stimulus will be shown to have a neurophysiological basis. Thus, in altricial nestlings (in contrast to precocial ones) the differentiation between conspecific signals giving two forms of behavior early in life is based solely on the difference in the frequency of the signals. All these findings suggest

,

I34

S.

N.

KHAYUTIN

that different heterochronously maturing frequency channels of the auditory system of altricial nestlings at certain stages of their ontogeny act as frequency detectors that differentiate between the stimuli leading to two different forms of behavior.

V.

ONTOGENY OF SOMEVISUALMECHANISMS

In studying the dynamics of visual mechanism formation we took for an index the EPs recorded from wulst-the highest integrative center of the avian visual system (Karten, Hodos, Nauta, & Revzin, 1975; Pettigrew & Konishi, 1976; Micceli, Giovanni, Reperant, & Peyrichoux, 1979; Ookawa, 1979; Denton, 1981; Bagnoli, Francesconi, & Magni, 1982). EPs in response to a change in light level (2 log units for 100-200 msec), imitating the natural visual stimulus of an adult arriving with food, appeared for the first time in the 2.5-day-old nestlings as a long latency positive-negative deflection. The probability of EP occurrence and its parameters in 2.5- to 3.5-day-old nestlings depended upon many additional factors. This juvenile EP was transformed into the definitive one through a succession of stages common to all nestlings studied. The actual duration of these stages, however, could vary in different young; so the exact ages of EP development presented below are somewhat schematized. 1. Age: 2.5 Days

EPs occurred in nestlings in the activated state, i.e., those with a high level of feeding motivation and showing movement in the nest such as preening etc. EP occurred in 70% of instances in response to the off-component of flashes 100250 msec long. Response latency (first positive peak latency) was 100+8.4 msec (Fig. 13). 2. Age: 2.5-3 Days EP in the form of a long-latency low-amplitude complex in response to the offcomponent of a flash occurred always, even in the nonactive nestlings. Active nestlings responded in the same way to the on-component of the signal. The probability of response to both components of the same signal was not higher than .25-.5 in active young. 3. Age: 3 Days EP in the form of a long-latency low-amplitude complex was invariably recorded in response to the on-component of the signal even in resting nestlings. Active nestlings responded to the off-component with high amplitude rapidly developing EP; the three main phases identified in the mature EP could be distinguished in it. The latency of this response was 8527.7 msec from the end

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FIG. 13. Development of wulst visual EP between 2.5 and 4 days of life. (A) Visual EP to flashes 250 msec long (flash duration, black bar below), (B) Visual EP to flashes 150 msec long ( A and B are different nestlings). In each panel: above, EP; below, EMG. Figures to the left: the succession of EP pattern maturation during ontogeny.

of a light flash. In all cases when both responses were recorded to the same flash, the off-response latency was 20-40% shorter than that of the on-response. 4 . Age: 3-3.5 Duys

EP in the form of a three-peak complex, with the parameters and appearance like those of the mature response, occurred in response to the on-component of the flash almost always. The probability of a second response to the same flash did not exceed .I-.25 at this age. Response form and parameters were practically independent of nestling activity level. Off- and on-responses in 30% of

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instances had equal latency; in other instances the amplitude of the former exceeded the amplitude of the latter, and the latency of the off-response was always shorter.

5 . Age: 3.5 Days EP consisting of three components was recorded in all cases. In nestlings with a high level of motivation the visually guided form of feeding behavior was exhibited for the first time. Begging occurred only sometimes and always in response to the off-component of the flash, its latency being somewhat longer than the latency of the evoked off-response. 6 . Age: 4 (4.5)-7 Days

EP in the form of a three-component complex, looking much like the fully developed potential, was recorded in all cases in response to the on-component of the flash and, in 10% of instances, in response to the off-component. Begging in nestlings with a high level of feeding motivation coincided with the highamplitude negative peak. Begging latency was 106k 17.7 msec. Thus the formation and final arrangement of visual EP in wulst was completed between days 2.5 and 4 of life. During the first 36 hr of postembryonic development the latency of response became 40 msec shorter and its amplitude (the highamplitude first negative peak was taken as an index) increased twofold (Fig. 14). The most significant shortening of latency took place in the interval between the first occurrence of EP and the onset of visually guided feeding behavior while the increase in amplitude continued even beyond this interval. The study revealed that wulst EP are recorded for the first time on day 2.5 of nestling life. Immediately after their appearance the responses d o not always occur and are unstable with varying paramaters. The unreliability of their occurrence has been mentioned as the most characteristic trait of responses to visual stimulation early in development (days 18-19 of incubation in chick embryos, Volokhov & Pisareva, 1969). The probability of the appearance of a response and its markedness clearly depend, according to our study, on the level of general activation including the level of feeding motivation. We have found that EP in the form of a low-amplitude short-latency complex is first observed in response to the off-component of the light flash. At the older age, when both responses to the same flash are recorded, offresponse latency is shorter and it matures earlier. Moreover, feeding behavior first occurs in relation to the off-component of the flash. All these facts suggest that general activational brain mechanisms play the most prominent role in the organization of responses early in life, in addition to the role of specific motivational mechanisms. It is well established that both systems may influence the activity of specific sensory structures in a phasic as well as a tonic way. In the study of visual E P formation in kittens it was discovered that the response, which

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FIG. 14. Age dynamics of latency (A) and amplitude (B) of three visual EP phases: PI (1: N , (2: 0- -O), and P2 (3: 0--0).Darkened area: time of appearance of visually guided feeding behavior.

0-o),

appeared first in the form of long-latency low-amplitude deflection, was mediated by “diffuse activating nonspecific visual mechanisms. ” The stable, shortlatency polyphasic response appearing later depended on the specific activity of the visual system (Rose & Lindsley, 1968). According to Ata-Muradova (1980), the nonspecific projections and general ascending systems maturing fastest are the primary afferent inputs to the higher integrative levels of the brain. The connection of avian reticular and hypothalamic structures to visual structures has been convincingly shown by morphological and electrophysiological studies (cf. Pearson, 1972). Thus, one of the most important effects of the early maturation of nonspecific and (motivational) specific activating mechanisms may be their decisive influence (demonstrated also in our study on the rate of sensory development) in mediating adaptation to ecological factors. The visual phenomenon described above may be understood in the context of the accelerated maturation of the visual system and its involvement in the organization of goal-directed feeding behavior which is also “ahead of schedule” in those nestlings that develop in a physically and socially enriched environment (Khayutin & Dmitrieva, 1981). This additional influence could have increased the level of nonspecific activation which, in turn, initiated the early onset of functioning of the specific visual

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mechanism. This is probably the basis for the phenomenon of accelerated and synchronous hatching in many bird orders under the influence of stimuli which are either specific to one sense (visual or acoustic) or more general, additional aspects of stimulation (Vince, 1966, 1974; Hess, 1973; Konishi, 1973; Adam, 1975; Tikhonov, 1977). These additional influences stimulate the systems of nonspecific activation which promote accelerated development of the relevant sensory mechanisms as well as a general increase in the rate of metabolic processes in the developing organism.

VI.

COMPLEXITY OF BEHAVIOR ORGANIZATION I N EARLY POSTEMBRYONIC DEVELOPMENT

This final section is aimed at defining the relationship between the complexity of nestling behavior during growth and development and the totality of the ecological factors that create the constant environment of a species throughout all of early postembryonic ontogeny. Attention will be paid, as before, mainly to the development of the sensory basis of the principal behavior forms during nestling life, i.e., feeding and defense behavior. The study was conducted on broods of the great tit (Purus mujor) and the redstart (Phoenicurus phoeriicurus). This section also includes findings obtained during a study of the behavior of cuckoos (Cuculus canorus) that parasitize redstart nests during the embryonic and nestling periods. The entire nestling life of these species is characterized by standard conditions and their living space is limited by the walls of a hollow or a nest-box. A.

SENSORY ORGANIZATION OF BEHAVIOR OF GREATTITNESTLINGS

From the moment of hatching and during most of the nestling period begging was induced in great tit nestlings by a “sonic complex of feeding.” However, the last stimulus of the complex, i.e, the food call, was observed only in 20-25% of feedings. Spectral characteristics of this sonic complex of feeding are presented in Table I and Fig. 15. The nestling behavioral repertoire was limited to feeding behavior until the sixth day. Thereafter acoustically guided behavior was modified, we believe due to the enrichment of the behavioral repertoire and primarily to the formation of a passive-defense reaction. The development of the defense integration was a rather long process, taking 1.5-2 days. The stereotyped alarm call of the species is presented in Fig. 15 and Table I. The eyes of great tit nestlings start to open on day 6 and are completely open by day 9-10. But the change in light level caused by the parent passing through the entrance hole of the nest-box became a relatively effective stimulus for begging only on the eighth day and lost its effectiveness by day 11-12. To

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Duration (see)

FIG. 15. Sonograms of the signals of adult birds eliciting nestling behavior (A) Pied flycatcher; ( B ) great tit; (C) redstart. ( 1 ) Nonconspecific signals: foot tapping on the wall and rustling of the nest material; (2) conspecific food call, (3) alarm call; (4)species song.

analyze the role of the diffuse luminosity change in the feeding behavior of nestlings, measurements of background light level and changes therein were undertaken in many nest-boxes inhabited by great tits. It was found that the background luminosity in great tit nests at the position of the eyes of resting young even on sunny days never exceeded 1.7 lux and in dark boxes was .3-.01 lux. When the hole was closed by a parent the luminosity decreased, the drop being 2-3 log units. However, this considerable luminosity change appeared to be of little importance to the organization of the nestlings’ feeding behavior. The arrival of a bird in an artificially lit nest-box, although causing no luminosity drop at all, induced quite normal begging with respect to duration and intensity.

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At the same time an experimental short-term luminosity change (2-3 log units) elicited begging only in nestlings with the highest level of feeding motivation. Thus the brief luminosity change resulting from the bird’s arrival played only a limited role, with little effect upon feeding behavior, and that during only a short period of nestling life. On the twelfth day nestlings started to turn their heads in the direction of the hole between feedings. On day 13-14 begging was elicited by the tap of feet, prolonged and enforced by the luminosity change, and directed by the moving silhouette of the adult. From then on till the end of a nestling life (day 18) feeding behavior was completely transformed into food acquisition elicited and directed by the bird’s silhouette. Any moving conelike object could be used to provoke normal begging in the experiments. From day 16 to 17 almost every arrival of the parents was accompanied by the species song (as the male constantly stayed nearby); the effect of this signal on feeding behavior was much more significant than that of any other. Even when reproduced very quietly it elicited vigorous begging in all nestlings, whatever their level of feeding motivation. The nestlings’ motor activity considerably exceeded that normal for that age during begging in response to the sound complex of an arriving adult. After some time the locomotion component of reaction to even very quiet song started to dominate over feeding behavior. The nestlings not only jumped high but flew to the hole. On day 17-18 this movement in response to a song completely suppressed the begging component of their reaction; jumping high, they even reached the hole sometimes. Nestlings usually fledged with the species song heard in the background. B.

SENSORYORGANIZATION OF BEHAVIOR REDSTARTNESTLINGS

IN

During the first 5 days begging was the dominant form of nestling activity. Under natural conditions during this period, it was elicited by the sonic complex of feeding. The food call was observed in 50-60% of feedings. Usually the nestling’s reaction began in response to the first or the second component of the complex. The food call only made it more active and involved one or two more of the nestlings with lower levels of feeding motivation. The parameters of redstart signals are presented in Fig. 15 and in Table I. When the modality and parameters of stimuli effective for begging were studied in the laboratory it was found that 1- to 5-day-old nestlings reacted only to acoustic stimuli. Besides the components of the sonic complex of feeding (reproduced by tape) begging could be induced in nestlings with the highest motivational level by a wide variety of sounds: whistles, speech, various mechanical sounds, etc. No other stimuli, e.g., tactile (including air flow), vibra-

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tional, or visual, caused begging in nestlings of that age. The same phenomenon was observed in the study of the sensory organization of feeding behavior in nestlings of two other tree hole nesters. The auditory sensitivity of redstart nestlings was investigated by presenting pure tone sounds of various intensities and a wide range of frequencies. Comparison of the auditory sensitivity range with the frequency spectrum of the sonic complex of feeding revealed two peaks of sensitivity: one, corresponding to the energy maxima of the first and second nonconspecific components of the complex (those that are mechanical in origin) and the other matching the high energy part of the conspecific food call (Fig. 16, Table I). On day 5-6 the nestlings’ eyes opened: consequently, there was an enrichment of eliciting stimulus modalities. From then until the eighth day diffuse luminosity change accompanied by mechanical components of the auditory complex were the main stimuli for feeding behavior in the wild. On the fifth day nestlings started to exhibit the passive-defense reaction in response to the alarm call. After the eighth day the organization of feeding behavior changed. The passive begging reaction was transformed into active food acquisition. Up to day 11 food acquisition behavior occurred in response to diffuse luminosity change together with the mechanical components of the “sonic complex of feeding,” but it was coordinated by the guiding stimulus of the moving bird silhouette.

6

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SPL (dB, above background level)

FIG. 16. Frequency thrcshold curves of auditory sensitivity of I - to 5-day-old nestlings of redstart (0-0) and cuckoo (0-0) reared by redstarts.

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After day 11 begging was elicited and directed only by the moving silhouette of a parent: this was clearly seen in the nest-boxes with a high level of background luminosity (10- 100 lux and more) that redstarts choose for breeding.

c.

ORGANIZATION OF CUCKOO NESTLING BEHAVIOR REDSTARTNEST

SENSORY

IN THE

Immediately after hatching, cuckoo nestlings exhibited two forms of behavior: begging and throwing nestlings and/or eggs out of the nest. The analysis of cuckoo nestling feeding behavior revealed that all the sounds accompanying the arrival of a bird with food were effective for begging. A comparison of the auditory sensitivity range of the cuckoo nestling with the spectrum of sonic complex of feeding of the foster parents (Figs. 15, 16, and Table I) revealed that a low-frequency sensitivity peak corresponded to the energy maxima of the first and second components of the complex while the second peak matched the highest energy part of the food call. Although the auditory sensitivity range and sensitivity peak of cuckoo nestlings corresponded to those of redstart young, in the range of low frequencies (i.e., the range of the mechanical nonconspecific components of the complex), cuckoo nestlings had auditory thresholds 1.5-2 times lower than redstarts. However, in the range of high frequencies which correspond to the redstart food call, cuckoos, by contrast had absolute thresholds several times higher than redstart nestlings of the same age [compare Fig. 15(3) and Fig. 161. Cuckoo young responded with begging to the same set of sounds that were effective for the redstarts. We also tried to discover other stimuli effective for the begging of cuckoos. Among all the influences we used, only vibration of the nest appeared to cause feeding reactions. This response did not differ from that of cuckoo nestlings to the sonic complex of feeding with respect to its intensity, duration, and prominence. On the sixth day the eyes of cuckoo young opened, whereupon short-term luminosity changes started to cause begging. The sounds accompanying the bird’s arrival, however, were still effective (and remained effective until the cuckoos fledged). At the same time redstart alarm calls started to cause the cessation of vocalization and freezing. The passive-defense reaction is of great importance for brood security (Khayutin & Dmitrieva, 1976b). The adaptive value of such behavior by cuckoo nestlings, which have very loud vocalizations, is quite obvious. On the eleventh day, the moving bird started to induce a food acquisition reaction in cuckoo nestlings. Until the end of nestling life (day 20) no changes in the behavior of the nestlings were observed. As before, the food acquisition response was elicited by the sounds accompanying the bird’s arrival at the nestbox as well as by the moving silhouette.

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DISCUSSION A N D CONCLUSIONS

A comparison of the factors of sensory organization of feeding and defense behavior of four species studied during their nestling life enabled us to define some common basic traits. First, at the beginning of nestling life, the young have only one behavior pattern, i.e., a begging behavior guided by acoustic signals. In all cases begging behavior is elicited by a complex of wide-band sounds of different origin joined in a simple mechanical succession. The experiments demonstrated that under normal conditions (with noise level in the environment about 50-60 dB) this behavior may be exhibited in response to any single component of the complex. The only factor determining selection of these signals is the level of feeding motivation of the young. In general one can conclude that for the nestlings with a high level of motivation the effectiveness of the first components of the complex is increased; for those with a low level of motivation, the increase is that of the last components. Moreover, the last component of the complex (i.e., the food call) usually occurred under natural conditions when the begging had already started in response to the first stimuli, it therefore being an additional stimulus largely as a backup, a “safety factor.” A high level of response probability is also a characteristic of the frequency spectrum of the complex: the fact that begging is elicited by pure tone signals with frequencies in only a small part of the spectrum of the complex testifies to the redundancy of the frequency spectra of all sonic components of the feeding complex. On the other hand, the fact that nestlings normally responded to the “nontypical” food call (Figs. 17 and 18) confirms that the frequency spectrum of conspecific signals, which elicit the behavior, may not coincide completely with the range of the nestling’s auditory sensitivity. The more general significance of this is the demonstration

Duration (sec)

FIG. 17. Sonagrams showing variation in the food call of the pied flycatcher (a-e); ( e ) the same as (d), but in 16 kHz band.

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FIG. 18. Sonograms showing variation in the food call of redstarts (a-f)

that the stimulus for this natural behavior only triggers it while the goal (i.e., getting the food) dominates the behavior organization. The coincidence of one or a few peaks in the sound spectrum and auditory sensitivity is probably enough to induce the normal goal-directed feeding behavior. This suggestion does not fit in with ideas now being developed in the literature that the range of frequencies perceived by nestlings immediately after hatching must exactly match all spectral characteristics of adult conspecific signals which elicit the behavior of the young (Milyagin, 1957; Konishi, 1970, 1973; Gottlieb, 1971; Saunders et af., 1974; Tikhonov, 1977; Golubeva, 1980). A more formal contradiction of the same idea is the observed sensitivity of the nestlings of all four species studied to the lowfrequency sounds which dominate the first two components of the “sonic complex of feeding”: being mechanically produced, these sounds are not strictly conspecific and are not represented in the spectrum of the feeding vocalization of the species. It is suggested that this range of auditory sensitivity ( . 2 - 1 kHz) is actively used by the studied species in full accordance with the ecological characteristics of their habitat, mediating feeding behavior in response to the set of sounds necessarily accompanying each arrival of a parent with food. It is possible that the increased sensitivity of nestlings of all four species studied in the range of the mechanical components of the sound complex is established due to learning in the last period of embryogenesis. Numerous studies of the ontogency of early forms of behavior in birds with different ecological settings have demonstrated the determining influence of late embryonic and early postembryonic sensory experience, especially acoustical, upon the organization of later acoustically guided behavior and consequently upon the preference for

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sounds with particular patterns and characteristics (Hess, 1973; Vince, 1973; Impekoven, 1976; Heaton & Miller, 1978). However, in spite of the coincidence of auditory sensitivity ranges and sensitivity peaks in redstart and cuckoo nestlings, the latter have low frequency auditory thresholds (i.e., corresponding to energy maxima of the mechanical components of the complex), 1.5-2 times lower than the foster parents’ own young. But in the high-frequency range, corresponding to the spectrum of redstart feeding vocalizations, cuckoos’ absolute thresholds are a few times higher than those of redstart nestlings of the same age (see Fig. 16). Thus, in spite of the fact that pre- and postembryonic development of the nestlings of both species takes place in the same acoustic environment, they have different characteristics of audition. This may be regarded as one argument against the general viewpoint accepted in the current literature, namely that the acoustic environment is the main embryogenetic determinant of auditory perception. It may be suggested at the same time that there is a general tendency in the development of vertebrates (and birds in particular) for the auditory system to be actively used in the biology of parasite species, through the accelerated (selective and heterochronous) development of an increased sensitivity in the range of low frequencies (Rubel, 1978). From such a viewpoint the greater sensitivity of cuckoo young, immediately after hatching, to the low frequencies that correspond to the spectra of mechanical components of the “sonic complex of feeding” of the foster parents (as well as of other hole nesters) may be considered as an important, albeit nonspecific, adaptive feature. While the feeding behavior of nestlings immediately after hatching is provoked by a simple mechanical succession of relatively wide-band sounds, the passive-defense response, which occurs for the first time in all four species at the end of the first half of nestling life at the same time as the enriching or change of modality of stimuli triggering feeding, is elicited by rhythmically organized signals. Recall that a single sound in a great tit alarm call resembles the conspecific food call very much, whereas the difference between the two kinds of signals in the pied flycatcher and redstart is very clear. Even when the single signals in the food and alarm calls are quite alike (as are those of a great tit) the presence or absence of a rhythmic organization is enough to cause an absolutely different behavioral response to those calls. An additional factor determining the differences in response to these signals is the totality of environmental factors creating the pretriggering integration (Anokhin, 1974). But the pretriggering integration may lead to goal-directed behavior even under the influence of a stimulus unlike the one that is anticipated. Figure 19 shows a great tit signal that in its organization cannot be taken for anything but a fragment of an alarm call. The bird, however, emitted it having already flown into the nest-box. This nontypical signal was reacted to by the 12-day-old young as if it were the food call because it was part of a complex consisting of this signal and the foot tapping preceding it. This is confirmed by the vocalizations (clearly seen in the same

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Duration (sec)

FIG. 19. Nontypical signal of a great tit. Vocalization by nestlings accompanying begging, underlined (see text).

sonogram) accompanying the begging. Under laboratory conditions the reproduction of this sound elicited begging in 10- to 13-day-old nestlings with a high level of feeding motivation when the whole fragment was presented with the preceding sounds, and the passive-defense response when reproduced alone. Cuckoo nestlings responded with freezing to alarm calls of all three species. The last kind of conspecific signal which also modifies the behavior of nestlings, species-specific song, starts to play a role at a later period of nestling life. Although the role of song in the organization of the behavior of nestlings of the three species studied is different in each case, this signal had several functions (as compared to the single functions of the other signals, the food call and the alarm call). The rhythmic and structural organization of this signal is even more intricate than that of the others; the frequency spectrum of the single sounds composing it is also much more narrow, especially in the great tit (Fig. 15). The general principles of the organization of the nestlings’ goal-directed behavior controlled by acoustic signals may be summarized as follows. During the first days of life the only form of behavior (begging) is manifested in response to a complex of mechanically joined wide-band sounds; the set and spectra of these sounds are redundant, so giving a high degree of certainty in eliciting the behavior response. The passive-defense reaction appearing at the end of the first stage of nestling life is controlled by rhythmically organized signals with a narrower frequency spectrum than that of food signals. And finally, behavior guided by the species song is activated only during late stages of nest life. Compared with the other signals, the growth of the rhythmic and structural complexity of this signal is accompanied here by a further narrowing of the frequency spectrum of the sonic units composing it. Thus the general line of growing complexity in the

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organization of acoustically guided behavior during the nestling’s development is paralleled by the increasing detail of the pattern of the controlling signals and by the narrowing of their frequency spectrum. Sonographic analysis of various signals used in the communication by adult birds of many passerine species does not contradict this conclusion (Marler, 1963; Bremond, 1963; Milligan & Olsen, 1969). Moreover, the calls of the nestlings, which can be regarded as providing information about the total level of feeding motivation of the whole brood addressed to the parents (Khayutin & Dniitrieva, 1981), also have a complicated rhythmic organization and energy maxima confined to a limited part of the frequency spectrum (Fig. 20). The analogous tendency to a growing complexity of the organization of visually guided behavior paralleled by the increasing complexity of a pattern of controlling signals also appears an obligatory factor in the early ontogeny of the four bird species studied. Some interspecies differences revealed during the analysis of visually guided behavior do not contradict this conclusion. Such differences concern the absolute dependence of feeding behavior, after the eyes open, on the luminosity level and its changes in the pied flycatcher nestling, the partial dependence in the redstart nestling, and the relative independence from the same factors during the same period for great tit young, but may be accounted for by the different degree of adaptation to the characteristics of nest ecology in these species. Measurements of background light level and its changes (caused by the activity of adult birds) taken in many nest-boxes occupied by pied flycatchers, together with the data of electrophysiological studies of visually guided behavior of their young, demonstrated that vision is characterized by a wide range of adaptiveness and is very sensitive even to the slightest luminosity change, down to only .4 log units. This range of adaptation (3-.4 log unit) of visual mechanism provides pied flycatcher nestlings with a secure adaptation of feeding behavior to the nest environment.

FIG. 20. Sonograms of the vocalizations of a cuckoo chick (a) and of a redstart brood (b). Age of nestlings, 4.5 days.

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In great tit young a high level of sensitivity of visual mechanisms to diffuse light was also discerned, but is not used in the organization of feeding behavior. The high level of safety of begging elicitation after eye opening and before the maturation of patterned vision is still based on the activity of auditory mechanisms. Feeding behavior of redstart nestlings after eye opening and before the maturation of structured receptive fields is based on parallel activity of visual and auditory mechanisms. The period of functioning of visual mechanisms sensitive to the diffuse light change in cuckoo nestlings is the shortest one observed in any of the species studied. Diffuse light change does not, in fact, play an important role in the organization of feeding behavior in cuckoo young (normally reared by redstarts, biological race, according to Promptov, 1941) as well as in great tit nestlings. During the terminal stages of nest life food acquisition behavior in the nestlings of all species studied is controlled only by the structured visual environment. The incorporation of the organized visual environment as a factor in the ontogeny of a goal-directed behavior is inevitably based on certain visual experiences (Jones & Horn, 1978; Brown & Horn, 1980) acquired during a fixed (for each species) developmental period. These periods may be shifted backwards or forwards in time under the influence of external factors: a specific sensory and socially enriched environment results in an earlier organization (acceleration), whereas sensory and social deprivation slows the organization (Khayutin & Dmitrieva, 198I ) . The transformation of simple visual fields into the complicated organized fields adequate to receive the information content of a specific environment (under the influence of early visual experience) has been demonstrated in many mammal species (Wiesel & Hubel, 1974; Grobestein, Chow, & Fox, 1975; Buisseret & Imbert, 1976). Probably birds (hole nesters, at least) are no exception to this general trend. Thus, the growing complexity of visually as well as acoustically guided behavior in the early postembryonic period is characteristic for the nestlings of the species studied. The increase in the level of organization of sensory mechanisms, and of the behavior patterns mediated by these mechanisms, is connected with the demands posed by the increasing complexity of organization of the specific environment.

Acknowledgments The author wishes to express his gratitude to Dr. Kira V . Shuleikina for her help in the organization of the studies and to Dr. Lubov P, Dmitrieva and L. 1. Alexandrov for their constant willing cooperation: Dr. L. 1 Alexandrov’s great help in the preparation and discussion of the English version is also gratefully acknowledged.

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References Adam, J.J.( 1975). The effect of embryonic stimulation on behavior development in the chick. Exp. Bruin Res. 23, Suppl. 4. Anokhin, P. K. (1964). Systemogenesis as a general regulator of brain development. Progr. Brain Rcs. 9, 54-76. Anokhin, P. K . (1974). In S. A. Corson (Ed.), Biology and neurc~pliysiologyqfthe conditioned refe.r and its role in adaptive behavior. New York: Pergamon. Ata-Muradova, F. A. (1980). The developing bruin: A svstemic analvsis. Moscow: “Medicine” (in Russian). Bagnoli, P., Francesconi, W., & Magni, F. (1982). Visual wulst-optic tectum relationships in birds: A comparison with the mammalian corticotectal system. Arch. Ital. B i d . 120, 21 2-225. Barn, A. V. ( 1978). Auditorv centers arid sound identification. Leningrad: Nauka (in Russian). Bengtsson, H., & Ryde, 0. (1981). Development of parent-young interaction in asynchronously hatched broods of altricial birds. Z . Tierpsychol. 56, 256-272. Best, L. B. (1977). Patterns of feeding field sparrow young. The Wilson Bull. 89, 4, 625-627. Bonke, D. (1978). Tonotopic and functional organization in the neostriatum (field L) of the guinea fowl (Numiriu meleagris). Verh. Dtsch. Z o o / . Ges. 193. Bremond, J . C. (1963). Acoustic behavior in birds. I n : R. G. Busnel (Ed.). Acoustic behavior of animals Amsterdam: Elsevier. Brown, M. W., & Horn, 0 . (1980). Plasticity in the developing chick brain: effects of visual experience on the responsiveness of hyperstriatal neurons. In Multidisciplinary approach to brain development. Dev. Ncwrosri. 9, 373-374. Buisseret. P.. & Imbert, M. (1976). Visual cortical cells: Their developmental properties in normal and dark reared kittens. J . Phvsiol. (London) 255, 5 I 1 -525. Coghill, G. E. (1929). Anatomy and the problem qfbehatior. London and New York: Cambridge Univ. Press. Curio, E. (1975). The functional organization of anti-predator behavior in the pied flycatcher: A study of avian visual perception. Anim. Behav. 23, 1-75. Dallos, P., Harris, D., Ozdamar, O., & Rayn, A. (1978). Behavioral compound action potential, and single unit threshold relationship in normal and abnormal ears. J . Acoust. Soc. Am. 64, 151167. Denton. C. J. (1981). Topography of the hyperstriatal visual projection area in the young domestic chicken. Exp. Neurol. 74, 482-498. Dooling, R . J . , & Walsh, Y. K. (1976). Auditory evoked response correlates of hearing in the parakeet (Melopsirtarus undulutus). Physiol. Psycho/. 4, 224-242. Gladkovitch, N. G. (1979). The formation of reticulo-spinal relations in ontogenesis. In K. V. Schuleikina & S. N. Khayutin (Eds.), Moscow: Nauka (in Russian). Nertronal mechunisms .f‘ developing brain (pp. 76-93). Golubeva, T. B. (1980). Development of audition in bird ontogenesis. In V. D. Ilyitchev (Ed.), Sensory systems and brain ofbirds (pp, 113-138). Moscow: Nauka (in Russian). Gottlieb, G . (1965). Prenatal auditory sensitivity in chickens and ducks. Science 147, 1596- 1598. Gottlieb, G. (1971). Development of species identification in birds. Chicago: Univ. of Chicago Press. Gottlieb, G. (1974). On the acoustic basis of species identification in wood ducklings (Aix sponsu). J . Comp. Physiol. Psvchol. 87, 1038-1048. Gottlieb, G. (1 979). Development of species identification in ducklings: V. Perceptual differentation of the embryo. J . Comp. Physiol. Psvchol. 93, 831-854. Grobstein, P., Chow, K. L., & Fox. P. C. (1975). Development of receptive field in rabbit visual

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cortex: Changes in time course due to delayed eye-opening. Proc. Natl. Acad. Sci. U.S.A. 72, 1543- 1545. Heaton, M. B., & Miller, D. G . (1978). Species-specific auditory discrimination in bobtail quail neonates. J . Dev. Psychobiol. 11, 13-21. Hess, E. N. (1973). Imprinting: Early experience and the developmental psychobiology of attachment. New York: Van Nostrand. Hinde, R. A. (l970), Animal behavior: A synthesis ojethology and comparative psychology. New York: McGraw-Hill. lmpecoven M. (1976). Prental parent-young interaction in birds and their longterm effects. Adv. Study Behav. 7, 201-253. John, E. R., & Morgades, P. P. (1969). Neuronal correlates of conditional response studied with multiple chronically implanted moving microelectrodes. Erp. Neurol. 23, 412-425. Jones, S . J., & Horn, I. (1978). Effects of visual experience on photically evoked potentials recorded in the chick forebrain. Brain Res. 159, 297-306. Karten, H. J . , Hodos, W., Nauta, W. H., & Revzin, A. M. (1975). Neural connections of the visual Wulst of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Spetulo cunucularia). J . Comp. Neurol. 150, 253-278. Kelley, D. B . , & Nottebohm, F. (1979). Projections of a telencephalic auditory nucleus-field Lin the canary. J . Comp. Neurol. 183, 455-469. Khayutin, S. N., & Dmitrieva, L. P. (1976a). Role of alimentary motivation in the organization of nest behavior of pied flycatcher nestlings. Zoologich. Zh. 55, 577-587 (in Russian). Khayutin, S . N . , & Dmitrieva, L. P. (1976b). On the interaction of alimentary and defence reaction in pied flycatcher nestlings. Zoologich Zh. 55, 1046-1052 (in Russian). Khayutin, S . N., & Dmitrieva, L. P. ( 1 9 7 6 ~ )Role . of natural sensory factors in the organization of alimentary behavior. Zh. vysshey nervn. deyat. 26, 932-939 (in Russian). Khayutin, S. N., & Dmitrieva, L. P. (1978). The development of conspecific acoustic sensitivity in hollow-nestling young. Zh. vysshey nervn. deyat. 28, 621-630 (in Russian). Khayutin, S. N., & Dmitrieva, L. P. (1981). Organization ojnatural behavior in nestlings. Moscow: Nauka (in Russian). Khayutin, S . N., Grinchenko, Y. V., & Dmitrieva, L. P. (1978). Role of species song in the organization of behavior of pied flycatcher nestlings. Zoologich. Zh. 57,413-419 (in Russian). Konishi, M. (1970). Comparative neurophysiological studies of hearing and vocalization in songbirds. Z. Vergl. Physiol. 66, 257-272. Konishi, M. (1973). Development of auditory neuronal responses in avian embryos. Proc. Natl. Acad. Sci. U.S.A. 70, 1795- 1798. Konstantinov, A. I., & Movchan, V. N. (197X). Adaptations of auditory system in wild rodents to the environment. Sensory Systems (pp. 34-56). Leningrad: Nauka. Kuo, L. Y. (1932). Ontogeny of embryonic behavior in Aves. I . The chronology and general nature of the behavior of the chick embryo. J . Exp. B i d . 61, 395-430. Kuo, L. Y. (1967). The dytiarnics oj'behavior development. New York: Random House. Leppelsack, H. J . , & Vogt. M. (1976). Responses of auditory neurons in the forebrain of a songbirds to stimulation with species-specific sounds. J . Comp. Physiol. 107, 263-277. Maksimova, E. V. (1979). Functional maturation of neocor1e.r it? prenatal ontogenesis. Moscow: Nauka (in Russian). Marler, P. (1963). Inheritance and learning in the development of animal vocalizations. In R . G . Busnel (Ed.) Acoustic behavior in animals. Amsterdam: Elsevier. McCondless, G . , & Best, L. (1964). Evoked response to auditory stimuli in man a summing computer. J . Speech. Hearing Res. 7, 193-207. Messmer, E., & Messmer, I. (1957). Die entwicklung der Lautausserungen und einiger Verhaltenweisen der Amsel (Turdus merula L.). Z. Tierpsychol. 13, 341-395.

ALTRlClAL BIRDS

151

Miccely, D., Gioanni, H.. Reperant, J . . & Peyrichoux. J . (1979). The avian visual Wulst. In A. M. Granda & J . H. Maxwell, (Eds.),Neural mechanisms ofbehuvior in the pigeon (pp, 233-254). New York: Plenum. Miller, D. B. (1980). Maternal vocal control of behavioral inhibition in mallard ducklings (Anus plutyrhynchos). J . Comp. Physiol. Psyclzul. 94, 606-623. Milligan, J . A., & Olsen, K . C. (1969). Communication in canary courtship calls. In R . A. Hinde, (Ed.). Bird voculization (pp. 165-186). London and New York: Cambridge Univ. Press. Milyagin, Y. A. (1957). The determining effect of ecologicalfactors on the embryogeny of unconditioned reactions. Doctoral dissertation, Moscow. Ookawa, T. (1979). Development of visual evoked potentials recorded from the telencephalon (the Wulst) of the chick embryo. J. Physiol. Soc. Jpn. 41, 325-334. Orbeli, L. A. (1967). Selected works: Problems of evolutionary physiology, (Vol. I ) . MoscowLeningrad: Acad. Sci. USSR. (in Russian). Pearson, R. (1972). The avian brain. New York: Academic Press. Pettigrew, J . D., & Konishi, M. (1976). Neurons selective for orientation and binocular disparity in the visual Wulst of barn owl (Tyro a h ) . Science 193, 675-678. Promptov, A. N . (1941). A modern situation in the studies of bird nest parasitism. Uspechi sovremennoy biol. 14, 30-32 (in Russian). Royama, T. ( 1966). Factors governing feeding rate, food requirement and brood size of nestling great tit (Purus major). Ibis 108, 313-347. Rose, G. H., & Lindsley, D. B. (1968). Development of visually evoked potentials in kittens: Specific and nonspecific responses. J . Neurophvsiol. 31, 607-634. Rosenblatt, J . S. (1970). Views on the onset and maintainance of maternal behavior in the rat. In L. R. Aronson (Ed.), Development and evolution of behavior (pp. 489-515). San Francisco: Frceman . Rubel, E. W. (1978). Ontogeny of structure and function in the vertebrate auditory system. In M. Jacobson (Ed.) Handbook ofsensory phjwiologv (Vol. 9, pp. 135- 198). Berlin and New York: Springer-Verlag . Saini, K . D., & Leppelsack, H. J . (1977). Neuronal arrangement in the auditory field L of the starling. Cell Tiss. Res. 176, 215-227. Saunders, J . C., Colles, R. B.. & Gates, G. K . (1973). The development of auditory evoked responses in the cochlea and cochlear nuclei of the chick. Brain Res. 63, 59-63. Saunders, J . C., Gates, G . K . , & Colles, R . B. (1974). Brain-stem evoked responses as an index of hearing threshold in one day old chick and ducklings. J. Comp. Physiol. Psycho/. 86, 426431. Schneirla, T. C. (1965). Aspects of stimulation and organization in approach: withdrawal processes. Adv. Study Behav. I , 1-74. Schneirla, T. C. (1966). Behavioral development and comparative psychology. Quart. Rev. B i d . 41, 283-302. Shuleikina, K . V. (1971). Systemic organization oj' u l i m e n r a ~behavior. Moscow: Nauka (in Russian). Shvirkov, V. B. ( 1978). Nt.urophy.siological study of systemic mecl7unism.s of behavior. Mobcow: Nauka (in Russian). Tikhonov, A. V. (1977). Acoustical signaling and behavior of precocial birds in ontogenesis. Thesis dissertation, Moscow, MSU. Tikhonov. A . V . , & Fokin, S. Y. (1981). Ecological determination of triggering stimuli of the alimentary functional systems in early bird ontogenesis. Zoologich. Zh. 60, 27 1-279, (in Russian). Tinbergen, N. (1953). The herring gull's world. London: Collins. Tinbergen, N. (1965). Animal Behavior. (Lifc Nature Library). Ncw York: Time Inc.

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Vince, M. A . (1966). Artificial acceleration of hatching in quail embryos. Animal Behuv. 16, 332335. Vince, M. A. (1973). Some environmental effects on the activity and development of the avian embryo. In G . Gottlieb (Ed.), Behavioral embriology (pp. 286-3 10.) New York: Academic Press. Vince, M. A , , (1974). Development of the avian embryo. Part I: Behaviour. In B. M. Freeman & M . study (pp. 3A. Vince (Ed.), Development ujthe avian embryo: A behavioral u~~dphysiological 116). London: Chapman & Hall. Volokhov, A. A. (1968). E.s,say.s on the physiology of central nervous system in early ontogenesis. Leningrad: Medicine (in Russian). Volokhov, A. A., & Pisareva, N. L. (1969). Evolution of midbrain tectum evoked responses to light stimuli in bird early ontogenesis. In V. V . Parin (Ed.), Systemic organization ojphysiological ,functions (pp. 127- 132). Moscow: Medicine (in Russian). Wiesel, T. N., & Hubel, D. H. (1974). Ordered arrangement of orientation columns in monkeys lacking visual experience. J . Comp. Neurol. 158, 307-325.

ADVANCES IN THE STUDY OF BEIIAVIOR. VOI.. 15

Food Storage by Birds and Mammals DAVIDF. SHERRY DEPARTMENT OF PSYCHOLOGY UNIVERSITY OF TORONTO TORONTO, ONTARIO, CANADA

1.

11.

111.

1V.

V.

VI.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Variation in Food Storing.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . , . . , B. General Patterns in Food Storing.. . . . . . . . . . . . . . . . . . . . . . . . . . , , , , Memory and the Recovery of Stored Food . . . . . . . . . . , . A . Field Studies.. . . . . . . . . . . . . , . . . . . . . . . . . . . . . . . . . . . , . , , . . , . . . . B. Laboratory Studies . . . . . . . . . . . . . . . . , . . . . . . . . . . . . . . . . , . C. Features of Memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . , , . , , . , Social Consequences of Caching . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . Early Breeding . . _ . _ . . . _ . . . . . . . . _ . . _ . . _ . . . _ . . _ . . . . . , , . . . . _ . . B. Irruption and Emigration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Social Organization. . . . . . . . , . .................... Economics and Decision Making . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , A . Spacing Scattered Caches. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . , , . , , B. Central Place Foraging.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . C. Inventory Decisions . . . . . . . . . . . . . . . . . . . . , . D. Timing of Recovery . . . . . . . . . . . . . . . _ . . _ . . _ Food Storing and Food Plants.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Nutcrackers and Pines. , . . . , . . , . . . . . . . . . . . . . . . . . . . . . . . . . . . , , , , B. Squirrels and Pincs.. . , , . , , . . . . . . . . . . . . . . . . . . . . . . . . . . , . C. Jays and O a k s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . ............................................

I.

i53 i54 158 160

160 162 164 168 168 169 170 171 171 173

174 175 176 177 180 181

181 183

INTRODUCTION

Food storing occurs in such a diverse group of animals and the advantages of storing food seem so obvious that it is surprising this behavior is not more common. Food storing occurs in 12 of 170 families of birds and in 19 of 120 families of mammals. These may, of course, be underestimates if caching occurs in some little-known species or has gone unnoticed in others. Animals that store food vary greatly in how they establish and exploit their supply of stored food, the uses to which they put stored food, and their reliance on the stored food I53

Copynght (0 1Y85 by Auadcmic Press. Inc. All rights OS rcprtrduclion in any S u m rcwrved. ISBN 0-12-oW515-X

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supply. This review discusses four aspects of these animals’ behavior: ( 1 ) how stored food is recovered; (2) the life history and social consequences of food storing; (3) the economics of food caching and the decision making it involves; and (4) the interrelations between food-storing animals and their food plants. The terms hourding, storing, and caching will be used as synonyms, and the material reviewed is restricted to birds and mammals. To the best of my knowledge, there are no well-documented cases of food storage by other vertebrates. Many invertebrates, of course, store food, and one well-studied instance is described in Heinrich (1979). Several topics not covered in this review, including the defense of caches from microorganisms and the sequence of use of different stored foods, are discussed in Smith and Reichman (1984). I would like to begin by briefly describing three animals that illustrate the variation that can occur in food storing. A.

VARIATION I N FOODSTORING

I . Acorn Woodpeckers (Melanerpesformicivorus) Acorn woodpeckers occur in the West and Southwest of the United States, and south through Mexico and Central America to northern Colombia. They are found in nonmigratory, communally breeding groups that usually number around five birds (Koenig, 1978; Stacey, 1979). The central feature of acorn woodpecker territories is one or more “granaries,” usually large oaks or pines, in which are drilled thousands of closely packed holes used for acorn storage. Concentrations of stored food such as acorn woodpecker granaries are often referred to as “larder” hoards. Granaries are the results of the efforts of generations of acorn woodpeckers occupying a particular territory. Individual group members may add only a few new holes per year. Although granaries are thus in short supply, they are a prerequisite for year-round occupancy and successful breeding in a territory (Koenig, 1978). Acorns are collected and stored as they mature in fall, and the supply of stored acorns is drawn on through the winter and spring. During the storage season, holes are cleaned of old shells and sometimes enlarged or modified. New holes are usually the work of several birds, working over a period of several days. In California an average acorn woodpecker stores about 300 acorns per year, or roughly 10% of its total metabolic requirement for the 8 months when acorns are only available from the granaries (Koenig, 1980). As MacRoberts (1970) has stressed, the diet of acorn woodpeckers is not exclusively acorns. They feed extensively on sap, flying insects, wild oats, buds, and fruit, and they may prefer these foods, when available, to stored dried acorns. Group members vigorously defend their granaries, not only from other acorn woodpeckers, but from ground squirrels, tree squirrels, nuthatches, crows, and

FOOD STORAGE BY BIRDS AND MAMMALS

155

jays. According to MacRoberts (1970), the birds sometimes fail to repel fox squirrels (Sciurus niger), and whole granaries may be lost.

2. South Island Robin (Petroicu uustrulis) The South Island robin is a muscicapid flycatcher found in New Zealand. It forages mostly on the ground, gleaning food from low-lying vegetation, logs, and soil litter (Powlesland, 1981). Earthworms are a major part of the diet, but slugs, insects, and spiders are also taken, along with berries in summer and fall. Most food storing occurs from April to July, the austral fall and winter, though some caching occurs throughout the year. Earthworms make up 70% of the food stored. Food items are stored singly in scattered sites in crevices, branch-trunk axils, and stump ends, usually a few meters off the ground (Powlesland, 1980). Such use of many dispersed storage sites is usually called scatter hoarding, a term coined by Morris (1962). South Island robins do not reuse storage sites. Most cached food is collected the same day it was stored, and although food may be cached at any time, retrieval tends to occur toward the end of the day. Although food-caching is not common during the breeding season, males have been observed collecting cached food and feeding it to the incubating female at the nest (Powlesland, 1980).

3. Eastern Chipmunk (Tumias striutus) The eastern chipmunk is a small sciurid rodent found in most forested areas of eastern North America. Its diet includes seeds, nuts, fungi, wildflower bulbs, and some invertebrate prey (Elliot, 1978). Food is stored in one of two ways: either in chambers in the extensive burrow system or in scattered caches, buried a few inches below the soil surface. Most provisioning of the burrow hoards occurs in fall when nuts and seeds, especially beech nuts and maple seeds, are gathered and carried into the burrow in the cheek pouches. Elliot (1978) estimated that burrow hoards of 15,000 to 20,000 beech nuts could be accumulated by one individual over the period these nuts are available. Burrows excavated in spring contained as many as 5,000 beech nuts from the previous fall. Inside the burrow, food is stored in galleries near the nest chamber and in small side chambers throughout the burrow system. There may be some segregation of different food types into different storage chambers. The animal’s scientific name, Tumias, is Greek for “housekeeper” and probably refers to burrow hoarding (Panuska, 1959). Three housekeeping problems beset burrow-hoarding chipmunks. Stored seeds and nuts germinate, and although the chipmunks can stop germination of beech nuts by nipping off the growing sprout, they do not attempt to prevent maple seeds from sprouting. Fungus and rot sometimes attack food cached in the burrows. Finally, insects, especially tenebrionid beetles, can be abundant in caches, though in those excavated by Elliot (1978) damage to the

TABLE I FAMILIES I N WHICH FOODSTORING OCCURS, W I T H A REPRESENTATIVE SPECIESFOR EACH FAMILY Species

Type"

Reference

Birds Accipitridae Lizard buzzard Kaupifulco monogrammicus Sagittariidae Secretary bird Sagittarius serpenturius Falconidae American kestrel Falco sparverius Tytonidae Barn owl Tyto alha Strigidae Boreal owl Aegolius funereus Picidae Acorn woodpecker Melunerpes ,formicivorus Laniidae Loggerhead shrike Lanius ludoviriunus Muscicapidae South Island robin Petroica austrulis Sittidae European nuthatch Sitta europaea Paridae Marsh tit Parus palustris Cracticidae Australian magpie Gymnorhina dorsalis Corvidae Clark's nutcracker Nucifraga columhiana

C

Brown and Amadon (1968)

C

Brown and Amadon ( I 968)

S

Mueller (1974)

L

Reese (1 972)

C

Bondrup-Nielsen ( 1977)

L

MacRoberts and MacRoberts (1976)

S

Applegate ( 1 977)

S

Powlesland

S

Dorka (1980)

S

Cowie et a / . (1981)

S

Robinson ( I 956)

S

Tomback ( 1977)

( 1980)

Mammals Talpidae European mole Talpa europaea Soricidae Short-tailed shrew Blurina brevicuuda Cebidae Squirrel monkey Saimiri sciureus

L

Ewer (1968)

L

lngram (1942)

C

Marriott and Salzen (1979)

I56

TABLE I (Continued) Species Ochotonidae Pika Ochotonu princrps Aplodontidae Mountain beaver Aplodontia rufa Sciuridae Pine squirrel Tumiasciurus douglasii Geom yidae Pocket gopher Geomvs bursarius Heteromyidae Pocket mouse Prrognathus interttiedius Castoridae Beaver Castor ,fibrr Cricetidae White-footed mouse Peromvscus leucopus Rhizomyidae Mole-rat Tachyorvctrs splendens Muridae Norway rat R a m s norvegicus Hystrichidae Brush-tailed porcupine Atherurus africanus Dasyproctidae Agouti Dasyproc f a punrtata Canidae Red fox Vulpes vulpes Ursidae Brown bear Ursus arctos Mustelidae Mink Mustela vison Hyaenidae Striped hyena Hvarna hyarna Felidac Leopard Panthera pardus

Type"

Reference

L

Kawamichi ( 1976)

L

Ewer (1968)

L

Smith (1970)

L

Nowak and Paradiso (1983)

L

Reichman and Fay (1983)

L

Ewer (1968)

L

Abbott and Quink (1970)

L

Jarvis and Sale (1971)

L

Steiniger (1950)

L

Ewer (1968)

S

Murie (1977)

S

Macdonald (1976)

C

Elgmork ( 1982)

C

Erlinge (1969)

C

Kruuk (1972)

C

Schaller ( 1972)

('Hoarding by animals ranges from scattering many caches (S), to maintaining a larder (L). to moving and concealing one or a few prey items (C). I57

158

DAVID F. SHERRY

seeds and nuts was not extensive despite the presence of tenebrionids. It has been noted that some fungi growing in burrows of desert heteromyid rodents may be toxic to insects and that rodents may promote the growth of these fungi to reduce insect predation on caches (0.J. Reichman, personal communication). Caching and torpidity may be alternative winter survival strategies for chipmunks. Individuals that gain body mass and enter torpor in winter usually have small burrow hoards, whereas individuals with large hoards do not gain body mass and may remain active (Wrazen & Wrazen, 1982). In contrast to burrow hoarding, scatter hoarding occurs predominantly in summer and early fall in adults (Elliot, 1978; Yahner, 1975) and in spring in juveniles without permanent burrows. Scattered caches usually consist of one cheek pouch load of seeds, nuts, or wildflower bulbs and are recovered within several days. Most scattered caches are eventually transported to the burrow. Yahner (1975) suggested that scatter hoarding was a “vestigial fixed action pattern” in chipmunks, but Shaffer (1980) has proposed an important function for scatter hoarding. Concentrated food stores, like the burrow hoards, are susceptible to pilfering by neighbors. Elliot (1978) and Shaffer (1980) have observed pilfering of burrows by neighbors during the resident’s absence. After such a robbery, Shaffer (1980) observed a chipmunk visiting scattered hoards and restocking the burrow with the food recovered. Scatter hoards, though small and dispersed, may be maintained because they are less likely to be lost to other chipmunks. B.

GENERALPATTERNSI N FOODSTORING

Valid generalizations about food storing are difficult to come by. Food storing is restricted to certain families of birds and mammals, as shown in Table I, but is widespread in most of the families in which it occurs. Explanations for its occurrence have been sought in diet, seasonality of the food supply, social structure, and other factors (Andersson & Krebs, 1978; Macdonald, 1976; Roberts, 1979; Turcek & Kelso, 1968; Vander Wall & Balda, 1981). Macdonald (l976), for example, observed that among the carnivores the omnivorous bateared fox (Orocyon megalotis) does not cache, perhaps because its major foods (insects and fruit) were too small and perishable, whereas many of the more strictly carnivorous carnivores do cache. But among birds this generalization does not hold. Nearly all of the omnivorous parids, corvids, and woodpeckers cache food. Andersson and Krebs (1978) suggested that a high degree of sociality may militate against food storing because of the possible presence of “cheaters,” that is, conspecifics that take stored food but store none themselves. But such highly social animals as acorn woodpeckers and African wild dogs (Lycaon picrus) both store food (MacRoberts & MacRoberts, 1976; Malcolm, 1980).

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There are clearly certain minimum conditions that must be met before food storing can evolve. The animal must, for example, be able to transport food. Not so trivial, however, is the observation that certain feeding methods lend themselves to leaving food secured in place until it can be revisited. Nuthatches, tits, crows, and jays often carry food to a spot where it can be securely held in place (e.g., against a branch) and broken up with the bill. Acorn woodpeckers remove acorns to “anvils” to break them into fragments, shrikes impale prey on thorns to assist in handling it, and many raptors remove food to a spot convenient for handling. Food left in place, wedged into bark or crevices, may have been the origin of caching in these families (Richards, 1958) and perhaps explains the restriction of the innovation to these groups. Additional minimum conditions are that the animal must be likely to return eventually to the cache site, even if, like Clark’s nutcracker (Nuc$raga columbiuna), altitudinal migrations take it away from the area where storing occurs (Tomback, 1978). And, of course, stored food must be sufficiently nonperishable and safe from pilfering to be potentially recoverable. But many animals could satisfy these requirements. What seems a more critical requirement is that the fitness gain attributable to a particular item of food is increased by storing it. This can arise for a number of reasons. Food may be less available at some future time so that access to stored food brings about a greater gain in fitness than would eating the food item immediately or relinquishing it. Roberts (1979) has proposed seasonal food scarcity as an important ecological factor leading to food storing. Alternatively, food requirements may be likely to increase, for example, as a result of a breeding attempt. Young pifion jays (Gymnorhinus cyanocephulus) in the nest are fed stored food (Bateman & Balda, 1973), and northwestern crows (Corvus caurinus) feed incubating females with stored food (James & Verbeeck, 1984). A fitness gain from storing may also occur when food is periodically, but temporarily, abundant. Storing food when the cost of obtaining it is low may lead to an overall reduction in the cost of obtaining food, without requiring any systematic change in either food availability or energy requirements. Finally, there may be benefits to decoupling the need for food from the need to forage for it, permitting an allocation of time to foraging and other activities that is not constrained by the moment-to-moment need for food. In this way, foraging need only occur when it is most profitable or when predation risk is at a minimum. Daan (1981) has suggested that caching by European kestrels (Fcilco tirznunculus) permits both optimal foraging and “optimal meal timing.” To summarize, food storing would be expected to occur when storing raises the mean expected contribution to fitness of a particular food item. Storing will increase this contribution to fitness if food is likely to become less abundant, if food requirements are likely to increase, if the immediate cost of collecting food is low. or if a constraint on the allocation of time is eliminated. This increase

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must exceed the contribution to fitness of eating the item immediately and must both exceed the cost of storing and allow for devaluation through spoilage or loss of the food item to other animals. 11.

MEMORYAND

THE

RECOVERY OF STOREDFOOD

Relocating food stored in a burrow or an acorn woodpecker granary presents no particular problem, though defending this concentration of food may. Widely scattered concealed caches are probably less vulnerable to total loss to other animals, as discussed further in Section IV, but relocating scattered caches presents special problems. Though some previous workers believed birds such as marsh tits could remember the locations of caches (Lohrl, 19501, others found it “inconceivable that tits can long remember where they have hidden even a small fraction of their stored food” (Gibb, 1960, p. 178). Gibb (1960) felt the birds might remember some caches for a short time, but he also presented an alternative-that the birds chose sites for storage that they were likely to reencounter again in the course of normal foraging. This idea was widely accepted (Haftorn, 1974; Kallander, 1978, Macdonald, 1976). But recent work with several species has produced convincing evidence that large numbers of cache sites are remembered for days and possibly months.

A . FIELDSTUDIES 1. Mursh Tits

Marsh tits will store several hundred food items per day, each in a separate site inside their winter territory. Storage sites were located in the field by Cowie, Krebs, and Sherry (1981) by offering marsh tits sunflower seeds labeled with radioactive technetium (99111T~). Technetium is a gamma emitter with a half-life of 6 hr, thereby allowing a short period of time during which seeds could be located with a portable scintillation counter. Seeds were stored in sites such as moss, hollow stems, tree bark, or dry leaves. Individual sites appeared never to be reused, probably because repeated use of sites would attract other animals and because suitable storage sites are abundant in most woodland areas. To determine whether seeds were recovered by the bird that stored them, two control seeds were placed in similar sites near each stored seed, at distances of 10 cm (the “near” control) and 1 m (the “far” control) from the stored seed. When these sites were inspected, at intervals of 3 hr during the 3 days following storing, it was found that seeds stored by marsh tits remained in place a mean of 7.7 daylight hr, near controls for 13.5 daylight hr, and far controls 20.4 hr. Daylight hours were measured because marsh tits are not active at night. This result shows that stored seeds are taken in preference to control seeds, though

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how they came to be taken was not observed directly. When it could be determined whether the stored seed or the near control seed had disappeared first, 93 times out of 121 it was the stored seed. If marsh tits reencounter their stored food by chance, all seeds ought to have disappeared at the same rate, and the same is true if other birds or rodents took seeds. The fact that stored seeds disappeared first is evidence, albeit indirect, that the seeds were removed by the animal that stored them. If this is so, the birds also returned quite accurately to the spot where seeds were placed, usually overlooking a control seed stored in an identical site 10 cm away. A mean survivorship of 20.4 daylight hr for far control seeds corresponds quite closely to the survivorship of artificially stored seeds placed between 1 and 2 ni apart and subject to normal predation by other birds and rodents (Sherry, Avery, & Stevens, 1982). A more refined technique for determining whether marsh tits recover their own stored food has been used by Stevens (1984). Marsh tits were fitted with leg bands to which a small cobalt-samarium magnet was attached. A Hall plate, which detects changes in the local magnetic field, was placed near the seed at each site. When the bird arrived at a storage site its magnet triggered the Hall plate, which stopped a small battery-powered clock, giving the exact time the bird attempted to recover its cache. Only one bird at a time was equipped with a magnet and given seed to store, so that triggerings showed that the bird which had cached a food item had returned to the site. Regular inspections of the sites also showed whether the bird was able to successfully recover the food item or whether it was taken by another animal before it could be recovered. Surprisingly, although all food disappeared within the 3-day duration of each replication, birds only attempted to recover about 30% of the food they had stored. Most of these attempted recoveries occurred within the first 2 days following storing. Stevens’ data and other experiments (Sherry et al., 1982) have shown that the rate of loss of stored food is very high, and this may be why no attempt is made to recover items after the first few days.

2. Nutcrackers Nutcrackers bury seeds in scattered caches made by digging in the ground with the bill. Each cache usually contains a number of seeds. When nutcrackers probe into the soil and attempt to recover stored seeds, they leave a record, in the form of discarded shells, showing which of their probes were successful. The expected spatial pattern of successful and unsuccessful probes generated on the assumpton that probes were random, or alternatively, were directed at remembered sites, were compared by Tomback (1980) to the pattern observed in the field. On the basis of the nearest-neighbor distances between successful and unsuccessful probes and the success rates, it was concluded that caches were not relocated by a random trial and error process. Tomback’s data also showed that during summer, after rodents had pilfered large numbers of caches, success rate declined. That

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nutcrackers continued to search for caches, although their probes were less successful, indicates that they were not detecting stored food under the soil directly by olfaction, as the rodents probably were (Howard, Marsh, & Cole, 1968; Murie, 1977).

3. Northwestern Crows Northwestern crows can successfully relocate clams they have stored in grass or beside rocks above the high-tide line (James & Verbeek, 1983). The evidence that birds recovering clams were the same ones that stored them is indirect since individuals were not marked, but James & Verbeek (1983) did observe that crows moved directly to storage sites and removed clams with success rates around 70%. Crows could not readily find clams hidden experimentally in similar sites and were no better at finding strong-smelling clams than they were at finding odorless, artifical clams.

4 . Red Foxes Red foxes establish scattered caches in their home range and recover food within a few days of storing. Macdonald (1976) found that foxes easily relocated their own caches but were much less successful at finding experimental caches placed nearby and caches created by other foxes. Thus, the scent of buried prey or any evidence of fox activity in the vicinity, such as scent marking, cannot be the major cues used to relocate caches. Foxes also returned to their own caches in Macdonald’s study after he had removed the prey, but they did not return to caches they had themselves emptied. It seems likely that foxes use some form of memory to relocate their caches but avoid revisiting emptied caches by urinemarking them (Henry, 1977), as do wolves (Harrington, 1981).

B . LABORATORY STUDIES 1. Marsh Tits and Black-Capped Chickadees

Although the field studies described in Section 11, A show that some animals can relocate their scattered caches quite effectively, none shows unequivocally whether memory or some other method is used to do so. Marsh tits and closely related black-capped chickadees will both store food in captivity, and a number of studies have investigated their ability to remember the spatial location of caches (Sherry, Krebs, & Cowie, 1981; Sherry, 1982, 1984b; Shettleworth & Krebs, 1982). Some of these results are described in Shettleworth (1983). A number of different methods and procedures have been used, and all results point to the same conclusion, that memory is the principal method used to recover stored food. Sherry, et al. (1981) studied marsh tits’ ability to relocate sunflower seeds stored in beds of moss. Seeds were removed by the experimenter between

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storage and attempts by the bird to recover them, to prevent direct detection of stored food by vision, olfaction, or some other means. The birds were able to accurately relocate storage sites, returned often to storage sites, and spent more time searching at these sites than at nonstorage sites. This tendency to return to storage sites greatly exceeded any initial preferences or biases to visit these places when food had not been stored. Relocation of cache sites thus did not come about by chance reencounter in the course of normal foraging. Shettleworth and Krebs (1982) performed a similar experiment in which marsh tits stored hemp seeds in small holes in tree branches. They counted the number of holes examined during recovery which actually contained previously stored food. Though performance was short of perfect recovery, that is, examining only holes containing a hemp seed, it was well above chance expectation. Sherry et al. (198 1 ) used the properties of interocular transfer in birds to assess the importance of memory in successful cache recovery. In pigeons, information that enters the visual system monocularly may fail to influence behavior controlled by the other eye (Goodale & Graves, 1980). Pigeons that have learned to perform a jumping stand discrimination with one of their eyes covered show no evidence of this learning when the trained eye is covered and they view the stimuli with the “naive” eye. The phenomenon is thus a failure of interocular transfer. The task must be relearned with the naive eye, and it is even possible to train conflicting discriminations to the two eyes simultaneously. Not all visual information fails to transfer, however. Stimuli falling on areas of the retina serving monocular vision, the largest part of the retina in birds like pigeons and marsh tits with panoramic vision, fail to transfer, whereas stimuli falling on the binocular regions do transfer (Goodale & Graves, 1982). In birds the optic fibers cross completely at the chiasm, and only input from the binocular visual fields projects to both hemispheres. Input from the monocular regions of the visual field projects to one hemisphere only (Goodale & Graves, 1982). Task difficulty and other features of the stimuli may also affect the amount of interocular transfer (Green, Brecha, & Gazzaniga, 1978). Marsh tits were trained to store seeds with one eye covered, then allowed to search for storage sites using either the eye that was open during storage or the naive eye. Birds using the eye open during storage performed as well as birds using both eyes, spending over 80% of their time at cache sites, while birds using the naive eye spent 40 to 50% of their time at cache sites, an outcome not significantly different from the chance level. Gibb (1960) noted that tits storing food give the site and its surroundings a rapid visual examination before flying off and that this reliably indicated a food item had been stored. Marsh tits fixate the storage site first with one eye, then with the other, and repeat this alternating fixation rapidly several times. Visual information acquired during this rapid examination must be essential in relocating the cache because, when it is unavailable to birds searching with the “naive” eye, stored food is not relocated.

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2. Nutcrackers The importance of visual landmarks in the recovery of stored food by Clark’s nutcracker has been examined by Vander Wall (1982). Nutcrackers cached seed in the sand-covered floor of an aviary on which was placed an array of prominent objects such as rocks and logs. Between storage of seeds and their recovery by the nutcrackers, the objects in one-half of the aviary were displaced by 20 cm, all in the same direction. Objects in the other half of the aviary remained in place. When nutcrackers attempted to recover their stored food, their probes were accurate with respect to the landmarks. On the undisturbed side of the aviary, these probes successfully turned up cached seed, while on the side where landmarks had been moved, probes missed the caches by about 20 cm. In the boundary area between halves of the aviary, where birds might be expected to have originally used as landmarks some objects which were later moved and others which were not, birds missed their caches by intermediate distances from 1 to 20 cm. If food-storing animals chose from among all available storage sites only those that share some particular distinctive feature, then successful cache recovery might not require remembering each of a large number of storage sites but only the feature that identifies them. Kamil and Balda (1985) tested this idea in an aviary that contained 90 sand-filled cups for storage sites, each of which could be covered with a plug to prevent access. During storage, only eight sites selected at random by the experimenter were unplugged and usable as storage sites. If a nutcracker must choose sites that have some feature in common in order to remember them, then it should have difficulty when it is restricted to storage sites selected at random by the experimenter. During recovery, however, when all 90 sites were unplugged, the nutcrackers performed as well as they had when their choice of sites during storage had been unrestricted.

C. FEATURES OF MEMORY Laboratory studies of captive birds have gone beyond supporting the assertion that memory is important in the recovery of stored food. Several properties of the birds’ spatial memories have been examined. The behavior of food-caching birds is compared with the results of laboratory studies of memory in other animals in Sherry ( 1984a). 1 . Avoiding Empty Caches Remembering where food was stored confers little advantage if caches that have been recovered or discovered to be lost to other animals cannot be distinguished, in memory, from caches that are intact. Both marsh tits and blackcapped chickadees can make this distinction (Sherry, 1982, 1984b). Birds were allowed to store seeds one day, then allowed to recover half of their stored food

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the following day. All remaining seeds were removed by the experimenter to eliminate direct cues to the presence or absence of seeds, and the birds were allowed to search for stored food on the third day. More time was spent at sites where food had not been previously removed by the bird, by both marsh tits and chickadees. In contrast, Balda (1980), working with a captive Eurasian nutcracker, found that emptied caches were not avoided. Kamil and Balda (1985) also found high rates of revisiting previously emptied caches in Clark’s nutcracker, but in their procedure all caches were reduced in size by the experimenter to two seeds between storage and recovery, and this may have produced high rates of revisiting as nutcrackers searched for the missing seeds. Other results with Clark’s nutcracker indicate that the ability to avoid emptied caches may develop with experience (Tomback, Bunch, & Sullivan, unpublished). The frequency of revisiting previously emptied caches declined from around 50% to near zero over the course of several trials and remained at this low level. Ralda (1980) suggested that nutcrackers in his study may have performed poorly at avoiding previously recovered caches because in the wild they are rarely faced with this problem. Discarded shells mark previously emptied caches, the birds range widely and may rarely reencounter previously emptied caches, and in some circumstances it may pay to reexamine previously emptied caches because nutcracker caches usually contain a number of seeds and some may remain even after the first recovery attempt. The data of Tomback et al., however, show that although Clark’s nutcracker may, like Balda’s Eurasian nutcracker, initially perform poorly, the ability to avoid previously emptied caches develops rapidly. It may be that the birds can retain information about the status of caches, but the rules for use of this information are flexible and permit behavior appropriate to prevailing circumstances. Food-storing birds lose a good deal of their cached food to other animals. Rodents and other birds remove food stored by marsh tits (Sherry, et al., 1982; Stevens, 1984), and loss of nutcracker caches to rodents may be particularly severe in early summer (Tomback, 1980). Black-capped chickadees have been found to be able to avoid revisiting storage sites they have discovered empty, and they perform as well at this task as they do at avoiding caches they have emptied themselves (Sherry, 1984b). 2. Retention Intervals Marsh tits and chickadees in the wild recover stored food a few days following storage, whereas nutcrackers recover their stored pine seeds several months after caching them. Do the accurate spatial memories shown to persist for short periods of time in the lab also last over longer intervals? For chickadees and tits they clearly do. A number of experiments have been conducted over 3-day periods, and accuracy of relocation does not decrease during this period. Recov-

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ery after 3, 24, and 72 hr does not differ (Sherry et al., 1981; Sherry, 1982, 1984b). Unpublished data show accurate memory 7 days following storage, though there appears to be some decrease by 14 days. These latter data are not sufficiently complete, however, to distinguish decay of memory from motivational changes over the 14-day period. For nutcrackers, Balda (1980) has shown accurate recovery of stored food up to 18 days following storage.

3. Serial Position Effects

A classic problem in the study of memory is the serial position effect, that is variation in the probability of accurate recall of items that depends on the order in which items were originally learned (Murdock, 1976). Serial position effects have been taken as evidence for the existence of separate short- and long-term memory processes, a view that originated with Broadbent (1958), though it may be currently in decline among memory theorists (Crowder, 1982). The sequence in which cache sites are created provides a natural series in which to look for serial position effects, and a number of studies have attempted this. In the field, Cowie et al. (1981) found a significant tendency for the seeds stored first to be recovered first. In the lab, Shettleworth and Krebs (1982) found that when seeds had been stored in two batches, separated by an interval of 2 hr, more of the seeds recovered in a test 2 hr later came from the second batch than from the first. A variety of other studies, however, have found no evidence of serial position effects, either in the sequence of recovery (Balda, 1980; Sherry et al., 1982; Sherry, 1982, 1984b) or in the amount of time or number of visits spent searching a particular site (Sherry, 1984b). Serial position effects could, of course, arise in the recovery sequence for reasons that have little to do with superior recall for some sites compared to others. It can easily be shown that if the probability of stored items being lost is constant over time, the expected number of seeds recovered is maximized by recovering in the reverse order of storage (D. W. Stephens, personal communication). This is because the items stored most recently are most likely to be still available, whereas the items stored longest ago are more likely to have been lost. The likelihood of loss of all items increases as time passes during recovery, so recovery in reverse order of storage results in more items being successfully recovered. Although this simple model does not appear to be a good description of what occurs in the wild, it makes the point that particular recovery patterns might be expected to occur for reasons unrelated to variation in recall for particular sites. From the mixed results concerning serial order effects, it can be concluded that a mnemonic based on storage order is not necessary for successful relocation of caches. Rank order correlations between storage and recovery sequences are rarely significant and have positive and negative signs with almost equal frequency (Sherry, 1982, 1984b).

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4 . Contents of Caches Chickadees and marsh tits store a variety of food types, including seeds, nuts, and invertebrate prey. In winter, black-capped chickadees’ preference for seeds of different sizes is affected by air temperature (Myton & Ficken, 1967), and there may be nutritional or energetic reasons for preferring different foods at different times. Evidence from one experiment indicates that black-capped chickadees can remember what kind of food is stored at a cache site (Sherry, 1984b). Black-capped chickadees in captivity prefer sunflower (Helianthus) seeds without shells to safflower (Catharmus) seeds with shells. They will store both, however, if given small numbers of each, sometimes storing the preferred sunflower seeds first. While searching for caches 24 hr later (all stored seeds having been removed to eliminate direct olfactory or visual detection), birds spent significantly more time at sunflower storage sites and visited these sites significantly more often than expected by chance. This was not true for safflower sites: birds did not visit safflower sites above the chance level. This effect was not due to the use of different types of sites for the two types of seeds; nor did visits to safflower sites, when they occurred, tend to occur at any particular time during the search trial. Whillans-Browning (unpublished), in a study in which several hundred chickadee storage sites were located in the wild, found no tendency to use different storage sites for sunflower seeds, safflower seeds, or Tenebrio larvae. Chipmunks and desert rodents sometimes segregate seeds stored in the burrow (Elliott, 1978; Shaw, 1934). Though memory for cache sites is not likely to be a problem for these animals, their behavior does indicate that as with scatterstoring birds, there may be functionally important reasons for being able to retrieve some types of food and not others at a particular time. Reichman and Fay ( 1983) have shown that food-storing rodents consume their caches in a way that maintains the diversity of their diet during periods when the hoard is the only source of food, and segregating types of stored food, either spatially or in memory, may assist in this.

5 . Neural Mechanisms In mammals, the hippocampus plays an important role in the performance of spatial memory tasks (O’Keefe & Nadel, 1978), though this may be due to its role in working memory rather than the spatial aspects of these tasks (Olton, 1982). In nutcrackers, Krushinskaya (1966) found that hippocampal lesions disrupted cache recovery but not caching or feeding. Lesioned birds continued to probe for food they had stored but could not accurately relocate their caches, whereas control birds with lesions in the neostriatum caudatum or in the hyperstriatum accessorium recovered their caches at the high level of accuracy found in intact birds.

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This early work on neural mechanisms of cache recovery has not been pursued. It could be fruitful to do so. Comparisons of the neural basis of the task would be possible between members of different food-caching families of birds, as would comparisons of the neural basis of spatial memory performance in caching and noncaching members of the same family.

111.

SOCIALCONSEQUENCES OF CACHING

A. EARLYBREEDING In many species of birds, breeding early in spring leads to greater production of young than breeding later (Perrins, 1970). Young raised early in the season have a greater likelihood of surviving the winter, probably because they have more time to gain weight and acquire foraging skills (Gochfeld & Burger, 1984). There are two constraints, however, on how early breeding may occur: the female must accumulate reserves of energy and nutrients for gonadal growth, egg laying, and incubation, and there must be food available to feed the young at the time they hatch. Food caching has enabled some species to surmount both of these hurdles and breed earlier than any other seasonally breeding North American passerines. In Ontario, gray jays (Perisoreus canadensis) have eggs in the nest by early March, earlier than any other corvid, or indeed earlier than any other passerine (James, McLaren, & Barlow, 1976). Clark’s nutcracker is another very early breeder, beginning nesting in late winter and early spring (Vander Wall & Balda, 1981). The young are fledged by late spring and move with the adults to subalpine elevations (Tomback, 1978). In the spring following a large pition pine crop, pifion jays also breed as early as February (Balda & Bateman, 1971; Ligon, 1978). In both nutcrackers and pition jays, females consume stored food late in winter, and though its contribution to energy and nutrient reserves has never been assessed directly, it seems likely that it helps these animals reach breeding condition. Whether it acts by providing additional food at the time reserves are being established or by ensuring reserves are not fully depleted over the course of the winter or by some other means is not clear. In Eurasian nutcrackers clutch size increases with the size of the hazel nut crop, and hazel nut stores, from the previous autumn (Swanberg, 1981). In pition jays much of the food given to the female during courtship feeding comes from stored supplies (Balda & Bateman, 1971, 1972). It is likely that young nutcrackers and pition jays are fed stored food after hatching. Clark’s nutcrackers in the nest are fed ponderosa pine nuts, though there is not clear evidence that they come from caches (Mewaldt, 1956). Vander Wall and Hutchins (1983) observed young fledged nutcrackers being fed white-

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bark pine seeds recovered from caches by adults. Pifion seed, which probably comes from the previous year’s caches, is fed to nestling pifion jays (Bateman & Balda, 1973; Balda & Bateman, 1971). Although the nestling pifion jay’s diet is over 80% animal matter, and most of this is insects, pifion seed occurred in 39% of the samples taken from collared nestlings by Bateman and Balda (1973). Nestling tits of some species are also fed stored food (Haftorn, 1973; Higuchi, 1977). For one Japanese population of the varied tit (Parus varius), kernels of beech (Castunopsis) nuts stored in autumn and winter are an important component of the nestling diet (Higuchi, 1977). Use of stored food by parent gray jays to feed nestlings has been demonstrated by Strickland in an ingenious experiment (Strickland, unpublished). Birds were provided with bread that had been colored with the food dye “Brilliant Blue.” Feeding with colored bread stopped at the onset of incubation. Parents were first observed removing colored fecal sacs during a period of bad weather when the young were 18 days of age. Dissection of one nestling revealed that its stomach had been brightly colored by the dye. Early nesting also has a consequence that may be necessary for a breeding strategy that involves seasonal food storing. Young not only hatch earlier but become independent earlier. Early independence in gray jays, pifion jays, and nutcrackers is necessary if young are to establish their own food stores and survive their first winter. This also frees the parents from parental care and allows them to begin caching. Thus, once the combination of seasonal food caching and early breeding has occurred, a number of factors may act to maintain it. Most food-caching birds are year-round residents of the area where they breed. This too may accelerate the date of breeding because territory establishment and pairing can occur at any time and neither time nor energy is consumed by migration. In other species, nonmigratory individuals are known to breed before migrants (Berthold, 1968).

B.

IRRUPTIONA N D EMIGRATION

Eurasian and Clark’s nutcrackers both undergo periodic irruptions, appearing in large numbers outside their usual range. These irruptions coincide with failures in their major food source, pine seeds (Davis & Williams, 1957, 1964). Large scale movements have also been observed within the normal breeding range, emigrant birds sometimes passing through areas where other resident birds are actively storing (Vander Wall, Hoffman, & Potts, 1981). These largescale emigrations illustrate what follows when the food-caching strategy fails to counter the effects of annual fluctuation in food supply. When the crop normally cached for use over the period of scarcity fails to materialize, the birds are without any alternative food supply and are forced to leave the area. Their

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reliance on cached food is complete, and without the option of caching these birds are unable to remain in areas that are now part of their normal range. C.

SOCJAL ORGANIZATION

In the cooperatively breeding acorn woodpecker, both social organization and breeding success are built around the granaries and the stored food supply. Fledging success in spring is significantly correlated with the size of the acorn crop the previous fall and with the number of available storage holes in a territory. Though young in the nest are fed mainly insects and only very occasionally acorns, stored acorns serve as an easily accessible food supply for the adults when they are feeding nestlings. Groups that have depleted their granaries before the young leave the nest fledge only 10% of their young successfully, whereas groups with remaining acorn stores fledge around 80% of their young (Koenig, 1978). Roberts (1979) has argued that “food storing augments evolution of kin selection by extending lifespans and subsequently limiting the availability of suitable habitat for younger birds” (Roberts, 1979, p. 434). Though kin selection is a mechanism rather than a product of evolution, what is probably intended in the quote is that food storing may lead to increased association among kin and thus to nepotism and cooperative breeding by kin. Long life spans and limited opportunities for breeding by younger birds are two factors that reduce the cost of forgoing breeding and may lead to remaining in the natal territory to help rear siblings (Emlen, 1978). Some evidence concerning acorn woodpeckers tends to support Roberts’ ( 1 979) view that food storing and cooperative breeding co-occur. Certain members of the Arizona population of acorn woodpeckers breed as pairs on territories without storage granaries (Stacey & Bock, 1978). They store limited numbers of acorns in loose bark and crevices, and this food supply is quickly depleted. In winter the birds migrate, returning in spring to form new pairs and breed. In the same area, other individuals with storage facilities on their territories are yearround residents and breed communally as described earlier. Though the causal relation between food storing and cooperative breeding is not clear, the two tend to occur together in acorn woodpeckers. But kinship cannot be the full explanation for communal breeding in acorn woodpecker groups (Stacey, 1979). Established groups often acquire new members that are not kin. Only if these individuals were present during mating, which is promiscuous within the group, do they help to rear young (Stayce, 1979). Limited opportunitities for breeding elsewhere, perhaps due to reliance on stored food, may lead to communal breeding in acorn woodpeckers, but a direct link between food storing and cooperative breeding by kin is not apparent. It would

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be valuable to assess whether relatedness influences the relative contributions of different individuals to the communal caches. Apart from acorn woodpeckers, there are other species in which caching and cooperative breeding occur together: Florida scrub jays, for example. But many species which cache food do not breed cooperatively: most tits, nuthatches, and many jays. Furthermore, most cooperative breeders do not cache: white-fronted bee eaters, pied kingfishers, Arabian babblers, and many others. For species such as acorn woodpeckers, in which the availability of granaries does severely limit breeding opportunities, there may be a causal relation between caching, breeding opportunities, and communal breeding. But evolutionary scenarios in which either caching or cooperative breeding evolved first seem equally plausible.

1V. ECONOMICS AND DECISION MAKING

Caching food, like foraging for it, should be understandable in terms of its costs and benefits in time, energy, or other currencies related to fitness. Although no systematic analysis of this kind has been attempted, several of the economic problems faced by food-caching animals have been addressed. A.

SPACING SCATTERED CACHES

When a fox squirrel or a marsh tit takes food from a concentrated source and establishes scattered caches, it has the opportunity to determine the spatial distribution of the caches. It can vary the distance between neighboring caches and can vary the distance food is carried from the source. How the caches are placed will affect the cost in energy or time of storing food, the cost of collecting stored food, and the likelihood that the caches will be safe from other animals. Stapanian and Smith (1978) have produced a model in which the likelihood of loss of a cache is assumed to vary inversely with the distance to the nearest cache. The logic behind this is that although other animals will be able to detect some caches directly or will encounter them by chance, their effectiveness in locating many caches by area-restricted search will decrease as the distance between caches increases. The animal caching the food is assumed to be equally likely to successfully recover it no matter how it is spaced, either because it can remember the location of caches or because it places them in locations it is likely to revisit. The cost of traveling to cache sites is, however, affected by the spacing. Animals are expected to minimize the travel necessary to space caches a suitable distance apart. When food is being removed from a central source, this

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should result in the first caches being placed nearest the source and later caches further away to keep the distance between neighboring caches from decreasing as more food is stored. Stapanian and Smith (1978) tested their model with fox squirrels, and additional tests have been performed by Sherry et al. (1982) with marsh tits and by Kraus (1983) with gray squirrels (Sciurus carolinensis). Results with fox squirrels and marsh tits supported the model’s principal assumption, that loss of stored food decreases with increasing spacing (Stapanian & Smith, 1978; Sherry et al., 1982), but results with gray squirrels did not (Kraus, 1983). In all of these studies, food was placed in artificial cache sites that were as similar as possible to natural caches. The spacing between neighboring caches was varied systematically and the survival of caches was monitored. Stapanian and Smith (1978) found that increasing spacing resulted in increasing survival of caches, as did Sherry et al. (1982). Results with marsh tits also showed that survival reached an asymptote at 7 m between neighboring caches, the spacing observed between neighboring marsh tit caches in the wild. Further spacing did not significantly increase the survival of caches. Kraus (1983), however, found that 95% of experimental caches were removed within a day, no matter what the spacing. Kraus offers an interesting explanation of why food caches are separated at all if, as his results suggest, spacing has little effect on their survival. Removing food from a central concentrated source may decrease the attractiveness of an area to competitors by increasing the amount of time necessary to collect the food. As mentioned earlier, the animal doing the caching would be expected not to incur the same time or energy cost while searching for caches because it determined the sites of caches originally. Nevertheless, it is possible that at spacing greater than the maximum of 8 m used by Kraus (1983) an effect on cache survival would be found. It is also possible that squirrels were able to detect caches directly, by olfaction. Stapanian and Smith’s model is based on the idea that spacing reduces the effectiveness of area-restricted search that occurs after a single cache has been found. If the rate of direct detection is high, the spacing of caches will not protect them. Despite Kraus’s negative result, it seems likely that spacing of caches does affect their likelihood of loss to other animals, and ethological studies of the effect of spacing on predation also support this assumption (Croze, 1970; Tinbergen, Impekoven, & Franck, 1967). There is no evidence, though, that spacing is achieved in the manner the Stapanian & Smith model proposes is the most economical, that is, carrying successive food items further from the source as the density of caches around the source rises. Results with fox squirrels showed no systematic relation between distance and storage sequence. Results with marsh tits showed that in sequences of storage of 100 sunflower seeds, the first seeds were taken significantly further from the source than the last (Sherry et al., 1982). Cowie et al. (1981) also found a significant negative correlation between storage order and distance from the

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source. The cost in time and energy of carrying a seed to a cache can reasonably be assumed to increase with the distance to the cache, so the first items, stored further from the source, were stored at greater cost. There was also a tendency for these seeds to be more widely spaced, and this, in addition to the distance they were removed, would make them less likely to be lost to other animals. Later seeds cost less to store but were more likely to be lost to other animals because of their nearness to the source and their closer packing. The explanation for this pattern may be that animals which store food for a period of only a few days, such as marsh tits, may require a certain minimum quantity of cached food for this period of time. Once this has been attained, additional food will only be stored if the cost of doing so is low. Storing later items nearer the source reduces the cost of storing. This explanation has not been tested directly, however. Given that spacing is advantageous, it is not clear how spacing is achieved while caching. Animals that remember the location of caches could decline to cache unless they were a minimum distance from previous caches. Morris (1962) has suggested that the green acouchi (Myoprocta pratti) disperses its caches by a process of “positive scattering,” that is, by avoiding caching in areas where food was previously cached. Alternatively, animals could vary at random either the direction of departure from the food source or the distance they travel and then cache in any suitable sites they encounter. Marsh tits in the laboratory cache seeds at random with respect to previous caches established during the same bout of storing (Shettleworth & Krebs, 1982). The birds may behave in this way in one part of their territory, then move to another after a particular number of caches are in place. B. CENTRAL PLACEFORAGING Gathering food and carrying it to a burrow hoard is a central place foraging problem (Charnov, 1976; Orians & Pearson, 1979). Food must be collected on repeated foraging trips and carried back to a central place, in this case the burrow. When more than one food item can be carried at a time, the problem the animal faces is how many items to collect before leaving the patch of food and returning to the central place. It can be shown that if the rate of collecting food decreases as a function of the time spent in the patch of food, then larger loads should be carried as the distance between the food source and the central place increases (Charnov, 1976; Orians & Pearson, 1979). Giraldeau and Kramer (1982) found that as chipmunks filled their cheek pouches with seeds, the rate of filling them decreased and that both the time spent gathering seeds in a patch and the size of the resulting cheek pouch load increased with the distance between the burrow and the food source. Vander Wall and Balda (198 1) have also analyzed the problem of how much food can be cached as the distance between the food source and suitable cache

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sites varies. Their model combines a number of the constraints that operate on birds like nutcrackers and pition jays that cache seasonally, such as the amount of time available to harvest and store food, the distance food must be transported, and the minimum amount of stored food required to survive seasonal food scarcity and to breed. Though the model makes no explicitly testable predictions, it points out that adaptations of different kinds, for example, adaptations that increase the load that can be carried or the distance that can be traveled, can affect food storing.

C. INVENTORY DECISIONS Food-caching animals store a supply of food and later use it up. If this process is continual over a period of time, as it is for short-term cachers like marsh tits and South Island robins, decisions about how much food to store are made repeatedly. Acquiring and storing food has many benefits, some of which have already been discussed. But it also has costs. It is reasonable to suppose that natural selection has acted to minimize these costs. In a recent study, Mott-Trille (1983) varied some of these costs systematically in an attempt to discover whether chickadees are sensitive to the costs of storing food. The two costs varied were the cost of gaining access to a patch of storable food and the cost that arises from loss of stored food through spoilage or pilfering by other animals. To vary the first, chickadees were required to hop on a perch to obtain free access to storable sunflower seeds. The number of hops required could be varied, but once the required number of hops had been completed the bird had ad lib access to seeds. In a separate experiment, seeds stored by the bird were removed at random by the experimenter, in an attempt to simulate natural pilfering. The bird’s supply of cached food was pilfered at a rate of either 0, 25, or 50%. The number of seeds stored in a bout of caching increased as the ratio of perch hops required to gain access to seeds increased. The number of seeds stored in a bout decreased as the rate of pilfering increased. Neither experimental manipulation had a significant effect on the number of seeds eaten during a bout, a finding indicating that the manipulations had their effect on storing without influencing immediate energy requirements. A fixed cost for obtaining access to food, which then decreases on a per item basis as more items are stored, and a cost such as pilfering, which increases per item as more items are stored (for example, because in the wild later items are stored nearby in more closely packed sites, as described earlier), resemble the costs incurred in maintaining an inventory of any kind, whether it is stored food, manufactured goods, or raw materials. Inventory theory (Buffa & Miller, 1979; Moore, 1973) labels these costs preparation and holding costs, respectively, and identifies the number of items to add to inventory-the economic order quan-

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tity-as the number that minimizes the sum of preparation and holding costs. Raising the preparation cost raises the economic order quantity, much as raising the ratio requirement raised the number of seeds stored. Raising the holding cost decreases the economic order quantity, much as raising the rate of pilfering decreased the number of seeds stored. Inventory theory may provide a suitable model for some of the decisions made by food-storing animals. Birds like nutcrackers, which use stored food long after it was cached and so are not involved in a continual cycle of storage, depletion, and further storage, may not be faced with quite the same decisions or have the information necessary to behave in the way described for chickadees. D.

TIMING OF RECOVERY

In addition to varying how much food they store, animals that cache food have the opportunity to vary when they use it. Sometimes the pattern is seasonal, as with nutcrackers or ground squirrels that cache in fall and use the stored food several months later, in winter or in spring. Recovery of stored foods supplies is integrated into the nutcracker’s annual cycle of altitudinal migration and nesting, and the ground squirrel’s cycle of hibernation and arousal. For other animals, the cycle of caching and recovery has a much shorter periodicity. Chickadees and tits, South Island robins, northwestern crows, and many raptors show this pattern. Furthermore, these birds show similar diurnal rhythms of recovery, collecting the majority of their caches late in the day (Stevens, 1984; Powlesland, 1980; Collopy, 1977; Mueller, 1974; Rijnsdorp, Daan, & Dikstra, 1981). In the northwestern crow, a tidal cycle rather than a diurnal cycle controls the timing of cache recovery (James & Verbeek, 1984). One way to account for these patterns in recovery is to consider that the value, or contribution to fitness, of a food item may change during the day. For many birds, the hours before dusk are critical, especially in winter. Birds that are active during the day fast overnight and, if they are to survive, must carry with them when they roost sufficient energy reserves to last through the night. McNamara and Houston (unpublished) have shown that, even if food availability is constant during the day, food ingested late in the day will be of greatest value because it is the last opportunity to lay down overnight reserves. If food that is surplus to immediate needs when it is encountered can be stored and recovered later in the day, the risk of failing to find enough food before dusk will be reduced. If, in addition, food is abundant and easy to obtain early in the day and scarce later, this effect will be even more pronounced. Caching is a way of turning food of little value at the time it was encountered into food of high value by investing the time and energy necessary to store it. Kestrels (Falco sparverizis and F . tinnunculus), both in the wild and in captivity, exhibit a peak in cache recovery at the

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end of the day (Collopy, 1977; Mueller, 1974; Rijnsdorp et al., 1981). Recovery of cached food by marsh tits reaches a maximum at the end of the day, not only on the day food was cached, but also for several days afterward (Stevens, 1984). Northwestern crows show a pattern of recovery that is similar, where the availability of food during high tide, rather than overnight, is important (James & Verbeek, 1984). On the western coast of Canada, these birds collect intertidal clams and invertebrates at low tide and store them in grass and among rocks above the high-tide line. Later, when the rising tide covers the major source of food, cached food is collected. James and Verbeek (1984) point out that food may be scarcest early in the breeding season, when females are forming eggs or incubating almost continuously. Males feed females a great deal at this time, and caching may be essential to maintain the supply of food to the female when the tide is high and food difficult to obtain. James and Verbeek tested this by removing the caches of some males as soon as they were established, and observing the effects on the mates of these birds at high tide. Females whose mates could not provide food from their caches left the nest to feed, exposing it to predation and temperature fluctuations more often and for longer periods than the mates of control males with intact caches (James & Verbeek, 1984). In their analysis of caching and recovery by European kestrels, Rijnsdorp et al. (1981) make the point noted earlier, that caching can decouple the need for food and the need to forage for it. Whether we assume a peak in food demand at dusk or a constant demand for food during the day as occurs in incubating female kestrels and northwestern crows, there may be times when availability and demand do not coincide. The major prey of kestrels in the Netherlands, the vole Microtus arvalis, shows several distinct peaks in aboveground activity in the first half of the daylight period and rarely occurs above ground at other times. Prey can be collected when it is available and eaten when needed if caching is an option. Red foxes also deal with short-lived abundance of small mammals in this way (Macdonald, 1976). By decoupling foraging and feeding, caching may permit the timing of meals and the timing of foraging to occur independently, in a way that increases the benefits and reduces the costs of both.

V.

AND FOODPLANTS FOODSTORING

Food-storing animals and the plants from which they obtain food can be interdependent. Food-storing birds rely on the occurrence of large seed or nut crops, in excess of immediate requirements, to reside in an area and breed successfully. Crop failure can result in large-scale irruptive movements and failed breeding attempts (Koenig, 1978; Vander Wall & Balda, 1977). But foodstoring animals are also important agents of dispersal for seed- and nut-bearing plants. In this way the interests of food-storing animals and their food plants

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coincide. Both benefit from storage of seeds where they will survive intact, free from attack by rot, fungus, insects, or other seed predators. Scattering of storage sites can aid both dispersal by the plant and successful recovery by the caching animal. But in other ways the interests of plant and animal are opposed. Germination means loss of energy and nutrients for the cacher. Some rodents notch stored acorns-thereby killing the embryo-to prevent germination (Barnett, 1977; Fox, 1982); others cache large numbers of pine cones in burrow hoards where germination is unlikely (Hutchins & Lanner, 1982; Smith, 1970); and the storage behavior of acorn woodpeckers probably results in little successful dispersal by oaks (Koenig, 1980). One of the most striking and best-described interdependences between plants and food-storing animals is that between two pines of western North Americathe whitebark pine (Pinus albicaulis) and the pifion pine ( P . edulis)-and Clark’s nutcracker (Tomback, 1982, 1983; Hutchins & Lanner, 1982; Vander Wall & Balda, 1977). The benefits to nutcrackers of storage of the seed crops of these pines, including early nesting and year-round residence, have been described earlier. In the following sections, 1 shall describe how some pines benefit from storage of their seeds and the adaptations they possess to promote caching. A.

NUTCRACKERS AND PINES

I. Caching by Nutcrackers Before the cones of whitebark pine ripen, they are attacked by nutcrackers and the seeds are removed and eaten. This is a simple case of seed predation and is a loss to the pine, both reproductively and energetically, with no dispersal consequences. But when the seeds ripen, in August and September, nutcrackers begin to store large numbers of them. They are buried in the soil at a depth of 1-3 cm, a depth suitable for germination. For artificial cultivation of whitebark pine, seeds are covered with about 1.25 cm of soil (Tomback, 1982). Although some caches are made in conditions unsuitable for germination or maturation, for example, off the ground or at the base of a large tree, many caches are made in open areas away from neighboring trees (Hutchins & Lanner, 1982; Tomback, 1982). Clark’s nutcrackers cache three to five times the number of seeds they require-estimated on the basis of their energy demands and the length of time they are resident at the elevations of whitebark pine. Even assuming breeding by each bird, there is still about twice as much seed cached as is required for survival and feeding the young. Each bird leaves behind some unharvested seed-as much as 10,000 cached seeds per year for some individuals. Not all will be in conditions suitable for germination, but from field observations of cache sites, Tomback (1982) estimated that about 40% would be. Seeds stored

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by nutcrackers have been shown to remain viable after storage, and the birds are capable of discriminating ripe seeds from aborted or diseased seeds at the time they collect them from the tree. A variety of food-storing animals possess morphological adaptations for storing: the salivary glands of gray jays, which are used to produce sticky boli of food that adhere to the cache site (Dow, 1965), and the cheek pouches of rodents (Long, 1976) are two examples. Nutcrackers possess a distensible sublingual pouch with a volume of 20-30 ml that enables them to carry 50 or more pine seeds at a time (Bock, Balda, & Vander Wall, 1973).

2. Adaptdons of Pines Whitebark pines possess a number of features which promote seed collection by nutcrackers. Cones are found near the top of the tree and point out, perpendicular to the vertical branches, in contrast with the cones of wind-dispersed pines, which normally point down toward the ground. Ripe whitebark pine cones are indehiscent: they do not open. They must be pried, pecked, or chewed open to release the seed and do not possess the protective spines found on the cones of most wind-dispersed pines (Tomback, 1982). The seeds of the whitebark pine are wingless, large, energy rich (about 32 kJ g - ’ ) , and high in fat content, all adaptations to promote dispersal by vertebrates. It should be stressed that this is unusual for pines. Many species of pines have a variety of traits which function to discourage vertebrate predation (Smith, 1970). Whitebark is not the only pine dependent on seed-caching animals for dispersal. Piiion pine seeds are also cached by Clark’s nutcracker, and this pine shares many features with the whitebark. Piiion pine produces a large wingless seed that is energy rich (31 kJ g - I , Vander Wall & Balda, 1977). Cone orientation is horizontal and inclined slightly upward. In addition, fully developed seeds are rich dark brown in color, whereas aborted seeds are a much lighter color, and nutcrackers use this cue to select seeds. In a group of six pines examined by Vander Wall and Balda (1977), some of which were vertebrate-dispersed and some not, piiion pine seeds had the lowest ratio of shell thickness to seed volume, a feature which facilitates rapid hulling of seeds by nutcrackers. The cone itself also possesses unique traits. Cones of piiion pine, unlike those of whitebark, open fully, thereby presenting the large seeds to view from above. The cone has shorter scales and fewer of them than other pines, and the scales are shaped to prevent seeds from being dislodged before being removed by the bird. The availability of both whitebark and piiion pine seeds is timed in ways that favor removal and caching. To promote caching, a food must be available in large numbers over a span of time sufficiently long to attract food-storing animals and supply food in excess of immediate requirements. But the food cannot be continuously available either, for then storing would not be necessary to dampen fluctuations in the animal’s supply. Whitebark cones on the same tree ripen simultaneously, and ripening occurs from August to October only (Tom-

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back, 1982). Piiion pine are also available for a relatively long but clearly demarcated period of about 50 days in autumn (Vander Wall & Balda, 1977). In addition, the piiion pine exhibits masting-synchronous seed production by a population at irregular intervals longer than 1 year (Silvertown, 1980). The standard account of the evolution of masting is that the abundant crop satiates seed predators and ensures that some seeds survive and disperse. There is thus selection against seeding out of synchrony with the population (Janzen, 1971; Ligon, 1978). It has also been suggested that the years of no seed production keep the population size of seed predators from increasing. Silvertown ( 1 980) found that for some of the mast seeding data he examined, there were significant correlations between seed survival and crop size, data that tend to support the former idea. There was no indication, however, that the interval between mast years was an adaptation to prevent increase in the predator population. Instead, Silvertown (1980) concluded that the mast interval was an environmental constraint on the time required to produce a large seed crop. Caching can be seen as a form of seed predation which turns into dispersal only when seeds are available in excess of the food-storing animal’s requirements. Thus, masting may be promoted by food-caching animals. The presence of food-storing seed predators cannot, however, be the sole factor promoting masting, since many wind-dispersed pines show masting.

3. Dispersal of Pines There are several direct lines of evidence that the adaptations of pines just described, and the behavior of food-storing birds, do result in successful dispersal of pines. Whitebark pine seedlings and saplings are often found growing in tight clumps of two to five stems. This growth pattern, especially in young trees, is persuasive evidence of germination from caches (Tomback, 1982). Multiple stems in mature trees can arise for a variety of reasons, but multiple stems in young trees usually indicate multiple seeds, germinating together. Hutchins and Lanner (1982) found that whitebark pine seeds, placed experimentally on the soil surface, very rarely survived more than a few days, whereas seeds cached 3 cm below the surface survived at rates ranging from 10 to 63%. Of the potential seed predators observed feeding on whitebark seed, including steller’s jay (Cyanocitta stelferi), red-breasted nuthatch (Sitta canadpnsis), chipmunk, and red squirrel (Tarniasciurus hudsonicus), only Clark’s nutcracker effectively dispersed and established whitebark pine. Lanner and Vander Wall (1980) have described a similar, multiple-trunked growth pattern in limber pine, the seeds of which are also cached by Clark’s nutcrackers. They suggest that caching may be particularly important in dispersal of this tree into burned areas. At the burned site they examined, they found both wind-dispersed firs growing singly and nutcracker-dispersed limber pine, 23% of which had multiple trunks (Lanner & Vander Wall, 1980). The relationship between food-storing animals and their food plants has been

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called symbiosis (Bossema, 1979), mutualism (Tomback, 1982), reproductive interdependence (Ligon, 1978), coadaptation (Vander Wall & Balda, 1977), and coevolution (Smith, 1970). The relationship may, of course, vary from case to case, but most of these authors were describing very similar situations. The food plant had its seeds removed by a food-storer, the food-storer survived periodic scarcity or obtained the energy to breed successfully by recovering some, but not all, of its stored food. In some cases storage conferred a benefit on the plant, in the form of dispersal; in other cases storage of seed was a reproductive loss which the plant possessed adaptations to prevent. Various definitions of coevolution, broad and restrictive, have been advanced in the past 20 years (Futuyma & Slatkin, 1983). They range from “an evolutionary change in a trait of the individuals of one population in response to a trait of the individuals of a second population, followed by an evolutionary response by the second population to the change in the first” (Janzen, 1980, p. 611) to more relaxed definitions that embrace any adaptation to an identifiable feature of the biotic environment. It is clear that trees like the piiion and whitebark pine possess adaptations that promote removal and caching of seeds and that Clark’s nutcracker possesses adaptations for doing so. Because both the Cembrae pine group, to which the whitebark belongs, and the nutcracker have a Eurasian origin, they may be coevolved in the sense of the restrictive definition (Tomback, 1983). The piiion pine is thought to have originated in Mexico (Lamer, 1981). If its adaptations to promote caching are convergent with the Cembrae group, rather than derived from them, then some of its traits may have evolved in response to the presence of nutcrackers and other food-storing corvids in the western hemisphere. B.

SQUIRRELS AND PINES The course of coevolution does not always run smoothly. Pine squirrels (Tu-

miusciurus) store entire cones of lodgepole pine (Pinus cunturtu), which they cut

from the tree before the cones can open and shed their seeds. Cones are stored in large numbers in central middens where very few seeds successfully germinate (Smith, 1970). The squirrels are also major predators of cones on the trees. Lodgepole pine shows a suite of adaptations that, unlike the traits of whitebark or pifion pine, function to deter removal and storage of seeds and cones. Hard tissue is concentrated at the base of the cone and at the base of scales, the areas squirrels must bite through to remove cones or extract seeds. Cones are attached flush against the branch, making it difficult for squirrels to cut them free with the incisors. Cones occur in clumps or whorls of two to five, protecting their points of attachment, are equipped with spiny scales, and point back along the branch to which they are attached, deterring squirrels that approach from the direction of the trunk. Finally, scales that are larger than the others protect the point of attachment of the cone (Smith, 1970).

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These adaptations, occurring in a pine that fails to benefit from caching of its seeds, provide a striking contrast with the traits described earlier for pines that are dispersed and established as a result of caching by nutcrackers and other birds. But pine squirrels continue to collect and store the cones of lodgepole pine and possess a number of adaptations to this end. Tamiasciurus hudsonicus, which collects and caches lodgepole pine cones on the eastern slopes of the Cascade Range in western North America has a larger skull and jaw musculature compared to its congener Tamiasciurus douglasii, which is found on the western slopes of the Cascades, and which rarely collects lodgepole cones (Smith, 1970). Limber pine (Pinus flexilis) which has its seeds taken by both Clark’s nutcracker and Tamiasciurus hudsonicus possesses a compromise combination of traits, some of which hinder squirrel predation while others promote removal, caching, and dispersal of seeds by nutcrackers (Benkman, Balda, & Smith, 1984). C.

JAYS AND OAKS

European jays (Garrulus glandurius) and the pedunculate oak (Quercus robur) are involved in an interdependence similar to that of nutcrackers and pines (Bossema, 1979). Dispersal of acorns by jays reduces the probability of acorn predation under oaks, and storage in soil or leaf litter probably leads to high rates of germination, as well as reducing the exposure of acorns to temperature fluctations, moisture, and fungal attack. Jays prefer to store acorns in open areas, away from other trees. Such sites provide well-lit conditions suitable for seedling growth and reduced likelihood of attack by defoliating caterpillars. Jays are very discriminating in their choice of acorns for storage and may have selected for large-sized acorns in oaks they regularly disperse and for a long, thin acorn that can easily be carried in the esophagus. Seedlings with strong root systems that can withstand inspection by a jay attempting to recover its stored acorn in spring may also be an adaptation of oaks to dispersal by jays (Bossema, 1979). In North America, acorn storage by blue jays (Cyanocitta cristata) may result in dispersal and establishment of pin (Quercus palustris) and other oaks (DarleyHill & Johnson, 1981).

VI.

CONCLUSIONS

Despite the diversity alluded to in the introduction, a few common features do emerge in the behavior of food-storing animals. Memory is used by a variety of animals to relocate scattered caches. Storing food has become an essential feature of the annual cycle of many animals, is a prerequisite for successful breeding

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in some species, and has advanced the time of breeding in others. Animals that recover cached food soon after it is stored frequently show a diurnal pattern of caching early in the day and recovering late in the day. Finally, food-storing animals are used as agents of dispersal by a variety of plants. But many questions about the behavior of food-storing birds and mammals remain unanswered. Its restriction to certain families and its pattern of occurrence within these families are not well understood. I have mentioned that in some birds the methods of handling food may have been responsible for the original innovation of leaving food secured in place and returning to it later. Although this seems plausible, it is difficult to test such a conjecture about the evolutionary origins of the behavior. More amenable to testing are hypotheses about the current selective pressures that maintain food storing. To give an example, the largest European parids, the great and blue tits (Purus mujor and P. cueruleus) rarely, if ever, store food, whereas all of the smaller species, the marsh, willow, crested, and coal tits (P. pulustris, P . montanus, P. cristutus, and P. uter), do (Haftorn, 1956; Richards, 1958). The larger species may not store food because the energetic consequences of large body size make it unnecessary or because they can aggressively defend concentrated food sources more successfully as a result of their size, or for other reasons unrelated to body size. These hypotheses and many others about the current adaptive significance of storing seem testable using a combination of comparative methods and experimental behavioral ecology. One particularly interesting comparative question concerns the nature of spatial memory in birds like nutcrackers, tits, and chickadees. It is clear that these birds can accurately remember large numbers of storage sites for periods ranging from a few days to weeks and possibly much longer. It is not clear, however, how these birds perform on spatial tasks that do not involve cache recovery or whether noncaching species have similar abilities that are used for other spatial problems, such as foraging. I have argued elsewhere that when more is known about the behavior of other species on comparable spatial tasks, the abilities of food-storing birds may not seem so unusual (Sherry, 1984a). Others have suggested that spatial memory in these birds is an “adaptive specialization” of memory for the task of recovering scattered food caches (Shettleworth, 1983; Shettleworth & Krebs, 1982). Adaptive specializations in the mechanisms of learning and memory were proposed by Rozin and Kalat ( I 97 I ) to account for poison avoidance and specific hungers in rats, which could not easily be encompassed by traditional models of learning and memory. An adaptive specialization may refer to a specialized ability within a species that is used for some learning and memory tasks but not others and may also refer to abilities possessed by some species but not others. The most fruitful approach to the question is probably to test the performance of closely related species such as corvids or paridssome of which store food and some of which do not-on a comparable set of

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spatial memory problems. Food-storers may possess unique abilities not shared by nonstorers, they may perform well only on cache recovery problems, or they may not differ in behavior from other species. Whatever the outcome, the results would have implications for the general question of whether there exist in animals and humans multiple memory systems serving different functions (Schachter & Moscovitch, 1984). Food storing has a number of social consequences, described earlier. In communally living species such as the acorn woodpecker, the social consequences of food storing are particularly interesting. The relative contributions to communal caches and the use of these stores by different members of the group remain little-understood problems. A number of attempts have been made to apply economic or optimality models to food storing. None of these has proved particularly conclusive, although this approach seems ideally suited to analyzing diurnal patterns in caching and the effects of food availability, loss of stored food, and energy requirements on caching. Furthermore, larder hoarding animals may have largely unknown repertoires of behavior that function to control parasitic attack on the hoard, to exploit different stored foods at their time of maximum nutrient or energetic value, and to disperse in time the use of foods containing essential nutrients (Smith & Reichman, 1984; Reichman & Fay, 1983). Finally, the relations between food-storing animals and their food plants, which appear in some cases to form suites of coevolved traits, present a number of interesting problems. The availability of food and the size of individual food items probably have major effects on how much food is stored and how storage sites are distributed. Variation in the size and number of seeds may provide plants with the capacity to finely tune the range of dispersal and the spacing of germination sites, through effects on the behavior of food-storing birds and mammals. Acknowledgments I would like to thank Jerry Hogan, John Krebs, Diana Tomback, and Stephen Vander Wall for their many helpful comments on the manuscript and Alasdair Houston and Catie Rechten for their help with inventory models. Alasdair Houston, Jim Reichman, Allen Stevens, Dan Strickland, and Karen Whillans-Browning kindly gave permission to quote unpublished material and provided many helpful suggestions. Ellen Blais and Glynis Cole Johnson are both gratefully thanked for their help in preparing the manuscript. This research was supported by the Natural Sciences and Engineering Research Council of Canada and a NATO Collaborative Research Grant.

References Abbot, H. G . & Quink, T. F. (1970). Ecology of eastern white pine seed caches made by small forest mammals. Ecology 51, 271-278.

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Anderson, M., & Krebs, J. R. (1978). On the evolution of hoarding behaviour. Anim. Behav. 26, 707-7 I 1. Applegate, R. D. (1977). Possible ecological role of food caches of loggerhead shrike. Auk 94,391392. Balda, R. P. (1980). Recovery of cached seeds by a captive Nucifruga caryocactes. Z . Tierpsychol. 52, 331-346. Balda, R. P, & Bateman, G. C. (1971). Flocking and annual cycle of the piiion jay Gymnorhinus cyanocephalus. Condor 73, 287-302. Balda, R. P, & Bateman, G . C. (1972). The breeding biology of the pition jay. Living Bird 11,s-42. Barnett, R. J. (1977). The effect of burial by squirrels on germination and survival of oak and hickory nuts. Am. Midl. Nut. 98, 319-330. Bateman, G . C., & Balda, R. P. (1973). Growth, development, and food habits of young pitionjays. Auk 90, 39-61, Benkman, C. W., Balda, R. P., & Smith, C. C. (1984). Adaptations for seed dispersal and the compromises due to seed predation in limber pine. Ecology 65, 632-642. Berthold, P. (1968). Die Massenvermehrung des Stars, Sturnus vulgaris in fortpflanzungsphysiologischer Sicht. J . Ornithol. 109, 11-16. Bock, W. J., Balda, R. P., & Vander Wall, S . P. (1973). Morphology of the sublingual pouch and tongue musculature in Clark's nutcracker. Auk 90, 491-519. Bondrup-Nielsen, S. ( I 977). Thawing of frozen prey by boreal and saw-whet owls. Can. J . Zool. 55, 595-601, Bossema, 1. (1979). Jays and oaks: An eco-ethological study of a symbiosis. Behuviour 70, 1-1 17. Broadbent, D. E. (1958). Perception and communication. Oxford: Pergamon. Brown, L., & Amadon, D. (1968). Eagles. hawks and falcons of the world (2 Vols.) New York: McGraw-Hill. Buffa, E. S., & Miller, J. G . (1979). Production-inventory systems: Planning and control (3rd ed.). Homewood, ILL: Irwin. Charnov, E. L. (1976). Optimal foraging, the marginal value theorem. Theor. Pop. Biol. 9, 129136. Collopy, M. W. (1977). Food caching by female American kestrels in winter. Condor 79, 63-68. Cowie, R. J., Krebs, J . R., & Sherry, D. F. (1981). Food storing by marsh tits. Anim. Behav. 29, 1252-1259. Crowder, R. G. (1982). The demise of short-term memory. Acta Psycho/. 50, 291-323. Croze, H. (1970). Searching image in carrion crows. Z . Tierpsycho/. Supp/. 5 . Daan, S. (1981). Adaptive daily strategies in behavior. Hand. Behav. Neurobiol. 4, 275-298. Darley-Hill, S., & Johnson, W. C. (1981). Acorn dispersal by the blue jay (Cyznocitta cristata). Oecologia 50, 23 1-232. Davis, J . , & Williams, L. (1957). Irruptions of the Clark nutcracker in California. Condor 59, 297307. Davis, J . & Williams, L. (1964). The 1961 irruption of the Clark nutcracker in California. Wilson Bull. 76, 10-18. Dorka, V. (1980). lnsektenspeichernde Kleiber Sittu europaea: Zur Unterscheidung von langfristjgem und kurzfristigem Nahrungsspeichcr-Verhalten. Okol. Vogel 2, 145- 150. Dow, D. D. (1965). The role of saliva in food storage by the gray jay. Auk 82, 139-154. Elgmork, K. (1982). Caching behavior of brown bears (Ursus arctos). J . Mammal. 63, 607-612. Elliott, L. (1978). Social behavior and foraging ecology of the eastern chipmunk (Tamias striatus) in the Adirondack mountains. Smihonian Cuntrih. Zoo/. 265, I- 107. Emlen, S. T. (1978). The evolution of cooperative breeding in birds. In J. R. Krebs & N. B. Davies (Eds.), Behavioural ecology: An evolutionary approach (pp. 245-281). Oxford: Blackwell. Erlinge, S. (1969). Food habits of the otter Lutru lutra L . and the mink Mustela vison Schreber in a trout water in southern Sweden. Oikos 20, 1-7.

FOOD STORAGE B Y BIRDS AND MAMMALS

185

Ewer, R . F. (1968). Ethology of’mammuls. London: Elek Science Fox, J . F. (1982). Adaptation of gray squirrel behavior to autumn germination by white oak acorns. Evolution 36, 800-809. Futuyma, D. J . & Slatkin, M.. Eds. (1983). Coewlution. Sunderland MA: Sinauer. Gibb. J. A. (1960). Populations of tits and goldcrests and their food supply in pine plantations. Ibis 102, 163-208. Giraldeau, L. -A,, & Kramer, D. L. (1982). The marginal value theorem: A quantitative test using load size variation in a central place forager. the eastern chipmunk, Tantias striatus. Anim. Beliav. 30, 1036-1042. Gochfeld, M., & Burger, J. (1984). Age differences in foraging behavior of the American robin (Turdus migratorius). Behaviour 88, 227-239. Goodale. M. A,, & Graves, J. A. (1980). Failure of interocular transfer of learning in pigeons Calumlm livia trained on a jumping stand. Bird Beha\,. 2, 13-22. Goodale. M. A,, & Graves, J . A. (1982). Retinal locus as a factor in interocular transfer in thc pigeon. In D. J . Ingle, M. A. Goodale, & R . J. W. Mansfield (Eds.). Analwis of’ visual behavior (pp, 21 1-240). Cambridge, MA: MIT Press. Green, L., Brecha. N., & Gazzaniga, M. S . (1978). Interocular transfer of simultaneous but not successive discriminations in the pigeon. Anim. Learn. Brhav. 6, 26 1-264. Haftorn. S . (1956). Contribution to the food biology of tits especially about storing of surplus food. Part IV. A comparative analysis of Parus atricapillus L.. P . cristatus L. and P . ater L. Det Kgl. Norske Videriskabers Selskahs Skrjfter 4, 1-54. Haftom, S . ( 1973). Lappnieisa Parus cinctus i hekketiden: Forplantning, stemmeregister og hamstring av naering. Sterna 12, 91-155. Haftom. S . (1974). Storage of surplus food by the boreal chickadee Parus hudsonirus in Alaska, with 50me records on the mountain chickadee Pants garnbeli in Colorado. Ornis Scand. 5 , 145161. Harrington, F. H. (1981). Urine-marking and caching behavior in the wolf. Behaviour 76,280-288. Heinrich, B. (1979). Bumblebee economics. Cambridge, MA: Harvard Univ. Press. Henry, J . D. (1977). The use of urine marking in the scavenging behavior of the red fox (Vulpes vulpes). Behaviour 61, 82- 106. Higuchi, H. (1977). Stored nuts Castanopsis cuspidata as a food resource of nestling varicd tits Parus varius. Tori 26, 9- 12. Howard, W. E., Marsh, R . E.. & Cole, R . E. (1968). Food detection by deer mice using olfactory rather than visual cues. Anim. Behav. 16, 13-17. Hutchins. H. E.. & Lanner, R. M. (1982). The central role of Clark’s nutcracker in the dispersal and establishment of whitebark pine. Oecologia, 55, 192-201. Ingram, W. M. (1942). Snail associates of Blarina brevicaudu talpoides (Say). J . Mammal. 23, 255258. James, R. D., McLaren, P. L., & Barlow, J . C. (1976). Annotated checklist of the birds uf‘Ontario. Toronto, Canada: Life Sci. Misc. Publ.. Royal Ontario Museum. James, P. C . , & Verbeek, N . A. M. (1983). The food storage behaviour of the northwcstem crow. Behaviour 85, 276-291. James, P. C . , & Verbeek, N. A . M. (1984). Temporal and energetic aspects of food storage in northwestern crows. Ardea 72, 207-215. Jan7,en. D. H. (1971). Seed predation by animals. Annu. R e v . Ecol. Syst. 2, 465-492. Janzen, D. H. (1980). When is it coevolution’?Evolution 34, 61 1-612. Jarvis, J . U . M., & Sale, J. B. (1971). Burrowing and burrow patterns of East African mole-rats, Tachvorvries, Hrliophobius. and Hererocephalus. J . Zoo/. (London). 163, 45 1-479. Kallander, H. (1978). Hoarding in the rook Corvusfrugilegus. Anser Suppl. 3, 124-128. Kamil, A. C., & Balda. R . C. (1985). Cache recovery and spatial memory in Clark’s nutcrackers (Nuc$raga colrimbiana). 1.Exp. Psycho/.: Anim. Behav. Proc. in press.

186

DAVID F. SHERRY

Kawamichi, T. (1976). Hay territory and dominance rank of pikas (Ochotonaprinceps).J . Mammal. 57, 133-148. Koenig, W. D. (1978). Ecological and evolutionar~v aspects of’ cooperarive breeding in acorn woodpeckers of central coastal Calif~rniu.Ph. D. thesis, University of California at Berkeley. Koenig, W. D. (1980). Acorn storage by acorn woodpeckers in an oak woodland: An energetics analysis. In T. R. Plumb (Ed.), Proceedings oj. the symposium on the ecology, management, and utilization of California oaks (pp. 265-269). Berkeley CA: Pacific Southwest Forest and Range Experimental Station General Technical Report. Kraus, B. (1983). A test of the optimal-density model for seed scatterhoarding. E c d o g . ~64, 608610. Krushinskaya, N. L. (1966). Some complex forms of feeding behaviour of nut-cracker Nucfraga raryocatactes, after removal of old cortex. Zh. Evol. Biachim. Fisiol. 11, 563-568. Kruuk, H. (1972). The sported hyaena. Chicago: Chicago Univ. Press. Lanner, R . M. (1981). Thepifionpine. A naturaland cultural histor-y. Reno: Univ. of Nevada Press. Lanner, R. M. (1982). Adaptations of whitebark pine for seed dispersal by Clark’s nutcracker. Can. J. For. Res. 12, 391-402. Lanner, R. M. & Vander Wall, S . B. (1980). Dispersal of limber pine by Clark’s nutcracker. J . Forest. 78, 637-639. Ligon, J . D. (1978). Reproductive interdependence of pition jays and pition pines. Ecol. Monogr. 48, 111-126. Lohrl, H . ( 1 950). Beobachtungen zur Soziologie und Verhaltensweise von Sumpfnieisen (Parus palustris communis) im Winter. Z. Tierpsychol. 7 , 4 17-424. Long, C. A . (1976). Evolution of mammalian cheek pouches and a possible discontinuous origin of a higher taxon (Geomyoidea).Am. Nat. 110, 1093-1097. Macdonald. D. W. (1976). Food caching by red foxes and some other carnivores. Z . Tierpsychol. 42, 170- 185. MacRoberts, M. H. (1970). Notes on the food habits and food defense of the acorn woodpecker. Condor 72, 196-204. MacRoberts, M. H., & MacRoberts, B. R . (1976). Social organization and behavior of the acorn woodpecker in central coastal California. Ornithol. Monogr. (21), I- 1 15. Malcolm, J. R. (1980). Food caching by African wild dogs (Lycaon pictus). J. Mammal. 61, 743744. Marriott, B. M., & Salzen, E. A. (1979). Food-storing behavior in captive squirrel monkeys (Saimiri sciureus). Primates 20, 307-3 I 1. McNamara, J., & Houston, A. 1. The common currency ,for behavioral decisions. Unpublished manuscript. Mewaldt, L. R. (1956). Nesting behavior of the Clark nutcracker. Condor 58, 3-23. Moore, F. (1973). Production management (6th ed). Homewood, ILL: Irwin. Morris, D. (1962). The behaviour of the green acouchi (Myoprocra pratti) with special reference to scatter hoarding. Pror. Zool. Soc. (London) 139, 701-732. Mott-Trille, R. (1983). Food storage: An inventory model. B.Sc. thesis, University of Toronto. Mueller, H. C. (1974). Food caching behaviour in the American kestrel (Falco sparverius). Z . Tierpsychol. 34, 105-1 14. Murdock, B. B., Jr. (1976). Item and order information in short-term serial memory. J . Exp. Psycho/: Gen. 105, 191-216. Murie, J. 0. (1977). Cues used for cache finding by agoutis (Dasyproc/apunctata). J . Mammal. 58, 95-96. Myton, B. A., & Ficken, R. W. (1967). Seed-size preference in chickadees and titmice in relation to ambient temperature. Wilson Bull. 79, 3 19-321. Nowak, R. M., & Paradiso, J. L. (1983). Walker’s mammals of the world (4th ed.). Baltimore: Johns Hopkins Univ. Press.

FOOD STORAGE BY BIRDS A N D MAMMALS

187

O’Keefe, J . , & Nadcl, L. (1978). The hippocampir.7 U S a cognitive map. Oxford: Clarcndon. Olton, D. S. (1982). Spatially organized behaviors of animals: Behavioral and neurological studies. In M. Potegal (Ed.), Spatial abilities: Development and ph,vsio/ogical,fi)undations (pp, 335360). New York: Academic Press. Orians, G . H., & Pearson, N. E. (1979). On the theory of central place foraging. In D. J . Horn, G . R. Stairs, & R. D. Mitchell (Eds.) A ~ I U / . Yojecologicul S~S svstems (pp. 155-177). Columbus: Ohio State Univ. Press. Panuska, J . A . (1959). Weight patterns and hibernation in Tamios striatus. J . Mammal. 40, 554566. Perrins, C. M. (1970). The timing of birds’ breeding seasons. fhis 112, 242-255. Powlesland, R . G . (1980). Food-storing behaviour of the south island robin. Maitri Oru 8, I I 20. Powlesland, R. G. (1981). The foraging behaviour of the south island robin. Notorni.y 28, 89-102. Reese, J . . G. (1972). A Chesapeake barn owl population. Auk 89, 106-1 14. Reichman, 0. J . , & Fay, P. (1983). Comparison of the diets of a caching and a noncaching rodent. Am. Nut. 122, 576-581. Richards, T . J . (1958). Concealment and recovery of food by birds, with some relevant observations on squirrels. Br. Birds 51, 497-508. Rijnsdorp, A., Daan, S . , & Dijkstra, C. (1981). Hunting in the kestrel, Falco tinnuticulus, and the adaptive significance of daily habits. Orcologiu 50, 391-406. Roberts. R. C. (1979) The evolution of avian food-storing behavior. Am. Nut. 114, 418-438. Robinson, A. (1956). The annual reproductory cycle of the magpie, Gvmnorhina dorsalis Campbell. in south-western Australia. Emu 56, 233-336. Rozin. P., & Kalat, J. W. (1971). Specific hungers and poison avoidance as adaptive specializations of learning. Psycho/. Rev. 78, 459-486. Schachter, D. L., & Moscovitch, M. (1984). Infants. amnesics, and dissociable memory systems. In M. Moscovitch (Ed.), lnfurir m e m o p (pp. 173-216). New York: Plenum. Schaller, G . B. (1972). The Serengeti lion. Chicago: Univ. Chicago Press. Shaffer. L. (1980). Use of scatterhoards by eastern chipmunks to replace stolen food. J . Mammal. 61, 733-4. Shaw, W. T. (1934). The ability of the giant kangaroo rat as a harvester and storer of seeds. J . Mammal. 15, 275-286. Sherry, D. F. (1982). Food storage, memory, and marsh tits. Anim. B e h m . 30, 631-633. Sherry, D. F. (1984a). What food-storing birds remember. Can. J . Psycliol. 38, 304-321. Sherry, D. F. (1984b). Food storage by black-capped chicadees: Memory for the location and contents of caches. Atiim. Behav. 32, 451-464. Sherry, D. F., Avery, M. A , , & Stevens, A. (1982). The spacing of stored food by marsh tits. Z . Tierpsyrhol. 58, 153- 162. Sherry, D. F., Krebs, J. R., & Cowie, R. J. (1981). Memory for the location of stored food in marsh tits. Anim. Behav. 29, 1260-1266. Shettleworth, S. J . (1983). Memory in food-hoarding birds. Sci. Am. 248, 102-110. Shettleworth. S. J . , & Krebs, J. R. (1982). How marsh tits find their hoards: The roles of site preference and spatial memory. J . Exp. Psycho/: Anim. Behut). Proc. 8, 354-375. Silvertown, J. W. (1980). The evolutionary ecology of mast seeding in trees. B i d . J . Litin. SOC. 14, 235-250. Smith, C. C. ( 1970). The coevolution of pine squirrels (Tamiasciurus) and conifers. Ecol. Motiogr. 40, 349-371. Smith, C. C.. & Reichman. 0. J . (1984). The evolution of food caching by birds and mammals. Ann. Rev. Ecol. Spsr. 15, 329-351. Stacey, P. B. (1979). Kinship, promiscuity, and communal breeding in the acorn woodpecker. Behap. Ecol. Sociohiol. 6, 53-66.

188

DAVID F. SHERRY

Stacey, P. B., &Bock, C. E. (1978). Social plasticity in the acorn woodpecker. Science 202, 12981300. Stapanian, M. A , , & Smith, C. C. (1978). A model for seed scatterhoarding: Coevolution of fox squirrels and black walnuts. Ecology 59, 884-896. Steiniger, von, F. (1950). Beitrage zur Soziologie und sonstigen Biologie der Wanderratte. Z . Tierpsychol. 7, 356-379. Stevens, A. (1984) The food storage behaviour of marsh tits and shrikes. D. Phil. thesis, Oxford. Strickland, D. A lifp history of the gray jay. Unpublished manuscript. Swanberg, P. 0. (1981). Kullstorleken hos nijtkrika Nucifruga caryocatactes i Skandinavien, relaterad till fijrengiende Brs hasselnottillglng. Var Fagelvarld 40, 399-408. Tinbergen, N., Impekoven, M., & Franck, D. (1967). An experiment on spacing-out as a defence against predation. Behaviour 28, 307-321. Tomback, D. F. (1978). Foraging strategies of Clark’s nutcracker. Living Bird 16, 123-161. Tomback, D. F. (1980). How nutcrackers find their seed stores. Condor 82, 10-19. Tomback, D. F. (1982). Dispersal of whitebark pine seeds by Clark’s nutcracker: A mutualism hypothesis. J . Anim. Ecol. 51, 451-467. Tomback, D. F. (1983). Nutcrackers and pines: Coevolution or coadaptation? In M. H. Nitecki (Ed.), Coevolution (pp. 179-223). Chicago: Univ. of Chicago Press. Tomback, D. F., Bunch, K. G . , & Sullivan, 0.S. Cache recovery by Clark’s nutcracker in a cuelimited environment. Unpublished manuscript. Turcek, F. J., & Kelso, L. (1968). Ecological aspects of food transportation and storage in the Corvidae. Commun. Behav. B i d . Part A 1, 271-297. Vander Wall, S. B. (1982). An experimental analysis of cache recovery in Clark’s nutcracker. Anim. Behav. 30, 84-94. Vander Wall, S . B., & Balda, R. P. (1977). Coadaptations of the Clark’s nutcracker and the pinon pine for efficient seed harvest and dispersal. Ecol. Monogr. 47, 89-1 1 1 . Vander Wall, S. B . , & Balda, R. P. (1981). Ecology and evolution of food-storage behavior in conifer-seed-caching corvids. Z . Tierpsychol. 56, 217-242. Vander Wall, S . B., Hoffman, S . W., & Potts, W. K. (1981). Emigration behavior of Clark’s nutcracker. Condor 83, 162- 170. Vander Wall, S . B., & Hutchins, H. E. (1983). Dependence of Clark’s nutcracker, Nucijraga columbiona, on conifer seeds during the postfledging period. Can. Field-Naturalist 97, 208214. Whillans-Browning, K. V. The influence of ,food iype on hoarding behaviour in black-capped chickadees (Parus atricupillus). Unpublished manuscript. Wrazen, J . A., & Wrazen, L. A. (1982). Hoarding, body mass dynamics, and torpor as components of the survival strategy of the eastern chipmunk. J . Mammal. 63, 63-72. Yahner, R . H. (1975). The adaptive significance of scatter hoarding in the eastern chipmunk. Ohio .I. Sci. 75, 176-177.

ADVANCES IN THE STUDY OF BEHAVIOR. VOI. 15

Vocal Affect Signaling: A Comparative Approach KLAUS R. SCHERER DEPARTMENT OF PSYCHOLOGY UNIVERSITY OF GIESSEN GIESSEN, FEDERAL REPUBLIC OF GERMANY

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Empirical Evidence on Vocal Indicators of Emotion. . . . . . . . . . .... A. Studies on Affect Vocalization in Animals , . . . . . . . , , . . . . . . . , , . . . . B . Studies on the Vocal Expression of Emotion in Humans.. . . . . . . . . . . 111. A Psychobiological Approach to Emotion . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. The Nature and Function of Emotion , . . . . . . . . , , . . . . . . , , . . . . . . , . B. Facet Description of Emotional States. . . . . . . . . . . . . . . . . . . . , , . . . . . C. The Phylogenetic and Ontogenetic Continuity of Emotion . . . . . . . . . . IV. Emotional Determinants of Vocalization . . . . , . . . . . . . . . . . . . . . . . . . . A. Types and Modalities of Vocalizations . , . , . . . . . . . . . . . . . . . . . . . . . . B. Internal Push and External Pull Effects.. , . . . . . . . . . . . . C. Relative Importance of Push and Pull Effects.. . . . . . . . . . . . . . . . . . . . D. Deception in Vocal Signaling. . . . . . . . . . . . . . . Expression. . . . . . . . . . . V. The Component Patterning Theory of Vo .................... A. The Conceptual Framework . . . . . . B . Detailed Predictions of Component .................... VI. Cross-Species Universality in the Component Patterning of Vocal Expression.. . . . . . . . . . . . , . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Major Types of Emotional States. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Transitions between Types. . . . , . . . . . . . . . . . . . . . . . . ............................. . . .. . . . . . . . VII. Conclusion . . , . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I. II.

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INTRODUCTION

In his seminal work The Expression of the Emotions in Man und Animuls, published over a century ago, Charles Darwin began his description of the means of expression in animals by discussing the role of vocalization: “With many kinds of animals, man included, the vocal organs are efficient in the highest degree as a means of expression. . . . when the sensorium is strongly excited, the muscles of the body are generally thrown into violent action; and as a I 89

Copyright (0 1985 by Acadcmic Prcss. Inc All right, of rrproduction in any lomi rewrved. ISBN ll-12-(x1451S-X

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consequence, loud sounds are uttered, however silent the animal may generally be, and although the sounds may be of no use” (Darwin, 1872/1965, p. 83). Unfortunately, a century has not been a period long enough to obtain sufficient evidence relevant to Darwin’s claim concerning the importance of vocalization in emotional expression. Recent reviews of the literature (Siegman, 1978; Scherer, 1979a,b, 1981a,b; Williams & Stevens, 1981) have shown that our knowledge about how emotions are expressed in voice and speech is still rather limited. The same seems to hold for animal communication. Although there are many important studies on patterns of acoustic communication in different species of animals (Green & Marler, 1979; Sebeok, 1977; Snowdon, Brown, & Petersen, 1982), biologists and ethologists have tended to shy away from using the term emotion in connection with animal signaling, using instead more neutral terms such as arousal, motivational stute, or behuvior intention. Consequently, the issue of emotional expression in animal calls rarely has been addressed directly. During the past two decades, the term-and the phenomenon of-emotion was considered to be somewhat dubious and rather unsavory in both biology and psychology. This avoidance has led to a marked decline in the number of scientific investigations of this important aspect of behavior in man and animals. There are signs that this situation is likely to change. Emotion is rapidly becoming a legitimate topic for theory and research in many social and behavioral sciences (see Ekman & Scherer, 1984), and it is tempting to predict that the “cognitive revolution” in the sixties will be followed by an “affective revolution’’ in the nineties. Similarly, the vocal expression of emotion is getting increasingly more attention. In the area of acoustic animal communication, important work by Eisenberg (1974, 1976), Marler and his associates (Marler, 1984; Green, 1975; Marler & Tenaza, 1977; Seyfarth & Cheney, 1982), Morton (1977), and Ploog and his associates (Ploog, 1974; Jiirgens & Ploog, 1976; Jiirgens, 1979, 1982), and Tembrock ( 1 97 1, 1975) has demonstrated the correspondence between acoustic characteristics of animal vocalizations and specific emotional and motivational states. In the area of human nonverbal communication research, there has been a revitalization of interest in the vocal expression of emotion, particularly in the clinical (Darby, 198I ; Scherer, 1982~)and developmental contexts (see Scherer, 1982b; Blount, 1982). In this article, a comparative approach focusing on the phylogenetic continuity and functional significance of vocal expression is advocated. After reviewing the empirical evidence on vocal indicators of emotion in different species, a theoretically derived set of hypotheses concerning the relationships between emotional states and phonatory-articulatory patterns as well as their acoustic correlates in affect vocalizations will be proposed. The theoretical arguments are based on a new model of emotion-the component process model-and a sequence theory of emotional differentiation (Scherer, 1981c, 1983a, 1984a), which will be outlined briefly to document the bases for the predictions concerning vocal indicators of emotional states.

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EMPIRICAL EVIDENCE O N VOCAL INDICATORS OF EMOTION

STUDIES O N AFFECTVOCALIZATION I N ANIMALS

Most animal vocalizations seem to serve as indicators of motivational state: “It is a commonly expressed view that the signalling behavior of animals is more susceptible to control by the kind of physiological states known in common parlance as ‘affective’ or ‘emotional’. . . . In most of the circumstances in which animal signalling occurs, one detects urgent and demanding functions to be served, often involving emergencies for survival or procreation” (Marler, 1977, p. 54). This does not imply that animal vocalizations signal only underlying affective states and their physiological manifestations. As the work of Seyfarth, Cheney, and Marler on vervet monkey (Cercopithecus urthiops) alarm calls has demonstrated, there are clear representational elements in some calls (e.g., alarm calls referring to specific predators) that may well be related to some kind of “cognitive” rather than purely affective processes (Marler, 1984; Seyfarth & Cheney, 1982). The types of categories commonly used to describe animal calls (alarm, threat, fear, contact, discomfort) show the importance of emotion-producing antecedent situations and the respective affective reactions for the classification of these vocal signals. So far, there has been little systematic work on animal communication in which an attempt is made to determine the nature of the relationships between specific affect states and their antecedents on the one hand and acoustic characteristics of the respective vocalizations (indicators) on the other hand. In most studies the authors carefully catalog the different types of calls, the frequency of their occurrence, the nature of the eliciting situation including context variables, and, in the more recent studies, provide detailed acoustic descriptions of the call (often using spectrographic analysis). The disadvantage of a strictly classificatory approach is that correspondences between specific acoustic characteristics found in several different calls and common affect-producing elements in the respective eliciting situations are difficult to characterize unless underlying relationships between acoustic dimensions and emotional states are explicitly conceptualized. A major impetus toward studying these underlying relationships between affective dimensions, such as arousal, and specific acoustic features stems from important work on the gradedness found in the vocalization systems of some species. For example, in many primate species, calls are not stereotyped; that is, calls are produced with essentially the same acoustic form over individuals and situations but are highly variable in terms of frequency, spectral composition, and duration (Eisenberg, 1974, 1976; Could, 1983; Green, 1975; Jiirgens, 1979; Marler, 1965; Marler & Tenaza, 1977; Rowell & Hinde, 1962). This work has shown that complex patterns of variations in the acoustic structure of the calls in species with graded call systems seem to be closely linked to continuously

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varying affective states. Furthermore, it seems rather likely that the variations in the acoustic signal are used by receivers to infer complex and subtle shadings in the meaning of a call both in terms of the specific nature of the eliciting condition as well as in terms of fine-grained variations in the affective response of the sender. A cautionary note must be added at this point. It is possible that many variations in acoustic structure that were interpreted as graded or continuous by early investigators reveal discrete call types upon closer investigation (see Gouzoules, Gouzoules & Marler, 1984, for the case of rhesus monkey screams). Furthermore, while some acoustic variations in animal sounds may sound continuous to the human ear, this is not necessarily so for the auditory system of the species concerned because of the major differences in the structures involved, the fineness of resolution, and the patterns of auditory processing (Beer, 1975; Marler, 1977; Snowdon, 1982). However, it seems highly probable that some degree of gradedness exists both within and between classes of calls. Because of the existence and complexity of graded repertoires in the vocal communication systems of many species and the adaptive value of communicating precise information about emotion-antecedent conditions and affective response, it is important to identify the nature of the acoustic cues that serve as indicators of specific aspects of affective meaning. It is particularly interesting to speculate about cross-species universality and phylogenetic continuity of such vocal indicators. Given that physiological factors determining the nature of phonation and resonance under emotional arousal might be similarly structured in many species (cf. the Darwin quote, “the muscles of the body are generally thrown into violent action”), this may not be too wild a speculation. So far, there have been two major attempts to examine this notion with the help of empirical data on the acoustic structure of affect sounds in different species of animals-by Ternbrock ( I 971, 1975) and by Morton ( I 977). Tembrock, adopting a systems theory approach to animal vocal expression, assumes that the system state of the animal (consisting of organismic variables as well as relevant environmental context variables including social status) affects three major dimensions of phonation: intensity, frequency, and temporal patterning. He proposes the following classification of calls in relation to system states.

I . Contact range (permanent communication): contact calls, comfort calls, play calls, threat calls, defense calls, distress calls, dominance calls, submission calls. 2. Transition range: distance defense calls, territorial calls. 3. Distance range (temporary communication): distance reduction calls (attraction), alarm calls. On the basis of spectrographic analyses of a number of these types of calls for many different species (based on his own work and published accounts), Tembrock concludes that there seem to be definite relationships between particular

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aspects of system states and phonation characteristics resulting in certain acoustic features across different species. He lists the following observations (1975, p. 66-68, translated by KRS): I . In the contact range, for calls reflecting states of relaxation and contentment, such as comfort and play calls, one tends to find repeated short sounds with relatively low frequencies. 2 . Low frequencies also characterize dominance calls in agonistic encounters and threat calls (i.e., when critical distances are violated). 3. Defense calls, which may be the result of a transition from threat calls, are short, with a high amplitude onset and a broad frequency spectrum. 4. Submission calls, which may be the result of graded transitions from threat or defense calls, are characterized by high frequencies, repeated frequency shifts, and a tendency toward temporal prolongation. 5 . Attraction calls in the distance range are also characterized by high frequencies and temporal prolongation. In trying to identify some of the physiological processes that might underlie these relationships, Tembrock speculates that calls in the contact range (particularly comfort calls) are produced by parasympathetic reactions, whereas agonistic calls are likely to be produced by sympathetic reactions. Voice register changes are assumed to produce acoustic differences between dominance and submission calls. Although some of these suggestions are highly speculative and based on insufficient empirical data and although Tembrock’s classification of animal calls might not find general consensus, he does suggest a number of fruitful hypotheses that could be subjected to empirical test. A similar attempt by Morton (1977) to identify similarities in the relationship between emotional states and acoustic features of vocalization across different species starts with an observation by Collias ( 1960) on the structural convergence of many animal sounds in “hostile” and “friendly” contexts. Arguing that selection would favor the development of vocal signals that are quick and reliable indicators of an individual’s motivational state, Morton proposes a “motivationstructural rule” concept to formalize the relationship between affective state and acoustic structure. In its simplest form, the concept is expressed as follows: “birds and mammals use harsh, relatively low-frequency sounds when hostile and higher-frequency, more pure tonelike sounds when frightened, appeasing, or approaching in a friendly manner” (Morton, 1977, p. 855). As an explanation for the hostility-harshness rule, Morton proposes the wellknown relationship between body size and low frequency of phonation (which tends to result in harshness at high intensity levels; see below). He argues for selective genetic development in favor of low-frequency , harsh vocalization because of the advantages of giving the impression of a large body size in agonistic encounters. Conversely, the high-frequency, tonelike structure in fearful or friendly motivational states is assumed to be based on the structural

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similarity to infant vocalizations and their tendency to attract rather than repel adults and to solicit support. Morton is able to marshall impressive evidence for this hypothesis by reviewing a large number of studies on bird and mammal sounds. Based on the examples in the literature, Morton hypothesizes that the motivation-structure rule operates on a continuum: the lower the frequency and the harsher the sound, the more hostility and aggressiveness; the higher the frequency and the more tonelike, the more fear or friendliness. In addition, frequency changes seem to be affected by this rule: rising frequency indicates lower hostility and increasing appeasement or fear; falling frequency indicates increasing hostility. A sound with equally falling and rising frequencies and a constant midrange seems to reflect approach-avoidance conflicts. In graded call systems, many blends of the acoustic characteristics associated with these two motivational continua are possible. Both Tembrock and Morton base their conclusions, at least in part, on published studies of vocalization patterns in different animal species. In many cases, the respective authors had to infer the underlying motivational or emotional state of the vocalizers from overt behavior and context. Tembrock and Morton had the difficult tasks of interpreting the written description of these states and trying to assimilate them into their respective category systems. In addition, at least in some cases, the acoustic characteristics of the sounds had to be inferred from natural language transcriptions or labels (e.g., growl, bark, harsh rasp) or onomatopoetic renditions (e.g., zwrack, rahh-rahh, cheh cheh cheh). In view of these methodological difficulties, well-controlled empirical studies with clearly operational measures of emotional state and objective measurement of acoustic cues are called for. Although such studies may be very difficult to conduct in the field, they may be feasible in the laboratory. In an excellent study on the calls of the squirrel monkey Saimiri sciureus, Jurgens (1979) was able to use a very powerful manipulation of emotional state. When he used electrical brain stimulation (25 1 intracranial electrode positions in 38 monkeys) and gave the monkeys the opportunity to switch stimulation on and off, he was able to detect a variety of emotional states, the “aversiveness” of which could be established by the amount of time the animals tolerated stimulation. In this manner, a total of 47 call types could be investigated, with the underlying states varying from highly aversive to highly rewarding or pleasurable. These call types were analyzed with the help of spectrographic methods and grouped into the following five groups (with the author’s suggestions on labeling the associated states, based on observation of the situations in which the calls occurred in parentheses): I . Purring-growling-spitting rhythmic sounds

(self-assertiveness): Nonharmonic, clicklike,

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2 . Groaning-cawing-shrieking (protest): Nonrhythmic, harmonic, or noise-

like sounds 3 . Chucking-yapping-alarm peep (worrying, warning): Short, loud sounds with a steep fall of energy from high to low frequencies 4. Chirping-peeping-squealing (socicrl unease, lack of corzfidence): Non-

rhythmic sounds with high fundamental frequency, little frequency modulation, at times short ascending frequency course (to draw attention) 5. Twittering-chattering-cackling (plemure, confirming social bonds): Rhythmic sounds with different shapes of frequency contours Since within each of these classes there are calls reflecting more or less “aversiveness,” it was possible to investigate the covariation between particular acoustic cues and an aversiveness continuum. Jurgens reports that the aversiveness of a call is positively correlated with its total frequency range as well as with (in high-pitched harmonic calls) higher fundamental frequency and irregularity of frequency contours. Because these acoustic patterns correspond well with the acoustic characteristics of calls of other primates in similar situations, as reported in the literature, Jurgens feels justified in assuming that the relationship between acoustic structure and functional significance of calls found in his study is valid for a number of primate species and that these results show a trend similar to the rules postulated by Morton (Jurgens, 1982, p. 61). However, the correspondence between the relationships reported by Tembrock, Morton, and Jurgens are less impressive than they might seem at first sight. The problems are manifold. One serious hindrance for exact comparison is the insufficiently precise specification of the acoustic parameters. Is “harsh” equivalent to “broad frequency spectrum”? If so, hostility should be an aversive state, like fear. Jurgens finds similar acoustic cues for several different highaversiveness states, both offensive and defensive, whereas Morton hypothesizes harshness only for hostile, aggressive states and the opposite for fear. Tembrock finds a broad frequency spectrum for “defense calls’’ which could be both hostile or fearful in nature. Since neither Tembrock nor Jurgens uses the term harshness. it is difficult to decide this issue. A detailed comparison is also hampered by the fairly imprecise specification of the emotional states associated with specific call types. None of these three authors can be held accountable since agreed-upon conceptual and operational description systems exist neither for characteristics of emotional states nor for acoustic features of complex vocalizations. Further discussion of this basic problem will be deferred until the empirical evidence for human vocal expression of emotion has been presented. STUDIES ON THE VOCAL EXPRESSION OF EMOTION IN HUMANS Since extensive review chapters on the relevant literature can be found elsewhere (Scherer, 1979a, 1981a,b), only a brief outline of the state of knowledge

B.

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KLAUS R. SCHERER

TABLE I S U M M A R Y OF

Emotion Happiness/joy Confidence Anger Fear Indifference Contempt Boredom Griefisadness Evaluation Activation Potency

RESULTSO N

V O C A L INDICATORS OF E M O T I O N A L STATES"

Pitch level

Pitch range

High High High High Low Low Low Low

> Wide Wide Narrow Wide Narrow Narrow

?

?

?

High

Wide ?

?

'?

Pitch variability

Loudness

Tempo

Large ? Large Large Small

Loud Loud Loud

,?

Loud Soft Soft Loud Loud Loud

Fast Fast Fast Fasc Fast Slow Slow Slow

?

Small

'?

?

?

?

Fast

"From Scherer (1981b, p. 206).

in this area will be presented in this article. Table I is a summary of the major findings on the vocal expression of human emotions, both in terms of common emotion labels and the major dimensions of feeling that many psychologists find useful to describe affective states. It contains specifications of the nature of particular cues for an emotion only in those cases which seem at least partly corroborated by results from independent, empirical studies (see source for references). Therefore, there are still question marks in some cells. However, even if these were replaced by pertinent information, the acoustic cues listed would still not be sufficiently specific to clearly differentiate the different emotional states. The entries in the table show a pronounced differentiation between cues for high activity emotions (joy, anger, and fear) characterized by high frequency and intensity and fast tempo on the one hand and cues for low activity emotions (sadness, boredom) characterized by low frequency and intensity and slow tempo on the other hand (Scherer, 1981b, p. 205). Consequently one might conclude that vocal cues carry only information about physiological arousal rather than about discrete emotional states. This seems highly unlikely, however, for a review of the literature on emotion recognition from vocal cues (Scherer, 1981 b, pp. 207-214) has shown that judges can accurately identify several discrete emotions from voice and speech samples (an average recognition rate of 56% accuracy-compared with 12% expected by chance-in 28 studies). One obvious conclusion is that the acoustic cues listed in Table I may provide information about physiological activation whereas other cues which have not been studied extensively enough to warrant inclusion in this table of established empirical findings serve to differentiate the various discrete emotions (see Scherer, 1984~).There is some evidence that this may be the case. In one of the first

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extensive studies on acoustic indicators of emotion to use sophisticated spectrographic analysis, Williams and Stevens (1972) reported a number of characteristics that seemed to be different for the emotions under study, such as irregularity of phonation, fundamental frequency contours, and energy distribution in the spectrum. For example, they reported that in the higher frequency region (above 1 kHz), relative to the lower region, there was more energy for anger and fear than for sadness, even though this criterion did not allow a definite differentiation between the two emotions. Energy in the upper frequency region of the spectrum has also been shown to increase under stress and tension (cf. Scherer, 1982a, p. 167). These findings are of special interest since they seem to correspond to some of the results on harshness andlor broad frequency range in the animal literature. There is also some corroborating evidence from human judgment studies. In a series of studies using synthesized sound stimuli (Scherer, 1974; Scherer & Oshinsky, 1977), the judgment of anger correlated highly with the presence of higher harmonics in the spectrum (i.e., a broader frequency spectrum). These results, originally found for American judges, were replicated with German judges (Scherer, 1984c), indicating that the effect may be independent of the language of the judges and may reflect a universal tendency. Similarly, in a recent study using speaker simulation of voice quality along with digital resynthesis, a harsh voice quality was judged to be less friendly and more aggressive than the speakers’ normal voice (unpublished data, see Scherer, 1984~). Thus, there is a strong possibility that specific acoustic characteristics do exist for different emotional states. However, our current state of knowledge is not yet sufficiently advanced to allow their definite identification. Given this state of affairs, it might be premature to advocate a comparative approach to the study of vocal communication of emotion. However, as this review of the literature on animal and human vocal expression has shown, there are some promising leads. For example, high frequencies seem to characterize aversive states with high levels of activation, and a broad frequency spectrum has been found to accompany states of anger and hostility across many of the species studied, including man. Yet, the pattern is not consistent and here are some glaring contradictions. Why is human joy expressed in high fundamental frequency when generally, in many animal species, it seems to indicate highly aversive arousal‘? Is a broad frequency spectrum with appreciable energy in the higher region a feature specific to anger and hostility, or can it also be found in fear? As mentioned earlier, the discussion of these issues is hampered by the lack of a conceptual scheme which allows an unambiguous comparison between the emotional states and the acoustic patterns reported in different studies on different species. Before venturing to propose some hypotheses on the possible phylogenetic continuity and cross-species generality in the vocal expression of emotion, a conceptual scheme for the definition and description of the organism’s

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affective state will be developed. This scheme is based on a new functionally oriented process model of emotion (Scherer, 1981c, 1982c, 1984a) which will be outlined in the next two sections. In this discussion no attempt will be made to review or reference all relevant work in the area of the psychology of emotion (for overviews see Plutchik & Kellerman, 1980; Ekman & Scherer, 1984).

111.

A PSYCHOBIOLOGICAL APPROACH T o EMOTION

OF EMOTION A. THE NATUREAND FUNCTION

Emotion serves as an interface between the organism and its environment, mediating between constantly changing situations and events and the individual’s behavioral responses. In this respect, emotion to a large extent superseded rigid reflex chains or innate releasing mechanisms in the course of the evolutionary history of many higher organisms, particularly the mammals. The major selective advantage of this development is the freeing of behavioral responses from direct stimulus control, resulting in a dramatic increase in the flexibility and variability of behavioral reactions. In organisms capable of emotion, simple feature detection and innate releasing mechanisms are at least partly replaced by “cognitive” evaluation processes for stimuli and events. Reflex-like fixed action patterns are succeeded by a combination of physiological activation, preparing the energy resources for appropriate action, and a set of alternative behavioral plans or intentions with a high probability of occurrence but a certain latency. For example, if an organism gets “angry” because it is frustrated by a conspecific, an aggressive response will be very high in the response hierarchy and will be prepared in terms of the physiological arousal and appropriate behavior tendencies (before an action is actually executed). However, the latency time provided by the emotion mechanism allows both a reevaluation of the eliciting antecedent event (maybe the frustration was only imagined) and an evaluation of the likely consequences of the behavioral response alternatives. Thus, the organism may choose flight rather than fight if the frustrator is clearly superior in strength. The advantages of the emotion of anger as a mediating mechanism between frustration and aggression were pointed out early by Berkowitz ( 1962). The more complex the physical and social environment in which an organism finds itself, the more it depends on complicated evaluations of antecedent events and probable consequences of behavioral responses. Reflexes or fixed action patterns are unlikely to provide the flexibility and complexity of the response patterns required to deal with the multitude of events impinging upon the organism, particularly in socially organized species. This view of the evolutionary

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origin of emotion is based in part on Hebb’s (1949) early observation that the degree of emotionality of a species seems to be directly correlated with the complexity of its evolutionary adaptation. So far, three different but interconnected functions of emotion have been mentioned implicitly: ( I ) the evaluation of stimuli and events in terms of the organism’s needs and preferences; (2) the adjustment and regulation of the “internal milieu” of the organism; and (3) the preparation of appropriate responses to environmental stimulation. In socially living organisms, there is a fourth function of emotion which greatly facilitates social interaction and social organization within groups: the communication of reactions and intended responses via motor expression. Again, Darwin was one of the first to point out that there seems to have been selective pressure toward the development of means of affect expression through ritualization of functional behavior patterns, as for example in “intention movements.” It is interesting to juxtapose these functions to the components of emotion as postulated in many recent theories of emotion (e.g., Izard, 1977; Lazarus, Averill, & Opton, 1970; Leventhal, 1979; Plutchik, 1980; Scherer, 1981c, 1982~). This is shown in Table 11. There is a remarkable correspondence between functions and components, and one is tempted to conclude that each of the components of emotion is indeed specialized to serve one of the major functions. It seems reasonable to argue that the first four functions have high adaptive significance, leading one to expect to find the respective components in many species of animals. This may not be the case for the last line in the table, representing the subjective feeling component, which is an important part of emotion only in humans, although a case has been made for a similar capacity in animal species (Griffin, 1976). In any case, although the selective advantage of the other four functions is easy to demonstrate, it is not immediately obvious what the survival value of subjective feeling state might be. Following this line of functional reasoning, the present author has proposed a TABLE I1 RtLATIONSHIPS B U T W k t N ORGANISMIC SUBSYSTEMS A N D A N D COMPONENTS OF EMOII O N Function Evaluation of stimulation System regulation Preparation and direction of action Communication of reaction and intent Reflection and monitoring

1H E

FUNCTIONS

Subsystem

Component

Information processing support Executive Action Monitor

Cognitive Neuroph ysiological Motivational Expressive Subjective feeling

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KLAUS R . SCWERER

component process model of emotion (Scherer, 1983a, 1984a). This model proceeds from the assumption that emotion needs to be conceptualized as a process of adaptation consisting of patterns of state changes in five major functional subsystems of an organism. These subsystems correspond to the functions and components of emotion presented in Table 11. The evaluation function is served by an information processing subsystem, with the system states characterized by perception, memory, prediction, or evaluation of situations, relationships, facts, events, or actions. Internal regulation is the task of the support subsystem which controls neuroendocrine, somatic, and autonomic states. The executive subsystem is responsible for planning, decision making, and the preparation of action, as well as arbitration between conflicting motives or plans. The action subsystem regulates neuromuscular states and processes and is thus responsible for motor expression and overt behavior. A monitoring subsystem, finally, is conceptualized as a control system determining the deployment of attention and reflecting the current states of all other subsystems. At least in humans, some elements of these representations constitute awareness or consciousness. A detailed description of these subsystems and their interrelationships requires a comprehensive psychobiological theory of behavior, a task which cannot be reasonably attempted at the present state of our knowledge. The subsystems are postulated to help order the different states or components of an organism’s response to external or internal stimulation. The component process model defines emotion as a sequence of interrelated changes in the states of the functional subsystems (for a more detailed account of the model see Scherer, 1984a). How does this model account for the occurrence of a number of differentiated, discrete emotions, such as anger, joy, fear, disgust? Most emotion theorists have, more or less explicitly, assumed that differentiated emotional experiences result from the outcome of an organism’s appraisal or evaluation of a stimulus or event in terms of its significance for survival and well-being (Arnold, 1960; Lazarus, 1968). Specifically, Scherer (1981c, 1982c, 1984a) has suggested a sequence theory of emotional differentiation which postulates that each organisms’s information processing subsystem continuously scans external and internal stimulus input and performs a series of stimulus evaluation checks (SECs). The theory specifies the five SECs listed in Table 111, which are expected to always occur in the same sequential order. A specific emotional state is the end result of the respective outcomes of these checks. For example, fear may result from evaluating an event as novel, unpleasant, hindering goal achievement, and requiring flight. On the other hand, if the outcome of the coping potential check indicates that one’s power is sufficient to fight an obstacle, the reaction to the very same event might be anger. A more detailed description of the sequence theory of emotional differentiation and the different SECs can be found elsewhere (Scherer, 1984a,b).

20 1

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TABLE 111 StiQLIIIN('E

O F S'I'IMUL-IJS EVA1.IJATION Cti1:CKS

(SECS)

Novelty check Determines whether thcre is a change in the pattern of external or internal stimulation. particularly whether a novcl event occurred or is to be expected Intrinsic pleasantness check Determines whether a stimulus event is pleasant, inducing approach tendencies, or unpleasant, inducing avoidance tendencies: hased on innate feature detectors or on learned associations Coallnced significance check Determines whether a stimulus event is relevant to important goals or needs of the organism (rclcvance subcheck), whether the outcome is consistent with or discrepant from the state expcctcd for this point in the goal!plan sequence (expectation subcheck), and whether it is conducive or obstructive to reaching the respective goals or satisfying the relevant needs (conduciveness subcheck) Coping potential check Determines the causation of a stiniulus event (causation subcheck) and thc coping potential available to the organism, particularly the degree of control over the event or its conscquences (control subcheck). the relative power of the organism to change or avoid the outcome through fight or flight (power subcheck), and the potential for ad.justinent to the final outcoinc via internal restructuring (adjustment subcheck) Norniiself compatibility check Determines whether the event, particularly an action, conforms to social norms. cultural conventions, or expectations of significant others (external standards subcheck), and whether it is consistent with internalized nornis or standards as part of the self-concept or ideal self (internal standards subcheck)

B.

FACETDESCRIPTION OF EMOTIONAL STATES

The component process model of emotion and the sequence theory of emotional differentiation have been discussed to justify the new descriptive system for emotional states presented in this section. As pointed out at the beginning of this article a comparative analysis of vocal indicators of emotional states is difficult if not impossible unless these states can be clearly specified by using a conceptual system that is equally applicable to animals and humans. Scherer (1983a,b, 1984a) has suggested a scheme for the systematic description of the respective states of the organism's subsystems during affective processes (the components of affective states), a scheme based on facet theory notions (Borg, 1981; Guttman, 1957). This,fucet code of emotional stute components differentiates emotional states by coding or specifying facets or characteristics for relevant antecedent and consequent states of the organismic subsystems as well as the outcomes of subsystem processes, such as the SEC outcomes in the information processing subsystem. Table IV shows an attempt, using a highly abbreviated subset of facets, to

TABLE IV PREDICTED ANTECEDENT SEC OUTCOMES FOR SOMEMAJOREMOTIONS“ Stimulus evaluation checks

Facets

Fear

Anger

Disgust

Sadness

Open

Open

Open

Open

Unpleasant

Relevant

Relevant

Vely unpleasant Irrelevant

Open Unjust Self Egoistic or malevolent Low Low Low

Irrelevant Irrelevant Open Open

Obstructive Irrelevant Open Open

Low High Low

Conducive Just Open Benevolent or chance Low High High

Low Low Low

Low Low Irrelevant

Open

High

Highly inconsistent

Irrelevant

Irrelevant

Expectation

Unexpected

Openb

Intrinsic pleasantness Goalheed conduciveness

Pleasantness

Open

Open

Relevance

Highly relevant

Conduciveness Justiceiequity Agent Motiveicause Control Power Norm compatibility

Obstructive Open Other Malevolent or chance Low Low Open

Highly relevant Obstructive Unjust Open Open

Self compatibility

Open

Normiself compatibility

Shame

Slightly unexpected Pleasant

Novelty

Coping potential

JOY

“From Scherer (1984a). It should be noted that these predictions are preliminary and are subject to change with revisions of the model. ““Open” indicates that several different outcomes for an SEC are compatible with the ensuing emotion.

Relevant

VOCAL AFFECT SIGNALING

203

indicate how a number of emotions characterized by different natural language labels might be categorized by the facet code. Trying to do this systematically nicely illustrates the problem of using natural language categories for scientific description. Language labels represent folk taxonomies. These folk concepts carve out of the vast complexity of structures and processes surrounding man those structural or temporal patterns and relationships that (phenomenologically) seem most relevant for human interaction. These patterns or relationships are labeled, they are the ones that need to be talked about. As is to be expected, this is a highly subjective way of categorizing the world, one that is rarely compatible with the standards of systematic scientific description. The affect and emotion terms in our language are a motley assortment of labels which tend to emphasize very different aspects or components of the emotion process. Some terms describe outcomes of the evaluation of antecedent conditions (surprised, disgusted), sometimes with special emphasis on prior expectations (discontent). Some specialize in describing reactions of subsystems, for example, physiological arousal (aroused, tired) without any consideration of different types of antecedents. Others have their main focus on motivational antecedents (interested, longing) or consequences (dejected, hopeless) of affective processes. Still others refer mainly to the type of behavior that is likely to follow the emotion (aggressive, sleepy). Then there are a number of terms that specify the object or content area with which the emotion is concerned (horny, amused, jealous). Given the importance of social relationships and social interaction in human life, it is not surprising that there are many labels that focus specifically on the affective nature of relationships (love, hate). A serious problem with natural language emotion labels is that many near-synonyms may imply somewhat different referents in terms of some of the features listed above. This renders the comparison of scientific descriptions of emotional states using different natural language terms exceedingly difficult. These problems are aggravated when such terms are used to describe animal states, and this is obviously the reason many biologists and ethologists have been hesitant to use the term emorioii in connection with animal behavior. Many of the natural language emotion terms, in addition to the multiple semantic dimensions involved, seem to emphasize conscious subjective feeling states. Understandably, the connotations that surround these terms make one hesitate to use them to describe animal states, quite apart from the anthropomorphic inferences that are necessary precursors to the imputation of any such term. The use of the facet code proposed here to characterize emotional states may help to solve some of these problems. It also requires inferences about nonobservable processes in the organism, but these are more limited and usually more clearly tied to context factors or behavioral evidence. It is hoped that it will be possible to work out more detailed suggestions on how to assess the momentary state of various organismic subsystems and to devise more objective measure-

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ment procedures, as our knowledge about the structure of the organism and the biological and psychological processes increases. Even at the present time, a specification of emotional states in terms of this facet code, even though the coding may still be imprecise, would seem to be preferable to the use of illdefined natural language terms, particularly in comparative work. For many applications, it may also be preferable to brain stimulation. The activation of pleasure and aversiveness centers in the brain represents only a net outcome of many different-often conflicting-evaluation processes, which are of great theoretical interest for the study of emotion. Often, one cannot predict on the basis of brain stimulation which kind of behavioral response (other than attempts at termination of stimulation) will result. AND ONTOGENETIC CONTINUITY OF C. THEPHYLOCENETIC EMOTION

Biologists might object that the component process model and particularly the sequence theory of emotional differentiation are still too closely modeled on the human organism and its capacities, particularly in terms of cognitive information processing. To some extent this is so by necessity. A model designed to serve as a basis for comparative analysis has to contain all of the elements and component processes found in the most complex case to be compared with other cases. Thus, it is most likely that many of the structures and processes described will only be found in man. Others may exist in the higher mammals, particularly in primates, but in a much more rudimentary form. Scherer (1984a) has suggested that the sequence theory should help to predict which types of emotional states can be expected to occur in a particular species if the information processing capacity can be clearly specified in relation to the SEC requirements. There should be phylogenetic development in the direction of increasing capacity for “cognitive” processing (complex evaluation of environmental contingencies) with an ensuing differentiation of emotional states (and a consequent increase in the flexibility and variability of behavioral response), as predicted by Hebb (1949). It is likely that there is not only a “vertical” growth in complexity (i.e., the more complex SECs emerging in the course of evolution) but also a “horizontal” increase in complexity, with the evaluation mechanisms in each of the SEC classes becoming more refined. For example, whereas some animals may conduct a very rudimentary goal conduciveness check, (probably based on innate feature recognition, e.g., concerning the extent to which a stimulus or event endangers their survival or their attainment of an essential goal), the same check in man may be based on a very complex problem-solving activity and may involve many more dimensions of evaluation, possibly also involving innate feature recognition. Of particular interest is the possibility that the ontogenetic development of

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emotional differentiation reflects the phylogenetic patterns of development of the capacity for emotion. One can argue that the order of appearance of different emotional states should be the same in both of these domains and should be linked to the development of increasingly complex cognitive information processing ability. A number of theoretical accounts in developmental psychology (Emde, 1984; Piaget, 1981; Sroufe, 1979) seem to support this notion. Unfortunately, it will be very difficult to obtain empirical evidence to support this suggestion. One of the major problems is the criterion for the existence of a particular emotional state. In terms of the component process model, there is no one component that is seen as a necessary or sufficient precondition for an emotional state. However, there are frequently recurring patterns of component state configurations that have led discrete emotion theorists to postulate the existence of a small number of innate emotions, and the motor expressive component has frequently been used as the identifying criterion. It would be useful to determine the characteristic elements of particular emotion displays (facial, vocal, or postural) which tend to be associated with a particular syndrome of emotion components in its most complex form in adult humans and to develop a procedure to discriminate reliably between them and clearly “nonemotional” displays. This pattern could then be used as a criterion to assess the appearance of particular emotional states in phylogenetic and ontogenetic development. A highly speculative attempt in this direction is shown in Table V , which relates the first appearance of facial expressions of particular TABLE V ONlOCtiNETIC DEVELOPMENT O k EMOTION“

STIMLII.IJS EVALUATION PREREQUISITES FOR THE

Stimulus evaluation checks required” Emotional expression Startle Displeasure surprise JOY

Anger Fear Sharne/guilt Contempt

Age of onset (in months) Novelty 0 0 1-3 3-5 4-6 5-9

12-15 15-18

.. . .

Intrinsic pleasantness

Goallplan relevance

Coping potential

Normlself-concept compatibility

X

X X

. .

X

X

X

X

X

.

X X

OFroni Scherer ( 1 9 8 2 ~ p. . 561). “ X indicates that the respective SEC is a necessary prerequisite for the occurrence of a particular emotion (albeit not necessarily sufficient); indicates that the SEC is available but may not be centrally involved in determining which emotion will occur as a result of the stimulus evaluation sequence.

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KLAUS R . SCHERER

emotions in infants (based on reports in the literature) to the SECs that are hypothesized to differentiate the emotional states labeled by the respective language terms (see Scherer, 1982c, for a more detailed discussion). One would conceivably attempt a similar analysis for species differing in their position in the evolutionary branching. It is hoped that this section has shown the way in which a psychobiological attempt to define and describe emotional states renders a systematic comparative approach to the study of affective expression possible. For each of the species compared, rough estimates of equivalence in terms of the outcomes of the successive SECs, allowing for differences in horizontal and vertical complexity (see above), should be possible. When the comparability of the underlying affect states is ensured, it becomes possible to test the notion that at least some affective expressions (in this case limited to the vocal channel) are phylogenetically continuous.

IV.

EMOTIONAL DETERMINANTS OF VOCALIZATION

In the remainder of this article an attempt will be made to use the conceptual schema outlined in Section II1,C to develop some systematic hypotheses concerning the nature of the effects of emotional states on animal and human vocalization. This attempt is based both on the patterns of empirical findings reported in the first section and on theoretical considerations concerning the interrelationships of the components of emotion processes and their effects on voice production. This discussion will be prefaced by outlining the major acoustic characteristics of vocalization and the most important determinants of the phonatory and articulatory processes that produce them. A.

TYPESAND MODALITIES OF VOCALIZATIONS

For many species with vocal communication systems, the repertoire contains discrete classes of sounds with specific configurations of acoustic characteristics. However, even with classes of calls, individual acoustic parameters can vary within certain limits. Given this variability and gradedness of the acoustic features that constitute and differentiate discrete classes, one often finds transitions from one class to the other (see later discussion of gradedness). A nice illustration of this phenomenon is the vocalization system of the squirrel monkey shown in Fig. 1 (from Jurgens, 1982). The concentric circles represent different degrees of arousal or aversiveness (as measured by avoidance response in electrical brain stimulation). Call types are identified by roman numerals and one token for each level of aversiveness is shown. The type of organization of a communication system exemplified in this figure suggests a dual code: On the one hand, infor-

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FIG. I , Vocalization system of the squirrel monkey. For reasons of simplicity, only one call type per class and self-stirnulation category is shown. (- -), highly aversive calls (self-stimulation, (20%); (-), slightly aversive calls (self-stirnulation, 20-40%); (k), neutral calls (self-stimulation, 40-60%); (+). pleasure calls (self-stimulation, >60%). The names of the 16 vocalizations shown are, beginning with the innermost circle, I, spitting, growling, purring; 11, shriek-cackling, cackling, chattering, twittering; 111, squealing. isolation peep, chirping; IV, alarm peep, yapping, clucking; V, shrieking, cawing, groaning. From Jurgens (1982, p. 55).

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mation or meaning of a discrete, discontinuous kind is encoded by the structural relationships of the different acoustic features and the referents of the discrete classes of vocalizations. On the other hand, the individual acoustic parameters which constitute the call-specific structural configurations can change continuously within certain limits. This makes analog coding of continuous underlying dimensions such as arousal or aversiveness possible. A more detailed discussion of the interesting issues of the design features of communication systems and the different types of codes, such as discrete versus continuous, iconic versus arbitrary, or probabilistic versus deterministic is beyond the scope of this article (see Giles, Scherer, & Taylor, 1979; Hockett, 1960). It may be noted in passing that many of the issues relevant to coding have interesting implications for theories on the origin of language and the issue of referentiality in animal communication (see Green & Marler, 1979). In the following discussion of the emotional determinants of vocalization, a distinction between the class or type of vocalizations and the modality of production of that type, reflecting the specific values of the variable parameters for this token, will be made. Thus, as discussed earlier, in many animal communication systems there are a limited number of particular classes of calls, the types, which seem to have distinct emotional/motivational or, in some cases, object-referential (e.g., type of predators) meaning. In human vocal communication, language has developed as a second, more powerful system of communication which often dominates but has not entirely replaced the older nonverbal system of affect vocalization which is probably phylogenetically continuous (see Scherer, 1979a; and below; but see also Goerttler, 1972, for a description of some discontinuities dnd unique features of the human voice). The types in this nonverbal vocal system, sometimes called “interjections” by linguists, consist of the “uhs,” “ahs,” and “ohs” that humans tend to produce under strong emotional arousal (or, interestingly enough to assure their interaction partners that an emotion is truly felt). Scherer (1977), based on early suggestions by Wundt (1900), proposes a distinction between spontaneous affect vocalizations which are likely to be universal across languages and vocal emblems, stereotyped and ritualized vocalizations that have been integrated-phonologically and often lexicallyinto a language system (often without affective meaning). These types of vocalizations can be produced by many different patterns of interacting respiratory, phonatory, and resonatory settings in both animals and humans. The resulting acoustic waveforms differ in features which vary in the intensity, frequency, and time domains. As suggested above, variations in these features which do not change the type of vocalization will be called modality of production of a token, for example, variations in the energy distribution in the spectrum and in the height of fundamental frequency (FO). A more detailed nontechnical introduction to the processes of voice production and the major

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acoustic parameters as well as their measurement (including references to the more technical literature) can be found in Scherer ( 1982a).

B.

INTERNAL PUSH AND

EXTERNAL PULLEFFECTS

Which factors are likely to determine the occurrence of particular types of vocalization and the nature of their production, the modality? Scherer and his associates have distinguished internal push and external pull factors in trying to identify the determinants of paralinguistic behavior (Scherer, Helfrich, & Scherer, 1980, p. 279): “Are paralinguistic features such as tempo and rhythm of speech and pitch and quality of voice determined by an internal, intrapersonal ‘push’ exerted by personality traits and dispositions as well as affective states or by the external ‘pull’ of social norms and expectations concerning the appropriateness of particular speech patterns and the need for adequate self-presentation?” In terms of the component process model, these push factors are defined as those changes in the states of the internal support and action subsystems which affect the production of vocalization in an essentially nondirective manner. For example, increased muscle tension produced by ergotropic arousal can affect breathing patterns, the shape of the vocal tract, and facial expression. In addition, the behavior resulting from a particular emotional state, such as threat postures and rapid movement, for example, will also affect vocalization (Zahavi, 1982). These effects are exemplified by Darwin’s notion of “muscles thrown into violent action.” In other words, internal factors “push” voice production in various ways and without a predetermined direction or set point in terms of acoustic targets; the acoustical outcome, which results from the interaction of the different forces applied, is free to vary, whereas the factors that produce it are determined. For example, if an object is pushed down a hillside, the “pusher” usually does not intend to determine or predict the exact location of the final resting point, yet the laws of physics determine the course of the object. External pull factors, on the other hand, are defined as norms or expectations imposed by the external physical or social environment which require the production of specific acoustic features in terms of a set point or target. The sender needs to produce this acoustic pattern to achieve a particular effect, particularly in those cases where vocal communication serves adaptive purposes. In this case, the acoustic outcome or target is fixed, and the processes by which it is brought about are variable. In terms of the example used carlier, if an object is pulled up a hillside, the “puller” usually has very definite intentions concerning the final resting point of the object and will attempt to overcome all those physical forces obstructing the desired course. One such pull factor which is obviously important for socially living species in

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which members of a group might be dispersed over an area concerns the distance transmission characteristics of a sound structure and the locatability of a sender. In this case the physical environment imposes certain acoustic targets. Darwin wrote, “A scream, for instance, uttered by a young animal, or by one of the members of a community, as a call for assistance, will naturally be loud, prolonged, and high, so as to penetrate a distance” (1872/ 1965, pp. 90-91). Many recent surveys of animal communication emphasize the importance of these transmission and localization issues and the selective pressure that they are likely to exert on the acoustic structure of vocalization (Brown, 1982; Green & Marler, 1979; Tembrock, 1975). A second pull factor consists of self-presentation: the kind of impression the sender “wants” to create in the receiver. This might be a form of “vocal mimicry,” if one can assume that particular acoustic features serve as innate releasing mechanisms or always lead to particular inferences or attribution. Again, Darwin supplied an example: “When male animals utter sounds in order to please the females, they would naturally employ those which are sweet to the ears of the species; and it appears that the same sounds are often pleasing to widely different animals, owing to the similarity of their nervous systems. . . . On the other hand, sounds produced in order to strike terror into an enemy, would naturally be harsh and displeasing” (1872/ 1965, p. 91). Morton (1977, see earlier discussion) also seems to specify the mechanism for the harshness-hostility relationship in terms of a pull factor (i.e., trying to give the impression of a big, powerful body by low-frequency harsh vocalization). These examples show rather well to what extent pull factors are based on underlying push effects because big vocalizers naturally phonate at a lower fundamental frequency and small vocalizers at a higher fundamental frequency. The infant-helplessness impression created by the high-pitched harmonic sounds in fear, submission, and friendliness works according to the same principle, although in an opposite direction, that is, making the vocalizer appear smaller. In human communication, self-presentation may be a rather powerful determinant of voice quality and speech style (see Scherer, 1979b). In both animals and humans there seem to be self-presentation tendencies in terms of identity, ability, power, and intention, all of which are likely to affect vocal expression by amplifying or deamplifying the signals likely to result from push effects. Darwin suggested another possible mechanism that might be operative in selfpresentation-the “principle of antithesis”: “The interrupted, laughing or tittering sounds made by man and by various kinds of monkeys when pleased, are as different as possible from the prolonged screams of these animals when distressed” (1872/1965, p. 91). The following quote shows that Darwin thought of this principle in terms of a pull factor: “As the power of intercommunication is certainly of high service to many animals, there is no a priori improbability in the supposition, that gestures manifestly of an opposite nature to those by which

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21 I

certain feelings are already expressed, should at first have been voluntarily employed under the influence of an opposite state of feeling” (1872/1965, p. 61). Although this principle has not found much acceptance in the literature, it would appear to be a reasonable explanation for some situations in which selfpresentation pull factors seem to be the major determinants of expression. For example, in trying to control an affect expression they do not want to openly display (because of strategic intentions, shame, social display rules, or other reasons), many individuals do seem indeed prone to strive for an expression of an affect state exactly opposite to the one they are actually in. However, for some phenomena it may be possible to find other, more functional and/or parsimonious explanations than the principle of antithesis. For example, as shown in the quote above, Darwin uses the principle of antithesis to explain the acoustic features of pleasure sounds. In turn, he tried to explain the facial features found in smiling and laughter (“corners of the mouth retracted and upper lip raised”) as necessary adjustments of the “orifice of the mouth” to produce these sounds in such a way as to be as opposite as possible to distress screams. Ohala (1980) uses Morton’s (1977) motivation-structural rule explanation to propose an acoustic theory of the origin of smiling. He hypothesizes that in order to produce high-pitched, tonelike sounds, submissive and fearful organisms tend to retract the corners of the mouth to shorten the vocal tract (which raises the resonances). This facial movement may have become an autonomous visual signal in the course of evolution. While this might be a more parsimonious explanation for the smile than Darwin’s, it remains to be explained why the zygomaticus muscle is used to produce the appropriate shape of the vocal tract at the mouth opening rather than other muscle groups which would have the same effect and which would be closer to the facial expression of fear (Ekman, personal communication). A third type of pull factors which may just be a variant of the self-presentation variety concerns the attraction or repelling of others-conspecifics or members of other species. In this case the acoustic features pulled should be the ones that are likely to induce approach or avoidance tendencies, respectively, in potential receivers. A fourth, very clear-cut type of pull effects is associated with conventionalized social signals-stereotyped acoustic sounds that have a shared meaning for the group. For example, predator-specific alarm calls (Marler, 1984; Seyfarth & Cheney, 1982) would seem to belong in this category. In general, any formalized and conventionalized signal, particularly if it involves iconic or arbitrary referencing, will be the result of a pull effect on vocalization. There is a final, fifth type of pull effects-vocal accommodation to an interaction partner. For example, Mundinger (1970) described how flight calls in finches converge on a common group pattern. For humans research in the social psychology of language has shown that speakers converge or accommodate to

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various speech variables of a conversational partner if they have developed positive affect for the other and diverge in the case of negative affect (Feldstein & Welkowitz, 1978; Giles & Smith, 1979). C.

RELATIVE IMPORTANCE OF PUSHAND PULLEFFECTS

While push and pull factors can be analytically separated, they often seem to work in the same direction. For example, harsh sounds which have been shown to covary with a high degree of arousal, often antagonistic in nature (Green, 1975; Jiirgens, 1979; Morton, 1977; Rowell & Hinde, 1962), also seem to be optimally suited for perceptually focusing attention on the vocalizer. Thus, “collectively, these observations are consistent with the proposition that the level of arousal and the level of contact seeking registered by different calls may be communicatively reemphasized by the signal’s relative locatability. The ease of localization may be one of a number of prelinguistic codes in which a facet of the affective state of the vocalizer covaries with a perceptual dimension” (Brown, 1982, p. 159). Another case of push and pull factors operating in the same direction is the use of harsh voice in agonistic encounters, where aggressive intent and strategic use of this signal to enhance the threat value coincide, as described earlier. This is of course strongly related to the classic issue of the “ritualization of signals” in ethology: expressive behavior elements becoming more stereotyped, being produced with “typical intensity” (Morris, 1957) to provide unambiguous information to the receiver or to hide their true motivation in antagonistic encounters (Maynard Smith, 1972) and thus becoming “emancipated” from the motivational states they were originally connected with (Hinde, 198 1; Huxley, 1966; Lorenz, 1965; Smith, 1984; Tinbergen, 1952). The strong pressure exerted by impression (pull) factors on expression (push) factors during the course of the evolution of communication in socially living species is the topic of a stimulating paper by Leyhausen (1967). The relationship between the acoustic structure of the signal and the nature of the referent, then, is frequently similar for both push and pull effects, with the former having developed out of the latter. The difference between the two types of effects is the actual presence or strength of the referent-the referent being an affective or motivational state-at the time when the signal is produced.

D.

DECEFTION IN VOCAL SIGNALING

Producing signals of affective states that the organism does not really experience at the time implies deceptive or manipulative intent. Recently, a number of sociobiologists have claimed that almost all communication is manipulative and deceptive to gain a selective advantage in the reproduction of the organism’s

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genes (Caryl, 1979; Dawkins & Krebs, 1978). This claim implies that virtually all expressive behavior is almost exclusively determined by pull factors and does not provide any reliable information about push factors. If correct, this means that it is impossible to use expressive behavior to diagnose anything other than strategic intent of the sending organism. This rather extreme view has been challenged by a number of other workers in this area. Hinde ( I 98 1) pointed out that there are a number of situations in which cooperative behavior, and consequently truthful signaling, are clearly advantageous to the sender. It would be rather useless and wasteful, for example, to broadcast deceptive messages of sexual readiness to members of one’s own species. In agonistic situations, there is frequently a conflict between several behavioral alternatives (e.g., fight and flight), and the organism may not actually have decided about the behavioral response (a decision which may depend on the changes in the behavior of the opponent). In this case, rather than outright deceit, maximum ambiguity in the meaning of the expressive display would seem to be the optimal strategy (Hinde, 1981). Zahavi (1982, 1983) has argued that an individual who feels superior in an agonistic encounter, confident of winning, does not gain by deception (except by enhancing the expression of confidence to further frighten the opponent), whereas the weaker individual actually stands to lose: producing the deceptive signal is costly and may reduce the chances for successful flight (e.g., by depleting energy). Zahavi concludes that it is the cost of the signal which selects for its reliability. Signals low in cost, in terms of time or effort, can be easily used for deception, without much risk to the sender; the more costly the use of deceptive signals on the other hand, the greater the risk that the disadvantages will outweigh the advantages. “A display of relaxation during an encounter, which provides the rival with the option to attack first, is a reliable display of confidence (the display is reliable) because attacks by rivals select against weak individuals which relax in order to deceive their opponents about their confidence” (Zahavi, 1982). Intuitively, it seems that at least in human communication the sincerity attributed to a sender is directly correlated with the extremity (and thus the cost both in terms of muscular exertion and social image) of an affect display. Furthermore, a signal is seen as all the more trustworthy the closer it comes to being determined by push effects. Scherer (1977) has pointed out that “raw” affect vocalizations seem to be interpreted as more spontaneous and reliable signals, as well as more truly felt, than conventionalized, ritualized “vocal emblems,” produced in a socially stereotyped way with “typical intensity” (cf. Hinde, 1981). For example, the pain experienced by a sender emitting an unarticulated roar seems more real to us than the one indicated by the use of conventionalized emblems like “ouch.” These considerations support the notion that the pull effects cannot move too far away from the original push effects on which they are

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based, at least as far as signals of underlying affective states for self-presentation are concerned. This does not hold, of course, for vocalizations with iconic or arbitrary coding of external referents. Clearly, this does not mean that deception will not occur with high-cost signals. On the contrary, as Goffman (1969) has shown rather convincingly, deception is all the more profitable in those cases where the adversary thinks that a maneuver is too costly or risky to involve deception. To be able to fabricate cues commonly held to be difficult to fake is the high art of the skillful deceiver. However, because of the risk involved and the skills needed, the incidence of high-cost cheating is likely to be low. Quite apart from the cost, the efficacy of deceit clearly depends on the reliability of the signal. Nobody, for example, would be tricked by counterfeit money, even though it looked like the real thing, if the real money did not actually buy something. It is difficult to envisage an economy with only counterfeit money circulating. This is equivalent to the notion of a species with exclusively deceptive signal use. Just as deception requires the existence of truth, fake requires the real. If a signal does not represent anything but the deceptive intent of the signaler in most instances of its use (and if, in addition, it is a cheap signal), it would quickly lose its value. For example, if both opponents in an agonistic encounter were able to use the most powerful threat signal available, just because that would be strategically the most advantageous course of action, and if they could do this without incurring any cost or risk, a real fight with a costly outcome should invariably result (losing the advantage of avoiding actual fighting through the exchange of ritualized intention movements/signals). The outcome of such a fight, however, would not be related in any way to the signal use which preceded it, depriving the signal of its adaptive value. It seems more realistic to assume (as most social psychologists do) that self-presentation generally works to modify (enhance or play down) essentially truthful information about traits and states rather than to simulate nonexisting traits or states. It should be noted that the concern in this section has been exclusively directed toward the determinants of the form, that is, the acoustic structure of affective vocalizations. Although concepts like communicative intention, meaning, and message (see Mackay, 1972; Smith, 1977) are obviously related to this discussion, the issues of sender intentionality and signal meaning are too broad and complex to allow adequate treatment in the present context. Speculatively, one might expect push factors to characterize nonintentional, continuous, affective state signaling and pull factors to dominate intentional, discrete, representational signaling. On the whole, then, one has to assume that both push factors (providing essentially truthful information about the affective state of an organism) and pull factors (which may work in the same direction or which may counteract push

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effects if deceptive intent is involved) jointly determine affect expression. The relative predominance of the two types of determinants may vary widely across situations. This is of particular importance in the light of the suggestion that the evolutionary origin and the actual production of many displays may be related to conflicting motives or behavior tendencies (Baerends, 1975; Hinde, 198 I ; Tinbergen, 1959). Assuming that both push and pull factors can underlie motivation and behavior tendencies, this would support the notion that there is usually joint determination of the display by the two kinds of effects. In the next section, I shall propose a theoretical model which attempts to conceptualize the multiple determination of the dynamic patterns of affect expression by interacting sets of push and pull factors. This model is based on human vocalization as the most advanced form of vocal communication. An extension of the predictions to animal call systems and a comparative discussion will be offered in the final section.

v. A.

THE COMPONENT PATTERNING THEORY OF EXPRESSION

VOCAL

AFFECT

THECONCEPTUAL FRAMEWORK

Based on the component process model of emotion, Scherer (1984a) has proposed a theoretical approach concerning the determinants and the nature of emotional expression-the component patterning theory-which emphasizes the dynamic nature of emotional processes and the multiple determination of affective expression by push and pull factors. Since motor expression is produced by the action system (in particular, the striated musculature), expressive behavior will be affected by dynamic changes in response to SEC outcomes. In addition, motor expression is also affected by the changes in the other subsystems of the organism following stimulus evaluation. Thus, the characteristics of the vocal, facial, or postural expression at a particular point in time represent the net result of the effects of the outcomes of preceding SECs in the information processing subsystem and of the total effect of the changes in the other subsystems impinging upon the action system. Table VI (reproduced from Scherer, 1984b) shows some hypothetical predictions concerning the changes in the various organismic subsystems following specific SEC outcomes. While very speculative, the following changes in the various subsystems can be expected on the basis of functional considerations (changes in the functioning of the vocal organs will be described in more detail below). Evaluation of novelty, in addition to the orienting response, may lead to straightening the posture, raising eyelids and eyebrows for scanning, interrupting ongoing loco-

TABLE VI COMPONENT PATTERNING THEORY PREDICTIONS OF SEC OUTCOME EFFECTSON SUBSYSTEMS“ Action system SEC outcome Novelty Novel

N

Organismic functions

Social functions

support system

Muscle tone

Orienting Focusing

Alerting

Orienting response

Local changes

Homeostasis

Reassuring

No change

No change

Recommending

Sensitization Slight of decrease sensorium

Warning Decommending

Defense response: desensitization

lncrease

Announcing stability

Trophotropic shift

Decrease

o \

Old

Intrinsic pleasantness Pleasant Incorporation

Unpleasant

Expulsion Rejection

G o a h e e d significance Consistent Relaxation

Face

Voice

Instrumental

Posture

Locomotion

Browsilids UP Open orifices No change

Interruption Inhalation

Interruption

Straightening Intemption Raising head

No change

No change

No change

Expanding orifices, “sweet face” Closing orifices, ”sour face”

Wide voice

Centripetal Expanding movement Opening

Approach

Narrow voice

Centrifugal movement

Shrinking Closing in

Avoidance Distancing

Relaxed tone

Relaxed voice

Comfort position

Comfort position

Rest position

No change

Activation

Announcing activity

Ergotropic dominance

Increase

Cormgator Tense voice

Taskdependent

Taskdependent

Task-dependent

Readjustment

Indicating withdrawal

Hypotonus

Lowered eyelids

Lax voice

No activity or slowing

Slump

High power/ Control

Goal assertion

Dominance assertion

Slight decrease Tension in head and neck

Baring teeth Tensing mouth

Full voice

Agonistic movement

Anchoring body, lean forward

No movementor slowing Approach

Low power/ control

Protection

Indicating submission

Trophotropic dominance Ergo-tropho balance Noradrenaline Respiration volume UP Ergotropic dominance Adrenaline Peripheral vasoconstriction Respiration rate up

Hypertonus Tension in locomotor areas

Open mouth

Thin voice

Protective movement

Readiness for locomotion

Discrepant

Coping potential No control

-

N

-4

OFrom Scherer (1984b).

Fast locomotion or freezing

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motion and instrumental action, and deep inhalation. A pleasantness evaluation is likely to cause autonomic sensitization of the sensory organs and orofacial changes maximizing taste and smell sensations as well as instrumental and locomotor approach behavior. Unpleasantness evaluations should result in autonomic desensitization of the sensory organs and defense reactions, including orofacial actions to close the orifices or to expel noxious matter. This involves faucal and pharyngeal constriction (see below) and instrumental and locomotor distancing or avoidance behavior (Andrew, 1963; Gratiolet, 1865; Huber, 1931; Piderit, 1858; Trojan, 1975). The major function of the goal/need significance check is to prepare the organism for appropriate action if things do not happen according to plan. Cannon (1929) was the first to describe the important functions of “emergency” responses in several organismic subsystems in the case of a threat to the organism. Adopting the functional description of the organismic arousal states in terms of a balance between an ergotropic (mostly sympathetic ANS activation) and a trophotropic (mostly parasympathetic ANS involvement) system proposed by Hess (1954) and Gellhorn (1964, 1970), it is suggested that a state of ergotropic dominance follows a discovery of a mismatch between desired state and actual state. A positive outcome of the goal conduciveness check should produce a shift to the trophotropic side of the ergotropic-trophotropic balance, an effect which I will call trophotropic “tuning,” and a balanced tone in the striated musculature, as well as comfort and rest behavior. A negative outcome-a mismatch between actual and desired state-on the other hand, should produce ergotropic dominance, that is, increasing arousal or activation. The effect on the action system should consist of strongly increased tonic innervation of the musculature as well as phasic task-dependent innervations. A facial expression frequently found in response to this condition is the frown (corrugator activity) which has often been treated as a sign of “something difficult or displeasing encountered in a train of thought or action” (Darwin, 1872/1965, p. 222; see also Ekman & Friesen, 1975; Redican, 1982). When the organism sees no possibility of controlling or avoiding a negative event and its consequences, trophotropic dominance and general hypotension of the musculature with slumping posture, slow movement, and a flaccid facial tone is to be expected. When events or outcomes are still controllable but flight is indicated, ergotropic dominance increases still further to provide the organism with sufficient energy for an emergency reaction. Increased adrenaline secretion redirects blood flow to the muscles of the peripheral organs (for running or defense). The hypertension of this musculature may give rise to trembling. Another effect is peripheral vasoconstriction, which reduces the amount of bleeding in the case of injury. Peripheral vasoconstriction also results in a drop of skin temperature. Finally, respiratory rate increases. If the power subcheck results in the evaluation that there is enough power to

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threaten, and if necessary to fight an adversary, dominance assertion will occur. This is predicted to be accompanied by increased noradrenaline secretion (cf. Ax, 1953), which has a “thermogenetic” effect (van Toller, 1979). This may be the reason why anger feels “hot” (Ekman, Levenson, & Friesen, 1983; Scherer, Summerfield, & Wallbott, 1983). Blood flow is redirected to the head and chest to support threat displays and fighting responses (cf. Baccelli, Albertini, Del Bo, Mancia, & Zanchetti, 1981). The i’acial musculature is predicted to show preparatory biting patterns and tensing of the muscles in the neck and around the mouth. A more detailed discussion and justification of these predictions is provided in Scherer (1984b). However, since there is very little pertinent research evidence in most of the areas addressed in this discussion, the predictions are very speculative and will have to be revised as data become available. Apart from changes in the predictions of details in the patterns, the component patterning model is expected to be borne out by future work. The following simple example for a human vocal response, reproduced from Scherer (1984c), illustrates component patterning in somewhat more detail for vocal expression: Following the appraisal of a stimulus as dangerous and requiring action (obstructive to the important goal of survival; coping potential not guaranteed), FO (fundamental frequency of the voice, heard as pitch) will increase because of the effect on the action system (increased muscle tension); at the same time salivation will decrease because of the changes in the support system (sympathetic dominance in the ANS). Both effects will tend to make the voice sound more high pitched (changes in vocal fold vibration and vocal tract resonance). If a split second later the event is reevaluated as a hoax, the state of the fast-responding action system will change again, lowering pitch because of a decrease in muscle tone. The ANS is slower, and it is likely that the effect of reduced salivation on vocal tract resonsance will persist for some time. This example shows that different aspects or features of affective expressions can be differentially affected by system changes over time, such that the pattern of features at any one point in time reflects the impact of a number of very different factors that occurred at different points in the process. These {actors consist not just of the push factors mentioned earlier (e.g., muscle tone driving up FO) but also of pull factors. In the example given earlier, increased FO is likely to be registered by the monitor subsystem (“My voice is terribly high all of a sudden”), and a control command may be routed to the action system (possibly via the executive system) to reduce FO to a level corresponding to the individual’s baseline (or even below that, to ward off all speculation by observers that arousal might be present). However, this voluntary muscular action, because of the force applied or the particular mechanism chosen to reduce FO, may result in other changes in the phonation pattern that may make the voice sound harsh, for example. Thus, the pattern of vocal features immediately after this command

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TABLE VII COMPONENT PATTERNING THEORYPREDICTIONS OF VOCAL CHANCES SEC OUTCOMES" FOI.LOWING DIPFEREN.~ Novelty check Novel

Old No change

Interruption of phonation Sudden inhalation Silence Ingressive (fricative) sound with a glottal stop (noiselike spectrum)

No change

Intrinsic pleasantness check Pleasant

Unpleasant

Faucal and pharyngeal expansion, relaxation of tract walls Vocal tract shortened by mouth corners retracted upward More low-frequency energy, FI falling, slightly broader FI bandwidth, velopharyngeal nasality Resonances raised

Faucal and pharyngeal constriction, tensing of tract walls Vocal tract shortened by mouth corners retracted downward More high-frequency energy, FI rising, F2 and F3 falling, narrow F1 bandwidth, laryngopharyngeal nasality Resonances raised

Wide voice

Narrow voice

Goallneed significance check Relevant and discrepant

Relevant and consistent ~

~~

~~

~

~

Shift toward trophotropic side: overall relaxation of vocal apparatus; increase of salivation FO at lower end of range, low to moderate amplitude, balanced resonance with slight decrease in high-frequency energy

Relaxed voice If event conducive to goal: relaxed voice + wide voice If event obstructive to goal: relaxed voice + narrow voice

~~

~

~

~~

~

Ergotropic dominance: overall tensing of vocal apparatus and respiratory system, decrease of salivation FO and amplitude increase, jitter and shimmer, increase in high-frequency energy, narrow FI bandwidth, pronounced formant frequency differences Tense voice If event conducive to goal: tense voice wide voice If event obstructive to goal: tense voice + narrow voice

+

has been executed is the net result of a multitude of push and pull effects which have consecutively modified the vocal settings and may have all left their traces in determining the vocal features at a particular point in this dynamic process. To understand the factors determining a particular affective expression, the

22 1

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TABLE VI1 (Continued) Coping potential check Control

No control

Ergotropic dominance: (see tense voice)

Trophotropic dominance: hypotension of the musculature in the vocal apparatus and respiratory system Low FO and restricted FO range, low amplitude, weak pulses, very low high-frequency energy, spectral noise, formant frequencies tending toward neutral setting, broad FI bandwidth

(see tense voice)

Lux voice

Tense voice

Power

No power

Deep, forceful respiration; chest register phonation Low FO, high amplitude, strong energy in entire frequency range

Rapid, shallow respiration; head register phonation Raised FO, widely spaced harmonics with relatively low energy

Full voice

Thin voice

Norm/self compatibility check Standards surpassed

+

Wide voice full voice + Relaxed voice (if expected) Tense voice (if unexpected)

+

Standards violated Narrow voice + thin voice + Lax voice (if no control) + Tense voice (if control)

(‘From Scherer ( 1 9 8 4 ~ )

effects of the various components of emotion, including monitor control attempts, on the dynamically changing patterns of motor expression have to be taken into account. It may help to consider the example of the “value-added’’ notion in industrial production (and taxation in some countries) to visualize the process. Each consecutive SEC adds to the meaning of the stimulus or event for the organism, and at each step changes in the different subsystems are instigated which may enhance or modify the states resulting from earlier SEC outcome changes. A vocalization beginning during the evaluation process will be continuously modified as the “value” of consecutive SEC outcome changes are addsd. A vocalization that begins only after the sequence has been completed will reflect the combined effect of the sequence of changes in the various subsystems. According to the component process model and the component patterning model, the outcome of each of the SECs postulated in the sequential evaluation theory of emotional differentiation will have direct effects and indirect effects on

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affective expression. The direct effects consist of the adaptive changes in the action system (i.e., changes in the tonic and phasic tension of the striated musculature) following the SEC outcome (and possibly mediated through the monitor and executive systems). The indirect effects are the push effects from the changes in other subsystems, such as the support system (particularly the ANS). While these consecutive changes continuously modify the pattern of affect expression, it is possible to analytically separate the specific changes produced by the SEC outcomes. B.

DETAILED PREDICTIONS OF COMPONENT PATTERNING

On the basis of this model, Scherer ( 1 9 8 4 ~ has ) proposed a set of predictions concerning the vocal effects of the different SEC outcomes. Table V11 shows a summary listing of these predictions which will now be described in somewhat more detail. For each SEC, the major adaptive function, the predicted push effects, and possible pull effects will be described (and will closely follow the descriptions in Scherer, 1 9 8 4 ~ ) . 1. Novelty Check

The response of the organism after encountering a novel stimulus is an orienring response: an interruption of ongoing processes, a focusing of attention, and a sensitization of sensory mechanisms in order to gather information about the novel stimulus event and to evaluate its significance. The changes in the organism’s subsystems have been rather well studied: cortical arousal, cardiac deceleration, vasoconstriction in peripheral organs and vasodilation of the blood vessels in the head, pupil dilation, skin conductance increase, and changes in the respiratory pattern (Graham, 1973; Lynn, 1966). Also, postural changes directing the sensory organs (particularly eyes, ears, and nose) in the direction of the novel stimulus, will occur. On the whole, these changes will barely affect vocalization (except, possibly, to interrupt ongoing vocalization). Because the SECs follow each other in very rapid succession, various inspiration and expiration sounds which are often associated with surprising events (Darwin, 1872/ 1965, p. 92) are likely to be the joint result of the novelty check and consecutive SECs. Thus, a positive outcome of the intrinsic pleasantness check will have a differential effect on vocalization, depending on whether the stimulus was evaluated as novel or expected (e.g., the joyful surprise “oh” versus the quiet enjoyment “aah”). In general, the characteristics of vocalizations following a novelty evaluation are predicted to show higher amplitude and steeper onset (more explosive) given the preceding deep inhalation and the need to exhale rapidly. As far as pull effects are concerned, while there may be adaptive value in informing other group members about novel

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events, it may also be dangerous to allow oneself to be localized on the basis of a sound before the stimulus has been analyzed further. 2. Intrinsic Pleasantness Check

In terms of adaptive function, “pleasant” outcomes lead to approach behavior tendencies in the action system, whereas “unpleasant” outcomes instigate avoidance tendencies (Berlyne & Madsen, 1973; Schneirla, 1959; Tobach, 1970). Based on speculations by Darwin (187211965, pp. 21 I , 257) and Trojan (1975), it is argued that the approach-avoidance response most directly relevant to vocalization has to do with the acceptance or rejection of pleasant or noxious foods or smells. The assumption is that the oropharyngeal constriction observed in food rejection or regurgitation has generalized to all unpleasant or painful stimuli, whereas oropharyngeal expansion common in the enjoyment and swallowing of food has become associated with nonnutritive or nonolfactory stimuli evaluated as pleasant. On the basis of the phonetic literature, the following acoustic effects are predicted for an unpleasant outcome: faucal and pharyngeal constriction and tensing as well as shortening of the vocal tract should lead to higher energy in the high-frequency region, narrow formant bandwidth, a rise in F1, a fall in F2 and F3, and some degree of “pharyngeal nasality.” This pattern is called “narrow voice.” The effects of a pleasant outcome are more difficult to predict. Faucal and pharyngeal expansion and relaxation should result in a fall in FI and a lowering of the high-frequency energy. On the other hand, a shortened larynx might offset the latter effect. The net result might be a balanced resonance throughout the frequency range, yielding a clear harmonic structure, as postulated by Trojan (1975). In addition, one might expect some velopharyngeal nasality. The summary description is “wide voice.” It seems likely that pull effects developed in response to this SEC outcome since the sharing of the information that particular stimuli deserve approach and others avoidance would reduce the overall trial-and-error behavior in a group and thus be of adaptive value. An issue of particular interest is the question whether the smile may be a ritualized signal originally based on food enjoyment responses and the accompanying vocalizations characterized by oropharyngeal expansion. In terms of the other explanations for the origin of the smile which have been suggested so far (Andrew, 1963; Ohala, 1980; Redican, 1982; van Hooff, 1972), it would seem possible that there are different kinds of smiles with different functions that might well have developed from different origins. 3.

GoullNeed Significance Check

The major functions of this check are ( I ) to establish the significance of a stimulus or event in terms of the goals or motives of the organism, (2) to

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determine whether it is conducive or obstructive to reaching a goal or satisfying a need, and (3) to determine the degree of deviation of the state reached after the stimulus impact from the expected state, thereby specifying the need for external action or internal adjustment. The outcome of this SEC determines the urgency of action and the degree of involvement of the organism. The major effect of this outcome is ergotropic tuning or in the case of emergency reactions, ergotropic dominance. The intensity of ergotropic arousal should increase with increases in the importance of the goals or needs of the organism affected by a stimulus event and increases in the deviation from the expected state. The acoustic effects of ergotropic arousal are fairly well established. On the basis of convergent hypotheses and findings in physiological and acoustic phonetics, the following changes are predicted. Assuming that there are no counteracting pull effects, FO and amplitude increase; there is moderate to extreme jitter and shimmer resulting in the auditory impression of harshness; relative energy of the higher harmonics increases, with corresponding changes in the energy distribution in the spectrum and a narrowing of formant bandwidth (producing the auditory impression of a metallic or piercing voice); and formant values should tend toward greater distance from a neutral position. These characteristics are summarized as “tense voice.” The effects of ergotropic arousal on vocalization are expected to be continuous and graded, that is, the effects should become increasingly stronger as ergotropic arousal goes up. There is no assumption, however, that this relationship is linear. The direction in which there is a discrepancy between desired and actual state affects vocalization in addition to the ergotropic effects. The model predicts that effects similar to a positive outcome of the hedonic valence check will occur if the discrepancy is in the direction of reaching or surpassing the goals: balanced resonance, low F1, and, possibly, velopharyngeal nasality. Conversely, faucal and pharyngeal constriction should occur with failure outcomes, reinforcing some of the characteristics of tense voice and possibly adding faucal nasality. A potential for pull effects is seen in the adaptive advantage of communicating arousal or activity level to the social surround, to advertise the likelihood of highly active behavioral responses to occur in the near future. If expectation and outcome match, the ergotropic-trophotropic balance should shift to the trophotropic side, thereby resulting in “relaxed voice”: FO close to the lower end of the range, low to moderate amplitude, and balanced resonance with slight decrease in the energy of the high frequency region. 4 . Coping Potential Check

This check serves to evaluate the organism’s response potential after a stimulus event requiring a behavioral reaction or internal adjustment has been detected with the goallneed significance check. Three major subchecks determine the nature of the reaction once the causation of a stimulus event (agent and

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motive) has been determined: (1) checking the degree of control over a stimulus event and its consequences (past, present, and future), (2) checking the amount of power to free the organism from domination by the event through external action (fight or flight), and (3) the possibility and difficulty of internal adjustment (e.g., restructuring of goals or self-concept). The outcomes of these subchecks determine the nature of the response, including the type and modality of vocalization. The following acoustic changes are predicted: trophotropic dominance in response to an evaluation of a stimulus event as not controllable and in the case of difficulties with internal adjustment should result in hypotension of the vocal musculature producing the pattern of “lax voice” (low FO and restricted FO range, low amplitude, absence of a clear pulse structure and interharmonic noise due to breathiness, severe energy loss in the upper partials, some nasality, formant frequencies tending toward the neutral setting, and wide formant bandwidth). If the event or its outcome is seen as controllable, the ergotropic system will remain dominant and push vocalization in the direction of tense voice. The second subcheck, the power check, further differentiates the vocal response. A confident outcome is predicted to reduce ergotropic arousal and to result in a shift from tense to relaxed voice. In addition, deep forceful respiration and chest register phonation should produce low FO, high amplitude, and strong energy in the harmonics throughout the frequency range, a pattern named “full voice.” Conversely, further increase in ergotropic arousal and thus tense voice, combined with a pattern referred to as “thin voice,” is expected when the power check is negative. Here, shallow respiration and head register phonation are hypothesized to yield raised FO and widely spaced harmonics with relatively low energy.

5 . Norm Conjormity Check This SEC is expected to occur very late in both phylogenetic and ontogenetic development, with the possibility that it is completely absent in many (or all) species of animals. Thus, it seems rather likely that there is no major biological mechanism responsible for specific vocal effects. The changes in vocalization that do occur may be combinations of the mechanisms described earlier (see Scherer, 1984c, for a more extensive discussion of this point). VI.

CROSS-SPECIES UNIVERSALITYI N THE COMPONENT PATTERNING OF VOCAL EXPRESSION

In Sections I11 and V a new conceptual scheme to describe emotional states in a form amenable to comparative analysis and detailed predictions on the patterning of vocal responses to major determinants of emotion (based on evidence for

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human vocalization) have been proposed. In the remainder of the article these tools will be used to attempt an integration and systematic interpretation of the findings on animal and human vocal expression of emotion reported in Section 11. Furthermore, a set of hypotheses for systematic comparative research in this area will be proposed. These hypotheses rest on the assumption that animal and human affect vocalizations are produced by similar central and peripheral processes, an assumption which may need some supportive argument given the enormous differences in structural and functional complexity between animal call systems and human speech on the one hand and animal affective states and human feelings on the other. However, as for many other organismic structures and functions, the specifically human capacities for vocalization make use of phylogenetically old structures, together with some newly evolved structures which supplement and control but do not replace the old, to achieve more complex results. There is good evidence that both in animals and humans, the limbic system is centrally involved in the mediation of emotion (Arnold, 1960; Heilman & Satz, 1983; MacLean, 1975; Pribram, 1984). Brain stimulation studies in animals have shown that the limbic system controls emotional vocalization (Jurgens, 1979; Jurgens & Ploog, 1970, 1976; Robinson, 1972; see also Steklis & Raleigh, 1979). The important role of the limbic system for human affective vocalization is well summarized by Robinson (1972, p. 442): “human speech normally depends on two systems rather than one. The first and phylogenetically older system is located in the limbic system, is bilaterally represented without hemispheric dominance, antedates primate development, is closely related to emotional, motivational, and autonomic factors, and is capable of transmitting only signals of low informational content. The second system is supplementary to the first, was developed in man, is neocortical, lateralized, and usually dominant in the left hemisphere. . . . The two systems seem to be intimately related and normal speech seems to represent a harmonious mixture of both. In rational and logical discourse, the neocortical system is dominant. In times of emotional stress, however, the limbic system reclaims its old primacy and rational thought and speech are subordinated.” Thus, in terms of central organization, animal and human affect vocalization may well share a number of central characteristics even though there are many important differences. The same seems to be true for the peripheral production site, the vocal apparatus. Apparently, only man is equipped with the phonatory and articulatory structures that are required for the production of speech sounds (see Goerttler, 1972; Lieberman, 1975). Neither the chimpanzees, our closest relatives, nor infants can produce all of the vowel sounds utilized in human languages because of the shape of their vocal tract. Yet, many of the major sound production features involved in respiration, phonation, and resonance are similar in many species of mammals (Negus, 1949; DuBrul, 1977). As will be shown later, even the inner-

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vation of differential groups of laryngeal muscles controlling register differences are the same for the squirrel monkey and for man. Certainly, the effect of heightened muscle tension on vocalization should be comparable (see Scherer, 19794. Therefore, in the hypotheses developed below, a generalization from the predictions in Table VII for human vocalization for a comparative approach will be attempted, although changes concerning articulatory processes are excluded (the term formcinr is used to refer to a neutral vocal tract resonance setting). While the component process model outlined earlier theoretically allows for a large number of combinations of different SEC outcomes, and consequently a large number of different emotional states, it seems reasonable to expect that only a small number of major types will occur very frequently, although there is likely to be much variety in terms of the specific combinations of differentially graded SEC outcomes within each type. The appearance of a small number of major types can be attributed to the existence of a few prototypical, recurring situations in the life of organisms, such as encountering pleasant or unpleasant stimuli or experiencing satisfaction or frustration of important needs or goals. Together with the respective coping potential of the organisms these antecedents seem to define the major types of emotions and their behavioral consequences. Given the frequent occurrence of a small number of typical emotional states, as compared to the less frequent appearance of more unusual combinations of SEC outcomes, one can understand why discrete emotions theorists postulate a small number of innate, basic emotions (Tomkins, 1962, 1963; Izard, 1977; Ekman, 1984). However, as pointed out earlier, the view suggested by the present author differs from that position in questioning the unitary and innately prewired nature of emotional responses. There is agreement, however, on the relative importance of a small number of phylogenetically continuous emotional states arising from a rather small set of antecedent situations. A.

MAJORTYPESOF EMOTIONAL STATES

In this section five major types of emotional states that can be expected to occur frequently in the daily life of many organisms, both animal and human, will be discussed: contentment/ happiness, displeasure/disgust, helplessness/sadness, apprehension/fear, frustrationianger. Using the facet description system proposed in Section Ill,J3, we can define these states in terms of the respective SEC outcomes in the information processing system as well as by the predicted states of the support and executive subsystems. For the executive subsystem, not only organism-centered motivations or behavior tendencies will be mentioned but interactional behavior tendencies likely to be evoked by a particular outcome of the SEC sequence. This is based on the assumption that socially living organisms are frequently in the presence of conspecifics when experiencing emotional states, and thus the behavior instigated by an emotional

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state is frequently social behavior, whether another individual caused the emotion or not. Given the special focus of this article, only the state changes relevant to vocal expression will be discussed for the action system. The labels used to refer to the five types of emotional states are tentative; they have been chosen in such a way as to deemphasize the “feeling” aspect by adding a description which is more antecedent-oriented in order to minimize the danger of anthropomorphizing in applying these labels to animal states. The feeling language cannot be avoided altogether, though, particularly in referring to the states of the monitor subsystem. Here both terms reflecting the intraorganismic state, using established emotion terms, and terms referring to the state of a relationship with an interaction partner will be used. Clearly, it is not suggested that animals experience such feelings in the same way as humans. However, it is not unreasonable to postulate a monitor subsystem with functions similar to the human case for many species of animals with flexible behavioral repertoires. As mentioned earlier, such a subsystem would be in charge of attention deployment and the mediation of feedback from other subsystems. The latter function is particularly important in emotion, a state which is frequently characterized by conflicting messages from the different subsystems and by competing behavior tendencies. As Jiirgens (1979, p. 98) points out, “Emotional terms . . . are often the only terms available for a brief description of complex motivational states of an animal, that is states which cannot be characterized by the probability of occurrence of a single behavior pattern but only by the probabilities of occurrence of a great number of different behavior patterns.” In summary, then, the types of emotional states discussed below are expected to be descriptions valid for both the human and a large number of animal species. They will be used as a basis for a comparative analysis of vocal expression of emotion. Detailed predictions of the acoustic features of vocalization to be expected for these five types of emotional states are listed in Table VIII. Based on the component patterning predictions for the major SEC outcomes in Table VII and the combinations of SEC outcomes postulated earlier for the five types of states, these predictions can be derived as hypotheses to be tested in further research. Each of the five types of states will now be described in detail. In each case, an attempt will be made to integrate the observations on animal vocal expression described in the first section with the major findings on human expression. While the evidence on animal vocalizations will be examined in some detail, the literature on human vocal expression is referred to only summarily since a detailed discussion is available in Scherer ( 1 9 8 4 ~ )While . the emphasis in this discussion will be on the modal patterns for each type of emotional state, some of the transitions and gradations between patterns will be mentioned. Indeed, the value of the conceptual system proposed earlier is seen particularly in its ability to

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TABLE Vlll PRbDlCTED ACOUSTIC FEATURES OF MAJOREMOTIONAL STATES“

Feature :O modulation ;O mean :O range :O variability :O shift contour :O shift regularity :I mean :2 mean ;I bandwidth ’otal intensity ntensity variation xquency range ligh-frequency energy ipectral noise hation :ate

Contentment/ happiness

Displeasure/ disgust

Helplessness/ sadness

Apprehension/ fear

>

> < >

< Q Q

B

< <

<

<

-

-

< >

< <

> >

B 9 B

> >

e

B

>

>

<

>

> >

>

Q

9

>

< < < <

Frustration/ anger

B

< <>

“<, Decrease; Q , strong decrease; >, increase; B , strong increase; =. no change. Combinations imply that lirection of change may vary. It should be noted that these predictions are preliminary and are subject to change with revisions of the model.

account for differences within and transitions between classes-in addition to providing a systematic description of the antecedents of an emotional state. 1. ContentmentIHuppiness

This type of emotional state is characterized by the encounter of an intrinsically pleasant stimulus and/or the satisfaction of a need or the reaching of a goal. The tuning of the support system moves toward the trophotropic side in line with the emphasis in the executive system on consummation, rest, or recovery with corresponding monitor states of contentment, pleasure, or happiness. The interactional behavior tendencies are likely to include social contact (e.g., grooming) and sharing (of food or other pleasant stimulation), thereby reflecting states of affection or friendliness. The state of the action system as far as the vocal organs are concerned is characterized by egressive respiratory sounds, relaxed phonation, and wide, relaxed vocal tract settings. The resulting vocalizations should be short and soft with relatively low FO, small FO range and variability, gradual and regular FO shifts with upward or downward directed contours, and a somewhat broader bandwidth of the first formant (FI). It should be noted here that “formant” is

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used in this section to refer to the resonances specific to a long-term vocal tract shape of an organism rather than to segmental vowel articulation as in human speech (see neutral setting, Laver, 1980, pp. 15-17). The predicted pattern corresponds rather well to Tembrock’s (see Section I1,A) characterization of comfort and play calls in the contact range. It also corresponds to our intuitive concept of the nature of contentment sounds in humans (such as emitted while sitting in a bathtub, getting down in a comfortable armchair for a restful evening, or seeing appetizing food). Unfortunately, this type of contentment and “quiet happiness” has rarely been studied empirically. In most studies, the positive emotions are represented by elation/joy/ebullient happiness, states which are characterized by a much higher preponderance of ergotropic tuning and consequently stronger general activation. In terms of the outcomes in the SEC sequence, these states are probably the result of an utiexperredly positive event (in terms of goal/need conduciveness), which should increase ergotropic tuning because of the mismatch between expected and actual outcome. It is not clear at present to what extent the kind of cognitive ability required for exact predictions of expected outcomes is present in animal species, and whether, in consequence, there are analogs to elation or joy. At least for chimpanzees, a pattern homologous to human laughter seems to exist (van Hooff, 1972; Redican, 1982). Also, there seem to be more excited forms of pleasure sounds than quiet comfort sounds in animals. Jurgens’ description of the twittering-chatteringcackling group found in a variety of primates (1979, p. 108-1 1 1 ) shows the involvement of a strong ergotropic component in the states underlying these calls. This component may be due to the expectation of food (i.e., pleasurable anticipation short of contentment, e.g., in the case of twitter in squirrel monkeys) or to a more or less strong aggressive component, resulting in bellicosity, for example. Since in these states there are no goal/need conduciveness or satisfaction antecedents compared to the contentment state, one expects and, indeed, finds a strong involvement of tense vocalization, as shown in higher FO and greater FO range (see also van Bezooijen, 1984). Jurgens points out (1979, p. 109) that all three of the aforementioned calls have a very pronounced social function: they serve to confirm social bonds between vocalizers. It is interesting to note that these calls are also very rhythmic, entailing the repetition of rather regular elements. Such regularity of rhythm could be due to pull effects in the service of social communication-both in terms of eliciting the attention of others as well as, potentially, providing symbolic reference. Another interesting possibility is that rhythm furthers the contagiousness of the emotional state underlying a call or the behavior following it. Jurgens mentions that all three calls have a high interindividual frequency of occurrence pointing to their functional significance in recruiting companions (for fighting or to share in pleasurable events). Human laughter is surprisingly similar

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23 1

to twittering and chattering in terms of acoustic features including rhythmicity, contagiousness, and aggressive overtones (Lorenz, 1963; see Table 10 in Jiirgens, 1979). It would be fascinating to explore to what extent such rhythmic call features might be based on very basic neuronal mechanisms in the form of rhythmical brain activity serving to integrate the sensory, visceral, and motor systems (Komisaruk, 1977, 1983). 2 . DispleasurelDisgust This type of emotional state results from encountering an intrinsically unpleasant stimulus which, however, does not obstruct the major needslgoals of the organism and the effects of which can be easily controlled by an avoidance response. There may be a slight tendency toward ergotropic tuning in the support system to prepare for avoidance and rejection responses. The corresponding monitor states can be labeled as disgust and, interactionally (probably only for humans), contempt toward a person responsible for producing the unpleasant stimulus, usually an undesirable action. The vocal response is likely to be a fast egressive sound through the mouth or nose or both. If voiced, phonation is likely to be slightly tense. The vocal settings are very narrow and also slightly tense. The most significant acoustic features of the resulting vocalization are noise components in the spectrum due to frication following forced exhalation, and, at least for humans, the reduction of the distance between Fl and F2lF3 and the narrowing of F1 bandwidth (associated with faucalization). Displeasureldisgust calls are not usually reported for animal species. It is possible that such sounds are mostly determined by push effects in animals and have not, as in humans, acquired communicative significance with pull effects leading to ritualized sound forms. However, warning of unpleasant stimuli through the use of vocal signals would seem to serve an important adaptive function since it should reduce the cost of trial-and-error behavior for the group as a whole. Thus, it may be worth the effort to search for such calls in animal repertoires. For humans, there is little empirical evidence for the predicted pattern except for some early case studies by Trojan and Winckel ( I 957). Fairbanks and Pronovost ( 1939) found low FO and a wide FO range, van Bezooijen (1984) low pitch, harshness, and slow tempo (as rated by judges), for the simulation of contempt. These results are in line with the predictions made here.

3. HelplessnesslSadness This emotional state is expected to follow the encounter of an event which obstructs the path to reaching important goals or satisfying major needs and whose consequences cannot in any way be controlled by the organism, that is, the negative consequences can be neither fought nor avoided. The only course of action open to the organism is internal restructuring, such as revising goals or expectations and rearranging relationships. Trophotropic dominance in the sup-

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port system reflects this turning inward, recovery-oriented behavioral reaction, leading to monitor states of sadness, hopelessness, and isolation. It should be noted that states in which an appeal for outside help is made are not included with this type of emotion, since the organism in this state has not given up hope of eventually avoiding or minimizing the negative consequences, with the help of others. The vocal response is likely to include passive exhalation, lax phonation, and a lax vocal tract setting, resulting in prolonged sounds with low FO, restricted FO range and variation, strong FO perturbation (because of the flaccidity of the vocal folds), downward directed FO contours, broad F1 bandwidth, very low intensity, presence of spectral noise (due to breathiness), decreased frequency range in the spectrum, and very little energy in the upper frequency regions. Calls corresponding to this pattern have not been reported in the comparative studies on animal vocalization that have been used to prepare this article. It is an interesting question whether animals can be “sad” in the human sense. While there are subjective reports about animals “mourning” the death of a mate or a master as well as experimental data on helplessness in animals (Seligman, 1975), the nature of the vocal response has not been systematically studied so far. The human evidence (see Scherer, 1981b, 1984~;van Bezooijen, 1984; Williams & Stevens, 1981) strongly supports the theoretical predictions for sadness. It must be emphasized that these predictions do not extend to states of mourning characterized by high arousal, such as hysteric grief. In such a case, there may still be an illusion of control or the strong desire for Lmtrol as well as protest accompanied by ergotropic arousal.

4. DungertFeur The defining characteristics for this type of emotional state are the occurrence of a signal event (with or without negative consequences) which precedes other events that will endanger major needstgoals of the organism such as survival and bodily integrity. The outcome of the coping potential check indicates that while there is not enough power to fight the event, control of the consequences may be possible through a flight or escape response. Control of the consequences being possible, if only via escape, is a central feature of the antecedents for this state. The support subsystem shows strong ergotropic dominance, the “emergency response,” to deal with the danger situation. The behavior tendencies of fleeing or freezing on the one hand or submission in terms of social behavior to escape negative consequences on the other hand are reflected in monitor states of wariness or fear and social unease or inferiority. The initial vocal response is likely to be a sudden deep inhalation, followed by a pattern of rapid, shallow breathing, very tense phonation in the head register, and a highly tense vocal tract setting. The acoustic results are predicted to consist of prolonged sounds with high FO, strong FO perturbation, very wide FO range

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and high variability, highly irregular FO shifts mostly with an upward contour, narrowing of Fl bandwidth, and an increase in the frequency range of the spectrum (due to the widely spaced harmonics for a high FO) with stronger relative energy in the upper region of the spectrum. This pattern is in perfect agreement with the acoustic effects described by Tembrock for submission calls and by Morton for motivational states characterized by fear or appeasement (see Section 11,A). Closely corresponding to this pattern are the yelling and squealing in the squirrel monkey and the screaming or screeching in other primates as described by Jiirgens (1979, pp. 105-108). His discussion of chirping and peeping in squirrel monkeys, calls which are acoustically similar, points to differences in function-these calls mainly serve as contact signals. While Jiirgens places them in the same group with yelling and squealing on the basis of acoustic similarity, labeling the common emotional state as social unease or a lack of self-confidence, the two subgroups of calls might actually be rather different in terms of their vocal determinants. Whereas low-power push effects seem to dominate in yelling and squealing, pull effects related to the function of maintaining the integrity of the group could be primarily responsible for the acoustic structure of chirps and peeps. The acoustic cues of the latter correspond to Tembrock’s description of attraction calls in the distance range. The rather smooth and regular FO contours in these calls seem to reinforce the impression that social communication-motivated pull effects determine the acoustic structure of these types of calls. It is interesting to speculate on whether grouping together fear, appeasement, and friendliness sounds, as proposed by Morton, is defensible from a functional point of view or whether it should be split into two groups. While some of the acoustic cues might be similar, it is possible that “friendly” sounds are more like contact calls with a different origin, differential involvement of pull factors and possibly also differences in the detail of the acoustic structure. Clearly, this issue is most relevant to the theories concerning the origin of the smile and the issue of facial or vocal priority in the evolutionary development of the signal (see earlier discussion; and Andrew, 1963; Ohala, 1980; Redican, 1982; van Hooff, 1972). Alarm calls are of specific interest in the context of apprehension/fear states. Here one would expect involvement of both push effects based on fear states as well as pull effects maximizing the signal clarity for warning purposes. Jiirgens concludes on the basis of his own work on squirrel monkeys and a review of observations of other primates that “short, loud calls with a plosive beginning and a rapid downward shift of main energy from higher to lower frequencies are very widely used among primates as alarm calls” (I979 , p. 104). While these alarm calls show some of the acoustic features expected as push effects in fear states, such as high FO and wide frequency range, there seem to be a number of

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standardized acoustic elements that are likely to be conventionalized and produced by pull effects. It is easy to see how such standardized elements could be differentiated to yield symbolic reference, for example, to different types of predators (Marler, 1984; Seyfarth & Cheney, 1982). The data available for human fear vocalizations also support the theoretical predictions: high FO with a wide FO range and large FO variability as well as fast tempo have been reported (see Scherer, 1981b, p. 206). In addition, Williams and Stevens (198 I ) report rapid FO shifts and discontinuities as well as relatively high energy in the upper frequency region. While there are a large number of findings on vocal response to stress (see Scherer, 1981a), it is difficult to compare the emotional states produced in stress experiments with fear, given the widely different stress induction techniques that have been used and the difficulty of predicting the subjects’ responses in terms of preceding SEC sequences (cf. Scherer, 1984~). It should be noted parenthetically that pain vocalizations represent a type of emotional blend. On the one hand, there is the typical response to an extremely unpleasant type of stimulation. On the other hand, more than in disgust responses to unpleasant taste or smell, the major goals of survival and bodily integrity may be at stake, producing high ergotropic arousal particularly when pain is intense and prolonged. Consequently, pain vocalizations can be expected to share attributes of both displeasure/disgust and apprehensiodfear vocalizations. 5 . FrustrationlAnger

The condition producing this type of emotional state consists of obstructing an organism from satisfying a need or reaching a goal in a situation where the organism feels confident that it is powerful enough to remove the obstacle by force or to otherwise prevent negative consequences. As shown earlier, there will be some ergotropic tuning because of the mismatch between desired and actual state but not ergotropic dominance. The behavior tendencies are directed toward vigorous pursuit of the original goal/need and toward threat or fight, accompanied by monitor states that can be labeled irritation, anger, rage, and, in terms of interpersonal feeling, hostility. If action system changes affect the vocal organs, this should result in prolonged, deep ingressive sounds, moderately tense phonation in the chest register, and tense vocal tract settings. In terms of acoustic features, one would expect an increase in FO (with mean FO remaining in the low range), wide FO range and large FO variation, some FO perturbation, narrow FI bandwidth, strong intensity, a very wide frequency range in the spectrum (due to strong energy in the harmonics throughout the frequency range), some interharmonic noise, and strong evidence of pulsing in the spectrogram. These characteristics correspond very well to Tembrock’s description of dominance and threat calls, Morton’s description of the sounds indicating hostility and

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aggressiveness, and Jiirgens’ conclusion concerning his purring-growling-spitting group: “non-harmonic calls, pulsed in a 50 2 20 Hz rhythm and containing energy between 1 and 3 kHz seem to be generally used in primates to express a state of self-assertiveness with a more or less threatening character” ( 1979, p. 100). Interestingly, in the squirrel monkey the probability of an attack following the vocalization increases in a direct relationship with increases in the frequency range of the call. The research results on the vocal effects of human anger are also very much in line with these predictions: strong intensity, wide FO range and large FO variation, strong FO perturbation, a broad frequency range with relatively higher energy in the upper region (see Scherer, 1981b, p. 206; van Bezooijen, 1984; Williams & Stevens, 1981). One exception is mean FO. It was predicted earlier that F0 should slightly increase but remain in the low range (which is confirmed by the observations of animal vocalizations). The empirical data on human anger portrayal, however, tend to show a rather high mean FO, often higher than in fear states. One possibility is that the actors, which were used in most studies to simulate the emotional expressions, produced extreme forms of anger with a very high arousal and a relatively low power or assertiveness component. B.

TRANSITIONS BETWEEN TYPES

This discrepancy raises the important issue of transitions between the prototypes presented. On the basis of the component patterning model, one would expect these transitions to be characterized by gradual changes in those parameters that are associated with the differential outcomes of specific SECs. For example, an organism involved in an agonistic encounter may evaluate its power to deal with the adversary as less and less adequate as the encounter progresses. As a result, chest register phonation should gradually change to head register phonation in a transition from threat calls to fear or submission calls. Similarly, in the case of the presence of conflicting evaluations and behavioral tendencies, when the organism may vacillate between the respective patterns, one would expect the changes in the transitions to be determined by the SEC outcomes that differentiate the two conflicting states. For example, goal obstruction situations, in which there is a negative outcome of the power check but in which flight is not a viable alternative or necessity, may result in vocalizations that are transitions between the apprehension/fear and the frustratiodanger types. Appropriate examples in animal communication might be defense calls, as described by Tembrock as transitions from threat calls, or by Jiirgens’ groaning-cawing-shrieking group, which he links to protest. These calls, typical for agonistic encounters, are used by both the dominant and the inferior animal indicating an increased flight motivation. While some of the acoustic elements are similar to those of the purring-growling-spitting group,

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indicating assertiveness, the major difference is that the former are never pulsed like the latter. This confirms the role of voice register in indicating the outcome of the power subcheck: high assertiveness seems to be accompanied by a phonation process in which supraglottal structures are recruited to participate in the voicing to “produce a loud voice with low pitch” (Sawashima & Hirose, 1983, p. 20). While the details of this process are not yet established, the phenomenon has been called pulse register, glottal fry, creak, or laryngealization-it seems to represent the extreme form of the chest register. Very low power, lack of confidence, or helplessness, on the other hand, are accompanied by head register or falsetto phonation. Interestingly enough, the voice register mechanism may be similar in the squirrel monkey (see Jurgens, 1979, p. 113, on the existence of separate registers in this species) and in Homo supiens. In both species the cricothyroid muscle, which is innervated by the external laryngeal nerve, seems exclusively responsible for controlling FO in head register (the upper region of the FO range) whereas other laryngeal muscles, particularly the vocalis muscle, which are innervated by the recurrent nerve, jointly act with the cricothyroid to control FO in chest register. “The difference in the muscle control between the two registers results in a difference in the physical conditions of the cover and body of the vocal folds, which is reflected in the mode of vocal fold vibration” (Sawashima & Hirose, 1983, p. 21). Thus, there seems to be a continuum from pulse register over chest register to head register along which phonation can vary in correspondence with the confidence or assertiveness of the vocalizer, allowing for a large number of transitions in line with changes in the outcome of the coping potential check. Independent of register, tenseness of the laryngeal structures involved in phonation seems also to vary continuously as a function of ergotropic arousal in response to goal/need, match/mismatch outcomes. Evidence from studies on animal vocalization (Ehret, 1980; Jurgens, 1979; Morton, 1977; Tembrock, 1975) and human vocalization (Scherer, 1981a,b) seems to show that FO and high frequency energy increase as a direct function of ergotropic arousal or activation. Again, many transitions from mismatch to match evaluations are possible as environmental stimulation or internal evaluation changes. The third acoustic dimension which allows continuous transitions is related to the intrinsic pleasantness check. Differential narrowness or wideness of the vocal tract occurs in response to unpleasant or pleasant stimulation, respectively. Unfortunately, the nature of the acoustic features which vary along this dimension cannot yet be established with any confidence. Presence of fricative noise due to the constriction and dampening of particular regions of resonance are features that are likely to be involved. It will have become obvious by now that the acoustic dimensions described earlier map directly onto the potency, activity, and positive/negative evaluation

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dimensions that have been proposed by many psychologists since Wundt (see Plutchik, 1980, for an overview). Scherer (1984b) has argued that dimensional approaches may indeed be useful to describe the response domain of the emotional processes in terms of some of the major continua along which the states of some of the subsystems can vary. However, dimensional theories cannot explain why certain emotions occur and which processes determine the specific patterning of the responses. Clearly, in addition to studying the vocal expression of the major types of emotional states outlined earlier, the many possibilities for transitions between these prototypes will have to be systematically charted. The existence in many animal species of chains of calls with continuous transitions between acoustic features which clearly follow changes in the evaluation of threat (varying with distance, for example) or changes in the evaluation of power (varying with the response of the adversary to threat displays, e.g., Marler & Tenaza, 1977; Rowel1 & Hinde, 1962) will be most useful for this purpose. This task will be more difficult for human vocalizations in which naturally occurring transitions are likely to be obscured by a variety of social control mechanisms involving masking, suppression, amplification, and segmentation. It is expected that important insights might result from investigating the relationship between power and vocal register, goal/need match/mismatch and muscular tension, as well as pleasure/displeasure and constriction versus expansion in a number of widely different species.

VII.

CONCLUSION

This article has attempted a very speculative survey of largely uncharted territory. In many cases assertions and predictions have been based on hunches expressed by individual workers or on isolated observations in case studies. Often, personal intuitions and inferences from everyday life have been used to complement fragmentary evidence. Furthermore, even though the term animals has been used literally in this article, most of the discussion has focused on mammals. It remains to be seen how much of the vocal affect expression patterning described here can be generalized across species. However, in spite of the preliminary nature of both the theoretical analysis and the data which support it, there can be little doubt about the promise of a comparative, functionally based approach to the study of expression, just as envisaged by Charles Darwin over a century ago. As mentioned in the introduction, our tools to address the problems of empirical research in this area are woefully inadequate, beginning with the lack of agreed upon conceptual definitions of the very phenomena to be studied. As the discussion in this article has made abundantly clear, progress in this area depends on the interdisciplinary collaboration between biologists, eth-

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ologists, neurologists, psychologists, phoneticians, and electrical engineers (working on acoustic signal processing and vocal tract modeling). It is hoped that the approach suggested in this article may help to stimulate interest in the topic of the vocal expression of emotion in several of these disciplines. Eventually, this might generate research which will help to answer the many questions raised and to test some of the predictions made. While the complexity of the processes involved may seem staggering, the promise is equally great. If we are able to establish a valid correspondence between the nature of specific acoustic cues and the underlying outcome of the consequences of an organism’s evaluation of its environment, both in terms of organismic states and behavior tendencies, we will have made major progress toward understanding the processes involved in the control of behavior. Acknowledgments

I wish to thank Drs. C. Beer, R. A. Hinde, P. Marler, J . Ohala, J . Rosenblatt, and P. Slater for critical comments and suggestions on earlier versions of this manuscript. I accept, of course, full responsibility for any shortcomings remaining despite the excellent advice. The manuscript was written during a sabbatical at UC Berkeley, supported in part by a stipend from the Stiftung Volkswagenwerk.

References Andrew, R. J . (1963). The origin and evolution of the calls and facial expressions of the primates. Behaviour 20, I- 109. Arnold, M. B. (1960). Emotion arid personulitv: Vol. 1 . Psychological aspects. New York: Columbia Univ. Press. Averill, J . R. (1980). A constructivist view of emotion. In R. Plutchik & H. Kellerman (Eds.), Emotion: Theory. research, and experience (Vol. I , pp. 305-340). New York: Academic Press. Ax, A. F. (1953). The physiological differentiation between fear and anger in humans. Psvchosom. Mrd. 15, 433-442. Baccelli, G . , Albertini, R., Del Bo, A , , Mancia, A,. & Zdnchetti, A. (1981). Role of sinoaortic reflexes in hemodynamic patterns of natural defense behaviors in the cat. Am. J . Phvsiol. 240, 42 1-429. Baerends, G . P. (1975). An evaluation of the conflict hypothesis as an explanatory principle for the evolution ofdisplays. In G . Bacrends. C. Beer, & A. Manning (Eds.), Function and evolution in brhaviour. Oxford: Clarendon. Beer, C. (1975). Multiple functions and gull displays. In G . Baerends, C. Beer, & A. Manning (Eds.), Function and evolutioii in brhaviour. Oxford: Clarendon. Berkowitz, L. (1962). Aggression: A social ps.ychologica1 unu/,vsis. New York: McGraw-Hill. Berlyne, D., & Madsen, K . B. (1973). Pleasure. reward, and preference: Their nuture. determinants and role in behavior. New York: Academic Press. Bezooijen, R. A. M. G., van (1984). Characteristics and recoKnizahility of vocal expressions of emotion. Dordrecht: Foris. Blount, B. G . (1982). The ontogeny of emotions and their vocal expression in infanta. In S. A .

VOCAL AFFECT SIGNALING

239

Kucza.1 II (Ed.), Lmigimge developmetit; V d . 2. Language, thought and culture (pp, I3 I - 162). Hillsdale, NJ: Erlbauni. Borg. J. ( 198 1 ). AnM.e,idimgsf,rienti~~rte multidirne,lsionalt.ne~isionul~,Skalierurrg. Berlin: Springer. Brown, C. (1982). Auditory localization and primate vocal behavior. In C. T. Snowdon, C. H. Brown, & M. R. Petersen (Eds.), Primate co~nmunication(pp. 144- 164). Cambridge: Cambridge Univ. Press. Cannon, W. B. (1929). Bodily choriges in pairi. hunger, ,fi,ar urzd ruxe (2nd ed.). New York: Appleton. Caryl. P. G. (1979). Communication by antagonistic displays: What can games theory contribute to ethology'? Brhaviour 68, 136- 169. Collias, N. E. (1960). An ecological and functional classification of animal sounds. In W. E. Lanyon & W. N. Tavolga (Eds.). Animal sounds arid commrtnicution (pp. 368-391). Washington, D.C.: Amer. Inst. of Biological Science. Darby, J. K. (Ed.) (1981). Speech evaluation in psvchiotry. New York: Grune & Stratton. Darwin, C. (1872). The expression of the emotions irz nian und animuls. London: Murray. (Reprinted, Chicago: Univ. of Chicago Press, 1965.) Dawkins, R . , & Krebs, J. R. (1978). Animal signals: information or manipulation'? In J. R . Krebs & N. B. Davies (Eds.), Behuvioitrul ecology (pp. 282-309). Oxford: Blackwell. DuBrul, E. L. (1977).Origin of speech apparatus and its reconstruction in fossils. Brairi La,zguage 4, 365-381. Ehret, G . (1980). Development of sound communication in mammals. In J. S . Rosenblatt, R . A. Hinde, C. Beer, & M.-C. Busnel (Eds.), Advatices i j i the stiic/y ojbehavinr (pp. 179-218). New York: Academic Press. Eisenberg, J. F. (1974). The function and motivational basis of hystcricomorph vocalizations. Svmp. Zool. Soc. London 34, 21 1-247. Eisenberg, J. F. (1976). Communication mechanisms and social integration in the black spider monkey (Ateles fusciceps robustus) and related species. Smithsoniafi Connib. Zool. 2 13. Ekrnan. P. (1984). Expression and the nature of emotion. In K. R . Scherer & P. Ekman (Eds.), Approaches to emotiori (pp. 3 19-344). Hillsdale, NJ: Erlbaum. Ekrnan, P., & Friesen, W. V. (1975). Unmuskirig the face. New York: Prentice Hall. Ekman, P.. & Scherer, K. R. (1984). Questions about emotion: An introduction. In K. R . Scherer & P. Eknian (Eds.). Approaches to emotion (pp. 1-12). New York: Erlbaum. Ekman, P., Levenson, R . W.. & Friesen, W. V . (1983). Autonomic nervous system activity distinguishes between emotions. Science 221, 1208- 1210. Emde. R . N. (1984). Levels of meaning for infant emotions: A biosocial view. In K. R . Scherer & P. Ekman (Eds.), Approaches to emotion (pp, 77-108). New York: Erlbaum. Fairbanks, G . , & Pronovost, W. (1939). An experimental study of the pitch characteristics of the voice during the expression of emotion. Speech Monogr. 6, 87-104 Feldstein, S., & Welkowitz. J. (1978). A chronography of conversation: In defense of an objective approach. In A. W. Siegman & S . Feldstein (Eds.), Nonverbal behavior and communicurion (pp. 329-378). New York: Erlbauni. Gellhorn, E. (1964). Motion and emotion: The role of proprioccption in the physiology and pathology of the emotions. Psycho/. Rev. 71, 457-472. Cellhorn. E. (1970). The emotions and the ergotropic and trophotropic systems. Psvchol. Forsch. 34, 48-94. Giles. H., & Smith, P. M . (1979). Accommodation theory: Optimal levels of convergence. In H. oflangurrgr (pp. 45-65). Oxford: Blackwell. Ciles & R. St. Clair (Eds.). The sociulpsvcholo~~ Giles, H., Scherer. K . R . , & Taylor. D. M . (1979). Speech markers in social interaction. In. K . R . Scherer & H. Giles (Eds.). Social murkers in speech (pp. 343-381 ). Cambridge: Cambridge Univ. Press.

240

KLAUS R . SCHERER

Goerttler, K. (1972). Morphologische Sonderstellung des Menschen im Reich der Lebensformen auf der Erde. In H.-G. Cadamer & P. Vogler (Eds.), Neue Anthropologie (Vol. 2, pp. 215-257). Stuttgart: Thieme. Goffman, E. (1969). Strategic interaction. Philadelphia: Univ. of Pennsylvania Press. Gould, E. (1963). Mechanisms of mammalian auditory communication, In 5. F. Eisenberg & D. Kleiman (Eds.), Advances in the study of mammalian behavior (pp. 265-341). New York: Amer. SOC.of Manimalogists. Gouzoules, S., Gouzoules, H., & Marler, P. (1984). Rhesus monkey (Macacu muluttu) screams: Representational signalling in the recruitment of agonistic aid. Anim. Behav. 32, 182. Graham, F. K. (1973). Habituation and dishabituation of responses innervated by the autonomic nervous system. In H. Peeke & M. Herz (Eds.), Habituation: Behavioral studies and physiological substrates (Vol. 1). New York: Academic Press. Gratiolet, P. ( I 865). De la phvsionomie et des mouvements d'expression. Paris: Hetzel. Green, S . (1975). Variation of vocal pattern with social situation in the Japanese monkey (Mucaca ,fuscata): A field study. In L. A. Rosenblum (Ed.), Primate behavior: Developments in.field and laboratory research (Vol. 4, pp. 2-102). New York: Academic Press. Green, S., & Marler, P. (1979). Analysis of animal communication, In P. Marler & J . G. Vandenbergh (Eds.), Handbook of behavioral neurobiology: Vol. 3. Social behavior and communication (pp. 73-13), New York: Academic Press. Griffin, D. R. (1976). The question of animal awareness. New York: Rockefeller Univ. Press. Guttrnan, L. (1957). Introduction to facet design and analysis. Proc. fnt. Congr. Psychol.. 15th. Brussels. Amsterdam: North-Holland Publ. Hebb, D. 0. (1949). The organization qf behavior. New York: Wiley. Heilman, K. M., & Satz, L. (1983). Neuropsychology of emotion. New York: Guilford. Hess, W. R. (1954). Das Zwischenhirn. Syndrom, Lokalisation. Funktionen. Basel: Schwabe. Hinde, R. A. (1981). Animal signals: Ethological and games-theory approaches are not incompatible. Anim. Behav. 29, 535-542. Hockett, C. F. (1960). Logical considerations in the study of animal communication, In W. E. Lanyon & W. N. Tavolga (Eds.), Animal sounds and communication (pp. 392-430). Washington, D.C.: Amer. Inst. of Biological Sciences. Hooff, J . A., van (1972). A comparative approach to the phylogeny of laughter and smiling. In R . Hinde (Ed.), Non-verbal communication (pp. 209-24 I ). Cambridge: Cambridge Univ. Press. Huber, E. (I93 I ). Evolution of,fucial musculature and,facial expression. Baltimore: Johns Hopkins Press. Huxley, J . (1966). A discussion on ritualization of behaviour in animals and man. Introduction. Philos. Trans. R. Sor. Br. 251, 249-271. Izard, C. E. (1977). Human emotions. New York: Plenum. Jiirgens, U . (1979). Vocalization as an emotional indicator: A neuroethological study in the squirrel monkey. Behaviour 69, 88-1 17. Jiirgens, U . (1982). A neuroethological approach to the classification of vocalization in the squirrel monkey. In C. T. Snowdon, C. H. Brown, & M. R. Petersen (Eds.). Primate communication (pp. 50-62). Cambridge: Cambridge Univ. Press. Jiirgens, U . , & Ploog, D. (1970). Cerebral representation of vocalization in the squirrel monkey. Exp. Brain Res. 10, 532-554. Jurgens, U . , & Ploog, D. (1976). Zur Evolution der Stimme. Arch. Psychiat. Nervenkr. 222, 117137. Komisaruk, B. R. (1977). The role of rhythmical brain activity in sensorimotor integration. Prog. Psychobiol. Physiol. Psvchol. 7, 55-90. Kornisaruk, B. R. (1983). Visceral-somatic integration in behavior, cognition, and "psychosomat-

VOCAL AFFECT SIGNALING

24 1

ic” disease. In J . S . Rosenblatt, R. A. Hinde, C. Beer, & M.-C. Busnel (Eds.),Advances in the study ufbehuvior (Vol. 12, pp. 107-140). New York: Academic Press. Laver, J . ( 1980). The phonetic description of voice quality. Cambridge: Cambridge Univ. Press. Lazarus, R. S . (1968). Emotions and adaptation: Conceptual and empirical relations. Nebr. Symp. Motivut. 16, 175-270. Lazarus, R. S . , Averill, J . R., & Opton, E. M. (1970). Towards acognitive theoryofemotion. In M. B. Arnold (Ed.), Feelings and emotions (pp, 207-232). New York: Academic Press. Leventhal, H. (1979). A perceptual-motor processing model of emotion. In P. Pliner, K . Blankstein, & I . M. Spigel (Eds.), Advances in the study of communication and affect: Perception and emotion in self’ and others (pp. 263-299). New York: Plenum. Leyhausen, P. (1967). Biologie von Ausdruck und Eindruck (Pt. I ) . Psychol. Forsch. 31, 113-176. Lieberman, P. (1975). On the origins of language: An introduction to the evolution of human speech. New York: Macmillan. Lorenz, K. ( 1963). Dus sagenannte BBse. Vienna: Borotha-Schoeler. Lorenz, K . (1965). Uber tierisches und menschliches Verhalten. Aits dem Werdegang der Verhultenslehre. Munich: Pieper. Lynn, R. (1966). Attention. arousal, and the orienting rej1e.r. Oxford: Pergamon. Mackay, D. M. (1972). Formal analysis of communicative processes. In R. A. Hinde (Ed.), Nonverbal communication (pp. 3-26). Cambridge: Cambridge Univ. Press. MacLean, P. D. (1975). Sensory and perceptive factors in emotional functions of the triune brain. In L. Levi (Ed.), Emotions: Their parameters and measurement. New York: Raven. Marler, P. (1965). Communication in monkeys and apes. In 1. DeVore (Ed.), Primate behavior (pp. 544-584). New York: Holt. Marler, P. ( 1977). Development and learning of recognition systems. Dahlem Konj: Life Sci. Res. Rep. 5, 77-96. Marler, P. (1984). Animal communication: Affect or cognition? In K . R. Scherer & P. Ekman (Eds.), Approaches to emotion (pp. 345-368). Hillsdale, N.J.: Erlbaum. Marler, P.. & Tenaza, R. (1977). Signaling behavior of apes with special reference to vocalization. In T. A. Sebeok (Ed.), How animals communicate (pp. 965- 1033). Bloomington, Ind.: Indiana Univ. Press. Maynard Smith, J. (1972). On twdufion. Edinburgh: Edinburgh Univ. Press. Morris, D. (1957). “Typical intensity” and its relation to the problem of ritualization. Behaviour 11, 1-12. Morton, E. S. (1977). On the occurence and significance of motivation-structural rules in some bird and mammal sounds. Am. Nut. 111, 855-869. Mundinger, P. C. (1970). Vocal imitation and individual recognition of finch calls. Science 168, 480-482. Negus, V. E. (1949). The compurutive unatomv and physiology of the latynx. London: Heinemann. Ohala, J . J . (1980). The acoustic origin of the smile. J . A C U U SSoc. ~ . Am. 68, 33. (Abstr.) Piaget, J . (1981). Intelligence and affectivity: Their relationship during child development. Annu. Rev. Monogr., Palo Alto, Calif. Piderit, T. ( 1858). Grundzuge der Mimik rrnd Phvsiognomik. Braunschweig: Vieweg. Ploog. D. ( I 974). Die Sprache der Afen und ihre Bedeurung fur die Verstandigungsweisen des Menschen. Munich: Kindler. Plutchik, R. ( 1980). Emotion; A psychoevolutionar~~ svnthesis. New York: Harper. Plutchik, R., & Kellennan. H. (Eds.). (1980). Emotion. Theory. research, and experience: Vol 1 . Theories of emotion. New York: Academic Press. Pribram, K . H. (1984). Emotion: A neurobchavioral analysis. In K . R . Scherer & P. Ekman (Eds.), Approaches to emotion (pp. 13-38). Hillsdale, N . J.: Erlbaum.

242

KLAUS R . SCHERER

Redican, W. K . (1982). Facial displays of emotion by monkeys and apes: An evolutionary perspective on human facial displays. In P. Ekman (Ed.), Emotion in the human face (2nd ed., pp. 212280). Cambridge: Cambridge Univ. Press. Robinson, B. W. (1972). Anatomical and physiological contrasts between human and other primate vocalizationa. In S. L. Washburn & P. Dolhinow (Eds.), Perspectives on human evolufion (pp. 438-443). New York: Holt. Robinson, J . G. (1982). Vocal systems regulating within-group spacing. In C. T. Snowdon, C. H. Brown, & M. R . Petersen (Eds.), Primate communication (pp. 94-1 16). Cambridge: Cambridge Univ. Press. Rowell, T. E., & Hinde, R. A. (1962). Vocal communication by the rhesus monkey. Proc. Zool. Soc. London 2, 279-294. Sawashima, M., & Hirose, H. (1983). Laryngeal gestures in speech production. In P. F. MacNeilage (Ed.), The production of speech (pp. 11-38), New York: Springer. Scherer, K . R. (1974). Acoustic concomitants of emotional dimensions: Judging affect from synthesized tone sequences. In S. Weitz (Ed.), Nonverbal communication (pp. 105-1 I I ) . New York: Oxford Univ. Press. Scherer, K . R. (1977). Affektlaute und vokale Embleme. I n R . Posner & H. P. Reinecke (Eds.), Zeichenprozesse-Semiotische Forschung in den Eirizelwissenschaften (pp. 199-214). Wiesbaden: Athenaion. Scherer, K. R. (1979a). Nonlinyuistic vocal indicators of emotion and psychopathology. In C. E. Izard (Ed.), Emotions in personality and psychopathologv (pp. 493-529). New York: Plenum. Scherer, K. R. (1979b). Personality markers in speech. In K. R. Scherer & H. Giles (Eds.), Social markers in speech (pp. 147-209). Cambridge: Cambridge Univ. Press. Scherer, K . R. (1979~).Nonlinguistic vocal indicators of emotion and psychopathology. In C. E. Izard (Ed.), Emotions in personality and psychopathology (pp. 493-529). New York: Plenum. Scherer, K . R. (1981a). Vocal indicators of stress. In J . Darby (Ed.), Speech evaluation inpsychiatry (pp. 171-187). New York: Grune & Stratton. Scherer, K . R. (1981b). Speech and emotional states. In J . Darby (Ed.). Speech evaluation in psychiatry (pp. 189-220). New York: Grune & Stratton. Scherer, K . R. ( 1 9 8 1 ~ ) .Wider die Vernachlassigung der Emotion in der Psychologie. In W. Michaelis (Ed.), Bericht Uber den 32. Kongress der Drutschen Gesellschufifur Psychologie in Zurich 1980. Gottingen: Hogrefe. Scherer, K . R. (1982a). Methods of research on vocal communication: Paradigms and parameters. In K . R. Scherer & P. Eknian (Eds.), Handbook of methods in nonverbal behavior research (pp. 136- 198). Cambridge: Cambridge Univ. Press. Scherer, K. R. (1982b). The assessment of vocal expression in infants and children. In C. E. Izard (Ed.), Measuring emotions in icfanfs and children (pp. 127- 163). Cambridge: Cambridge Univ. Press. Scherer, K . R. (Ed.) (1982~).Vokale Komrnunikarion: Nonverbale Aspekte des Sprachverhaltms. Weinheim: Beltz. Scherer, K . R. (l983a). Prolegomina zu einer Taxonomie affektiver Zustande: Ein KomponentenProzess-Modell. In G. Liier (Ed.), Bericht uber den 33. Kongress der Deutschen Gesellschaji fur Psychologie in Muinz. 1982 (pp. 415-423). Gottingen: Hogrefe. Scherer, K . R. (1983b). Coding the components of affective stares: A,facef approach. Unpublished manuscript. Scherer, K . R. (l984a). On the nature and function of emotion: A component process approach. In K . R. Scherer & P. Eknian (Eds.), Approaches to emotion (pp. 293-318). Hillsdale, N.J.: Erlbaum.

VOCAL AFFECT SIGNALING

243

Scherer. K . R. ( 1984b). Toic~rrrcl( I clynunzic theory of emotion: The component process model qf ufective states. Unpublished nianuscript. Scherer, K . R. ( 1 9 8 4 ~ )Component . pattcwing of ~ ~ o aflect c d expression. Unpublished manuscript. Scherer, K . R. & Oshinsky. J . (1977). Cue utilization in emotion attribution from auditory stimuli. Motivrrt. Emotion 1, 33 1-346. Scherer, K . R., Summerfield, A. B., & Wallbott. H. G . (1983). Cross-national research on antecedents and components of emotion: A progress report. Social Sci. /nf. 22, 355-385. Scherer, U., Helfrich, H.. & Scherer, K . R. (1980). Internal push or external pull‘? Determinants of paralinguistic behavior. In H. Giles, P. Robinson. & P. Smith (Eds.). Language: Socialpsychological perspectives (pp. 279-282). Oxford: Perganion. Schneirla, T. C. ( 1959). An evolutionary and developmental theory of biphasic processes underlying approach and withdrawal. Nehr. Symp. Motivat. 7, 1-42. Bloomington, Ind.: Indiana Univ. Press. Sebeok, T. A. (Ed.) (1977). How unimu1.s c~~tni~iiriii~~~rti~. Seligman, M. E. P. ( 1975). Helplessness: On depression. development and death. San Francisco: Freeman. Seyfdrth, R. M., & Cheney, D. L. (1982). How monkeys see the world: A review of recent research on East African vervet monkeys. In C. T. Snowdon, C. H. Brown, & M. R. Petersen (Eds.), Primate communication (pp, 239-252). Cambridge: Cambridge Univ. Press. Siegman, A. W. (1978). The telltale voice: Nonverbal messages of verbal communication. In A. W. Siegnian & S. Feldstein (Eds.), Nonverbal behavior and communication (pp. 183-243). Hillsdale, N. J . : Erlbauni. Smith, W. I. (1977). The behavior ofcommunicuring. Cambridge: MA: Harvard Univ. Press. Smith, W. J . (1984). Sources of flexibility in communicating. In G. Zivin (Ed.), The de\~elopmentof expressive behavior biolog~-errivirontnenr interactions. New York: Academic Press. Snowdon, C. T . (1982). Linguistic and psycholinguistic approaches to primate communication. In C . T . Snowdon, C. H. Brown, & M. R. Petersen (Eds.), Primuti~communication (pp. 212-238). Cambridge: Cambridge Univ. Press. Snowdon, C. T.. Brown, C. H . , & Petersen, M. R. (Eds.) (1982). Primate communication. Cambridge: Cambridge Univ. Press. Sroufe, L. A. (1979). Socioemotional development. In J . D. Osofsky (Ed.), The handbook of infant development (pp. 462-5 16). New York: Wiley. Steklis, H. D., & Raleigh, M. J . (Eds.) (1979). Neurobiologv ofsocial communication in primates. New York: Academic Press. Tembrock. G . ( I97 I ). Biokommunikation: lrlJorinationsuhertragung im biologischen Bereich (Pt. 2). Berlin: Akademie-Verlag. Tembrock, G. (1975). Die Erforschung des tierlichen Stimmausdrucks (Bioakustik). In F. Trojan (Ed.), Biophone/ik. Mannheini: Bibliogr. Institut. Tinbergen. N. (1952). “Derived” activities: Their causation. biological significance, and emancipation during evolution. Q. Rev. Biol. 27, 1-26. Tinbergen, N. (1959). Comparative study of the behavior of gulls: A progress report. Behaviour 15, 1-70. Tobacb, E. (1970). Some guidelines to the study of the evolution and development of emotion. In L. R. Aronson, E. Tobach, D. S. Lehrman, & J . S. Rosenblatt (Eds.), Development and evolution of behavior: Essays in memory of‘ T. C. S h e i r l u (pp. 238-253). San Francisco: Freeman. Toller, C.. van (1979). The nervous boclv: A n introduction t o the uutonornic nervous svstem and behaviour. New York: Wiley. Tomkins, S . S. (1962). Affect. imagerv. consciousness: Vol. I . The positive uffects. New York: Springer.

Tomkins, S . S . (1963). Aflecr, imagery, consciousness: Vol. 2. The negative affects. New York: Springer. Trojan, F. (1975). Biophonetik. Zurich: Bibliogr. Institut. Trojan, F., & Winckel, F. (1957). Elektroakustische Untersuchungen zur Ausdruckstheorie der Sprechstimme. Folia Phoniat. 9, 168-182. Williams, C. E . , & Stevens, K. N . (1972). Emotions and speech: Some acoustical correlates. J . Aroust. Soc. Am. 52, 1238-1250. Williams, C. E., & Stevens, K. N . (1981). Vocal correlates of emotional states. In J. K. Darby (Ed.), Speech evaluation in psychiatry (pp. 221-242). New York: Grune & Stratton. Zahavi, A. (1982). The pattern of vocal signals and the information they convey. Eehaviour 80, 1-8. Zahavi, A. (1983). The theory of signal selection and some of its implications. Unpublished.

ADVANCES IN THE STUDY OF BEHAVIOR. VOL. I S

A Response-Competition Model Designed to Account for the Aversion to Feed on Conspecific Flesh1 W. J . CARRA N D DARLENE F. KENNEDY DEPARTMENT OF PSYCHOLOGY BEAVER COLLEGE GLENSIDE, PENNSYLVANIA

Introduction .............................................. The Aversion by Norway Rats to Feed on Conspecific Flesh A. The Demonstrational Experiment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B . Research Methods.. . . . . . . . . . . . . . . . . . . C. Sensory Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Motivational Factors . . . . . . . . . . ................. E. Ontogeny.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . F. Phylogeny . . . . . . . . . . . . . . . . . ...................... 111. A Response-Competition Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Central Tenet.. . . . . . . . . . . . ...................... B. Other Assumptions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Evaluation.. . . . . . . . . . . . . . . . ....................... IV. Constraining Intraspecific Predation v se-Competition . . . . . . . . . . References . . . . . . . . ................................. 1. 11.

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INTRODUCTION

In recent years, a great deal of laboratory research has been devoted to the study of experimentally induced food aversions (Barker, Best, & Domjan, 1977; Milgram, Krames, & Alloway, 1977). Typically, animals come to reject an initially attractive food item, because its ingestion was paired with a malaiseinducing agent. Such acquired food aversions have been demonstrated under field conditions (Gustavson, 1977) and the experimental procedures used to induce them probably simulate events occurring in nature rather closely. Nevertheless, their demonstration requires some human interference. 'The subject matter of this article and several of the experiments reported may be repellent and objectionable to many readers. The editors believe, however, that it is a legitimate subject for study though not all of the methods are approved by all of the editors.

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The present article is concerned with a second and rather different kind of food aversion-one that requires no special experimental procedures because it occurs quite spontaneously in many species living in their natural environment as well as under laboratory conditions. We refer to the tendency by many scavengers to treat a dead conspecific as suboptimal food, sometimes rejecting it entirely, especially if the carcass is that of an adult, dead only for a short time (Bo2kov, 1968; Polis, 1981). Moreover, we will show that this naturally occurring food aversion is acquired in the sense that it develops during the course of the primary socialization process, at least in Norway rats and probably in many other flesh-eating species as well. Indeed, it seems safe to say that the tendency by flesh eaters to reject their own dead as food ranks among the more common acquired food aversions in nature. Because it is so widespread, this food aversion deserves its own experimental analysis, aimed at identifying its sensory and motivational bases, neural substrate, and ontogeny. Of course, many primitive flesh eaters not only feed on their own dead, but also prey indiscriminately on live conspecifics as well as on nonconspecifics (Fox, 1975; Polis, 1981). But these phenomena merely raise two additional questions concerning the present food aversion. First, during the course of evolution, how did the aversion arise (possibly more than once) and spread across so many taxa? In a world where animal protein is often in short supply, it is not immediately obvious how remaining hungry rather than feeding upon a dead conspecific could possibly raise or even maintain an animal’s inclusive fitness. It would seem more adaptive to recycle the protein within the species rather than permit it to pass on to other species in the food chain. Second, what is the relationship between the present food aversion and an even more powerful constraint in food-getting, i .e., that preventing intraspecific predation? Indeed, in the light of current thinking about “selfish genes,” some explanation is required to account for the evolution of the constraint against intraspecific predation itself (Dawkins, 1976, pp. 89-90; Fox, 1975; Polis, 1981). Interest in these two major constraints on food getting is not new (Buffon, 181 1, pp. 207-212; Schiff, 1860; Sherrington, 1900), and it persists today (Fox, 1975; Polis, 198I). But these constraints or general rules governing food-getting are recognized mostly “in the breach.” Many workers seem to take the general rules for granted and invoke special explanations for exceptions to them, e.g., extreme deprivation or pathology (Lorenz, 1970b, p. 94; Young, 1936, p. 108). While preparing this review, we read about 150 publications in which passing reference is made to animals feeding on their own dead, under conditions which make it difficult or impossible to determine the causes of such behavior. In this article we concentrate on those publications that describe attempts to identify experimentally the proximate or ultimate causes (Mayr, 1974) of the present food aversion because we wish to focus attention on the general rule

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(i.e., reject conspecific flesh as food) rather than on the occasional exceptions to that rule. Others have expressed similar views (e.g., Dawkins, 1976, pp. 89-90; Harris, 1979; Polis, 1981). Moreover, we are concerned primarily with the aversion by animals to feed on dead adult conspecifics. For recent reviews of the literature on infanticide and infantophagia see Dickeman (1975), Hrdy (1979), and vom Saal and Howard (1982). Apart from its own intrinsic interest, research on the present food aversion may also uncover important similarities and differences between this naturally occurring aversion and the malaise-induced aversions referred to earlier. Further, research on this food aversion may shed additional light on the interdependence of two major classes of behavior-sociality and food getting (Galef, 1977; Kuo, 1967, Chap. 3; Rozin, 1977). Finally, the experimental analysis of the present food aversion using animals may provide a useful perspective in which to view the current controversy among anthropologists concerning the ecological vs cultural determinants of cannibalism* among humans (Harner, 1977; Harris, 1977, Chap. 9; Price, 1978; Sahlins, 1983). The plan of this article is as follows. First, we summarize the findings from 12 years of research conducted in this laboratory on the aversion by Norway rats to feed on conspecific flesh. We believe ours to be the only sustained experimental analysis of this food aversion in any species, designed to explicate its sensory and motivational bases, neural substrate, ontogeny , and phylogeny. Second, we propose a response-competition model that is congruent with much of our experimental findings on the food aversion in rats. Third, we offer some tentative suggestions concerning the functional relationship between the present food aversion and the constraint against intraspecific predation. Briefly, the model assumes that so long as a dead animal retains the speciesspecific signal mediating species recognition, the carcass tends to evoke social responses in live conspecifics, and that these responses compete with and sometimes inhibit feeding behavior. In accord with the views of MacLean (1978, p. 325), the model also assumes that the present food aversion evolved conconiitantly with mammalian social patterns. Moreover, the aversion emerges in each developing animal during the primary socialization process (Scott, 1958, pp. 116- 118, 1967), and as the animal gains experience with its own body. Finally, 2We avoid the term, cannibalism, because its disparate usage by others subsumes several classes of feeding behavior, the determinants of which may differ (Boikov, 1968; Johnson, 1972. pp. 21-23). Most workers apply the term to cases in which animals feed on dead conspecifics, whatever the cause of death, but some use it as a substitute for intraspecific predation (Fox, 1975; Polis, 1981). Some limit the tern1 to cases where animals prey on conspecifics of the same age group, especially in those species (e.g.. certain fishes) where animals regularly prey on smaller conspecifics ( K . D. Carlander, personal communication). Finally, some even apply the term to cases where the predator and prey are of different but closely related species (Barber, 1971, pp. 95-96; Best, 1960; Ditmars, 1937, pp. 2021).

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the model assumes that there is nothing inherently maladaptive about feeding on one's own dead. Rather, the present food aversion represents a minor part of the combined costs associated with mammalian sociality which are more than offset by its combined benefits (Alcock, 1979, pp. 395-400).

11.

THEAVERSION BY NORWAYRATSTO FEEDON CONSPECIFIC FLESH

Feral Norway rats (Ruttus norvegicuu) scavenge almost any kind of animal tissue and prey upon a wide variety of living animals for food (Austin, 1948; Bandler & Moyer, 1970; Bernard, 1974; Gandolfi & Parisi, 1973; Hediger, 1964, p. 113; Herold, 1939; Norman, 1975; O'Boyle, 1974). Yet, contrary to a common misconception, field studies suggest that rats reject their own dead as food, especially during the first day or two following death (Calhoun, 1962, pp. 238-239; Steiniger, 1950). In this section, we describe a technique by which one can demonstrate such an aversion under laboratory conditions, and measure its strength. Then we review the literature on the determinants of the aversion in Norway rats and other species. A.

THEDEMONSTRATIONAL EXPERIMENT

As the expression is used here, an aversion to feed on conspecific flesh is said to occur in a group of hungry animals if most remain hungry rather than feed on conspecific flesh, whereas most feed on comparable nonconspecific flesh rather than remain hungry. Moreover, the difference between the two proportions of feeding serves as a measure of the strength of the aversion (for similar definitions of the term, food aversion, see Hill, 1978; Irwin, 1961; Rozin, 1976). The aversion may also manifest itself in reliably longer latencies to begin feeding on conspecific flesh than to begin feeding on comparable nonconspecific flesh, and in reliably smaller amounts consumed from the former than from the latter. A problem with the technique proposed here is that it requires the use of comparable nonconspecific flesh as a benchmark against which to measure the acceptability of conspecific flesh. Strictly speaking, comparable nonconspecific flesh is that which is identical to conspecific flesh in all respects, except that it comes from a nonconspecific-a requirement seemingly impossible to attain. Fortunately, there is a way to solve the problem, based on the assumption that the aversion to feed on conspecific tlesh is mediated by the same signal mediating species recognition. Later, we will cite evidence supporting this assumption, at least in the case of domestic rats (see Section 11,C). Norway rats exhibit an aversion to feed on conspecific flesh (Carr, Landaver, Wiese, Marasco, & Thor, 1979b). During the first 30 min of a 60-min test, 75%

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of 20 rats remained hungry rather than feed on the intact carcass of a freshly sacrificed adult conspecific. On the other hand, 73% of 1 1 Norway rats fed on the intact carcass of a freshly sacrificed adult roof rat ( R u m s r u m s ) , a congeneric species quite similar to the Norway rat in size and other external characteristics. The Norway rats offered a conspecific carcass also exhibited reliably longer feeding latencies and consumed reliably less tissue than those offered a roof rat carcass. Yet, when the carcasses were permitted to age for 24 hr prior to testing, 67% of 15 Norway rats fed on a dead conspecific, as did 64% of 1 1 Norway rats offered a dead roof rat. Moreover, the latter two groups did not differ reliably with respect to their feeding latencies or amounts of tissue consumed. These and other findings to be presented later (Section II,C) indicate that hungry rats tend to reject a dead conspecific as food so long as the carcass possesses the chemical signal mediating species recognition at or near full strength. But as the carcass ages, this chemical signal dissipates or is masked by other chemical signals associated with decomposition until finally the conspecific and nonconspecific carcasses are equally attractive as food. Thus, a dead conspecific which is relatively unacceptable as food shortly after its death is gradually reduced to unspecified flesh quite suitable for scavenging. We infer, therefore, that a fresh roof rat carcass constitutes comparable nonconspecific flesh because to the Norway rats being tested the essential difference between the two carcasses is that one is recognized as a conspecific and the other is not. Flesh-eating species that tend to reject their own dead as food probably differ with respect to the nature of the signal mediating species recognition. But regardless of its nature, that signal is likely to mediate the present food aversion. Indeed, species recognition may be a prerequisite to the aversion (Roy, 1980, Chap. I ) . B.

RESEARCHMETHODS

The demonstration that Norway rats exhibit an aversion to feed on their own dead opens the way for a thorough experimental analysis of the phenomenon. But first, a more detailed description of our research method is in order. The method has changed somewhat during the 12 years in which we have been engaged in this research program. Currently, it is as follows.

I.

Pretesting Conditions

In most experiments, the subjects are adult male rats (Long-Evans) that are offered a dead male conspecific or a dead male nonconspecific, hereinafter called a donor. The subjects are usually reared from the time of weaning until 3-4 months of age in like-sex groups (two to five per cage) with constant access to lab chow pellets and water. They are maintained in temperature-controlled rooms

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(21-22°C) on a 12:12 hr 1ight:dark cycle. Ten days before testing, pairs of subjects are housed in plastic cages (12 X 22 X 35 cni) and fed lab chow meal for 1 hr per day. The subjects are tested individually in their home cages, their cagemate having been moved to another room shortly before testing. The subjects are usually tested while 23-hr food deprived. In most of the experiments to be described we housed the subjects in pairs prior to testing to minimize isolation-induced stress which can disrupt social behavior in rats and other species (Moyer, 1976, p. 196), and because we felt that they should remain in close contact with a potential food item they would ordinarily reject, i.e., a live adult conspecific. But recently we learned that this precaution is not necessary. Adult rats reared individually from weaning exhibit the same aversion to feed on conspecific donors as do group-reared rats (Carr, Choi, Arnholt, & Sterling, 1983; Carr and Arnholt, 1983).

2. Testing Conditions At the outset of the feeding test which usually lasts for 1 hr, a conspecific or nonconspecific donor is placed on its side in the center of the subject’s cage. From behind a one-way viewing screen located about 80 cm away, we record the subject’s latency to begin feeding and the part of the donor’s body fed upon first. Feeding is said to begin when the subject pierces the donor’s skin or removes a digit and is seen to chew and swallow tissue. We also record whether the subject covers the donor with bedding (Pinel, Gorzalka, & Ladak, 1981) or exhibits filial huddling (Alberts & Brunjes, 1978), here defined as remaining motionless for at least 2 min while in contact with the donor’s body. After the feeding test is completed, the bedding is changed before the subject’s cagemate is returned so that subjects awaiting testing are not exposed to bits of tissue from the donor. In the experiements to be described each subject was tested only once, unless specifically stated otherwise. In some experiments the subjects were offered two donors, one conspecific and one nonconspecific. Two-donor tests can be used to explore the determinants of the present food aversion only after such an aversion has been demonstrated in a one-donor test (see Section 11,A). 3 . Donor Preparation

The donors are sacrificed by a technique said to produce no histological changes in nonpulmonary tissue and only slight pulmonary changes (Keller, 1982; Stevens, Prince, & Cummings, 1977). While still in their home cages, the donors are lowered into a large plastic bag containing 75-85% CO,. They appear to be unconscious within 1 min and are dead within 5 min. When fresh carcasses are used as donors, the elapsed time between their death and the beginning of testing is 10-20 min. The donors are weighed before and after testing to determine the amount of tissue consumed by the subjects. Wounds on the carcass of a dead animal may facilitate feeding by rats (Boice, 1972; Calhoun, 1962, pp. 238-239; Lore &

A V E R S I O N TO FEED O N CONSPECIFIC FLESH

25 1

Luciano, 1977; Paul & Kupferschmidt, 1975; Thor & Flannelly, 1976; D. J . Kelly, personal communication). Therefore, the donors are examined carefully and those with scars are discarded. Rats can identify one another as individuals via olfaction (Carr, Yee, Gable, & Marasco, 1976). Consequently, each subject is offered a donor that had never been housed with that subject. Having described our basic research method in some detail, we now present a review of our findings on the majoi determinants of the present food aversion in Norway rats. These determinants include the aversion’s sensory and motivational bases, ontogeny, and phylogeny. The limited findings on the aversion’s neural substrate are presented in Section lIl,C,3. C.

SENSORY FACTORS

The tendency by hungry Norway rats to reject fresh conspecific donors as food but to accept fresh nonconspecific donors implies that feeding is inhibited by stimuli from the dead conspecific’s body. A series of experiments conducted in our laboratory identified the anatomic source of these stimuli and the sense modality mediating the inhibition.

I.

The Anatomic Source of the Inhibitory Stimuli

The stimuli mediating the present food aversion in Norway rats are confined to the conspecific’s coat, and they do not pervade the interior of the carcass. In a two-donor feeding test, hungry rats offered a freshly sacrificed rat and house mouse fed on the mouse or on neither donor. But rats offered a pair of skinned donors fed indiscriminately, usually on both donors (Carr, Hirsch, Campellone, & Marasco, 1979a). Moreover, in a two-donor test, experimental lesions of increasing size on the coats of rat vs mouse donors gradually attenuated and finally eliminated the tendency to reject conspecific flesh (Carr, Dissinger & Scannapieco, 1982). Hungry Norway rats also fed indiscriminately on an homogenate of internal tissues (i.e., heart, liver, and blood) from freshly sacrificed conspecifics vs roof rats (Carr et al. , 1982), and the presence of the homogenate on the coat of an intact conspecific donor facilitated feeding (Carr, unpublished data)? Finally, Norway rats were less likely to feed on an intact mouse donor that had been smeared with Norway rat urine than on a mouse donor smeared with roof rat urine (Carr et al., 1979b).

2.

The Sense Modality Mediating the Aversion

The tendency by Norway rats to reject their own dead as food is mediated, at least in part, by olfaction. Hungry rats that have been rendered anosmic by ‘Other workers observcd fright reactions in Norway rat5 when presented with fresh conspecific blood, but not when presented with nonconspecific blood (Hornbuckle and Beale, 1974; Stevens and Cerzog-Thomas, 1977). No fright reactions were evident under present testing conditions.

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intranasal infusions of zinc sulfate were more likely to feed on fresh conspecific donors than were control rats receiving applications of physiological saline (Carr et ul., 1979b). Perhaps the zinc sulfate also inactivated the vomeronasal system, a sensory structure which plays an important role in the regulation of social behavior among rodents and other species (Johns, 1979). We do not know whether gustation is also involved in the present food aversion in rats. Taken together, the findings presented in this section suggest that the aversion by Norway rats to feed on their own dead is mediated, at least in part, by the same chemical signal from the dead conspecific’s coat by which rats identify one another as conspecifics. It is as though the conspecific’s coat serves as an envelope providing partial protection for its contents. To be maximally effective, the envelope must be fresh, intact, and free of extraneous stimuli that ordinarily evoke feeding behavior. The stimuli inhibiting feeding behavior do not pervade the interior of the carcass. This last finding stands in sharp contrast with findings reported by others concerning the aversion by domestic dogs to feed on their own dead. Even when quite hungry these animals usually reject conspecific flesh from which the skin has been removed, unless the flesh has been boiled prior to testing (Girden, 1932; Maslow, 1932; Schiff, 1860; Sherrington, 1947, pp. 262263; Wernicke, 1937). D. MOTIVATIONAL FACTORS

In this section, we consider two very different kinds of motivational factors involved in the control of the present food aversion. The first is concerned with the effect of hunger upon the tendency by rats and other mammals to feed on conspecific flesh. The second is concerned with internal events (i.e., mediating responses) that may prompt rats to reject their own dead as food. 1 . The Effect of Hunger in Ruts

As might be expected, the tendency by rats to feed on their own dead increases with the deprivation level of the subjects. Among 20 rats that were 0-hr deprived at the outset of testing, only 10% fed on a freshly sacrificed conspecific within 1 hr, whereas among 20 rats that were 96-hr deprived, 60% fed within I hr. Moreover, the latter group exhibited reliably shorter feeding latencies and consumed reliably more tissue (Carr et a / ., 1979a). The tendency by domestic dogs to feed on chunks of raw conspecific flesh is also deprivation dependent (Girden, 1932; Maslow, 1932; Wernicke, 1937). Interestingly, Girden (1932) reported that some dogs that had rejected conspecific flesh at a low level of deprivation, and accepted it at a higher level, later also accepted it when returned to the original lower level. This finding suggests an interaction between deprivation level and previous feeding experience.

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2.

The Eflect of Hunger in Ruts vs Mice

The strenth of the aversion to feed on conspecific flesh is said to vary across species (Cloudsley-Thompson, 1965, Chap. 6; Errington, 1946). If this could be demonstrated under laboratory conditions then the way would be open for research aimed at exploring the interactions between various experimental manipulations and species differences in the strength of the aversion. When equally food deprived, Norway rats are more likely to reject a dead conspecific as food than are house mice, this being the case in both a singledonor and a two-donor testing situation (Carr, Schwartz, Chism, & Thomas, 1981; Cam et al., 1983). But this species difference may stem from the diminished capacity of mice to cope with deprivation rather than from a relatively

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weak aversion to feed on conspecific flesh, Grecian, Melniczek, Early, and Carr ( 1984) recently completed a test of this hypothesis. In a single-donor feeding test lasting 5 days, domestic rats (Long-Evans) were offered an adult male donor-either a rat or a mouse. In addition, domestic house mice (Swiss-Webster) were offered a male donor-either an adult mouse or a juvenile rat of about the same size as an adult mouse. During the feeding test, some of the subjects in each of the four groups also had access to lab chow and water and some did not. All of the subjects had been reared on a diet said to be appropriate for both rats and mice (i.e., Zeigler Rat and Mouse Chow, RQ 3 1-634). As shown in Fig. 1, most of the rat subjects readily accepted a freshly sacrificed mouse donor as food, but all of the rats rejected a rat donor for at least 4 hr and most rejected their rat donor throughout the 5-day test. Such is the case in rats that had no lab chow or water available during the test (Fig. IB), as well as in those that did (Fig. 1A). These findings provide additional support for the view that rats exhibit an aversion to feed on their own dead, as we define aversion (see Sections II,A and 11,B). House mice behave quite differently under these testing conditions. Among the mice offered lab chow and water during testing, only a small percentage fed on their donor, and they did not differ reliably in their tendency to feed on mouse vs rat donors (see Fig. 2A). Moreover, denying the mice access to lab chow and water greatly increased their tendency to feed on their donor, without affecting their tendency to feed on either type (see Fig. 2B). We infer that house mice do not exhibit an aversion to feed on their own dead. Rather, they show a preference to feed on nonconspecific flesh over conspecific flesh only in a two-donor testing situation (Carr et al., 1982, 1983). Relative to rats, mice also appear to be less avid flesh eaters. They are likely to open and feed upon a dead rodent only if they are hungry (see Fig. 2B). 3 . Mediating Responses

In this section, we describe responses other than feeding made by animals when offered conspecific flesh. These may provide clues to how the animals perceive such flesh, which in turn may help us to understand why they reject it. Sherrington (1900) and Brummer and Theissen (1974) reported that hungry adult dogs reject chunks of raw conspecific flesh with obvious signs of disgust, including curling of the upper lip and wretching responses. Brummer and Theissen (1974) also observed bristling of the dorsal furry coat in six dogs offered a fresh conspecific carcass. Girden ( I 932) and Maslow (1932) reported that hungry dogs usually reject raw conspecific flesh, but they saw no signs of disgust. Kruuk (1972, p. 246) noted that in those rare cases where hyenas feed on their own dead, the rate at which they feed is atypically slow-they may take hours to consume the carcass, whereas they consume a nonconspecific carcass of the

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AVERSION TO FEED O N CONSPECIFIC FLESH

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,

Test Duration (hr) FIG. 2. Percentage of mice feeding on a mouse or rat donor as a function of test duration during 5-day test. (A) Lab chow and water present during test. (B) Lab chow and water absent during test (N = 15-22 per group.)

same size within an hour. Likewise, in reporting two cases of chimpanzees feeding on their own dead, Bygott ( 1 972) observed that their feeding behavior was unlike that directed toward nonconspecific prey. They handled the conspecific carcass tentatively, fed slowly, interrupted feeding frequently, and did not consume the carcass completely. Finally, others have observed signs of disgust in rats offered food items that are inherently unpalatable (e.g., quinine adulterated items) or which have acquired aversive properties because they were paired with malaise (Rozin, 1967; Rozin & Fallon, 1981; P. Rozin, personal communication). The signs of disgust include undue spillage, a gaping response, and redirected feeding, e.g., chewing on inedible objects. All of the above findings suggest the animals recognized conspecific flesh as food, albeit suboptimal. We have never observed the signs of disgust described in the preceding para-

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graph during the many tests of the present food aversion conducted in our laboratory. Among rats and mice, even the rate at which they feed on a rodent carcass (once feeding has begun) does not seem to depend on the donor’s species, i.e., whether it is a rat or a mouse, rather, we see signs of sociality. For example, we have frequently observed that rats are more likely to huddle next to a conspecific donor than a nonconspecific donor (Carr et al., 1983). Rats are also more likely to huddle next to a conspecific donor if it is fresh and intact than if it has been allowed to age prior to testing or if it has been skinned (Carr et al., 1982). Some rats also groom a conspecific donor (Carr, unpublished observations). Mice serving as subjects rarely huddle next to a conspecific donor, but they frequently exhibit tail-rattling which is sometimes followed by full-blown attacks. Some mice groom the donor (Carr et al., 1981). The above mentioned signs of sociality evoked by a conspecific donor suggest that some rats and mice may simply fail to recognize the donor as a potential food item. Others cover the donor, suggesting that they recognized it as suspicious food (Pinel et al., 1981; Steiniger, 1950). Occasionally, rats and mice react to a conspecific donor in a manner suggesting fear. They so position themselves in their cage as to mazimize their distance from the donor and they remain motionless for long periods of time, facing the donor or facing directly away from it. Fleming and Rosenblatt (1974) reported similar responses in virgin female rats when first confronted with live conspecific PUPS.

To sum up, we have observed a variety of preliminary responses made by rat and/or mouse subjects when first they encounter a dead conspecific. These include (1) social responses, e.g., huddling and grooming in rats and intermale aggression and grooming in mice, (2) covering behavior, and (3) indices of fear. Currently, we are attempting to develop better techniques to measure these variables and to explore their interrelations-all in an effort to learn more about their role as potential mediators of the present food aversion.

E. ONTOCENY A major objective of our research program on the aversion by rats and other animals to feed on conspecific flesh has been to explore its ontogeny. This segment of the program has proceeded along four lines, aimed at discovering the effects of an animal’s ( 1 ) previous experience with conspecifics and other animals, (2) previous experience with its own body, (3) dietary history, and (4) observing other conspecifics feeding on their own dead. Each line of research is described below. I.

Previous Social Experience Schiff (1860) reported that among domestic dogs puppies up to about 10 weeks of age readily accept chunks of raw conspecific flesh. But adult dogs

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usually reject such flesh, unless it has been boiled (Brummer & Theissen, 1974; Girden, 1932; Maslow, 1932; Sherrington, 1947, pp. 262-263; Wernicke, 1937). These findings suggest the present food aversion may emerge during the course of the socialization process-some animals may simply avoid feeding on dead members of the species with which they have been reared. Under ordinary circumstances, cohabitants are likely to be conspecifics. To test this hypothesis Carr et a/. (1983) reared Norway rats from early weaning until shortly before testing, each with a single cagemate-either another rat or a house mouse. At 14-16 weeks of age, the subjects were food deprived and given a I-hr feeding test during which they were offered either a mouse or a rat donor. Seventy-four percent of 19 rats reared with another rat fed on their mouse donor but only 31% of 16 rats reared with a mouse fed on their mouse donor. Moreover, the rats reared each with another rat exhibited reliably shorter feeding latencies and consumed reliably more mouse tissue than did the rats each reared with a mouse. We infer that the tendency by domestic Norway rats to reject conspecific flesh stems at least in part from previous experience with other animals. Similar findings were reported for domestic house mice (Potter, 198 I ) , but not for wild house mice (Wuensch, 1983). The findings from two recently completed experiments lend further support to the view that the present food aversion stems ontogenetically from previous social experience with living conspecifics (Carr, Bell, Erlichman, Kleiman, & Messori, unpublished data). Moreover, these experiments demonstrate that having cohabited with a particular type of living conspecific tends to inhibit rats from feeding on a dead conspecific of that type. In the first experiment, 30 juvenile male rats that had been reared from birth until 35-37 days of age with their sire as well as their dam and littermates were less likely to feed on a dead adult male rat than were 34 juveniles that had been reared with their dam and littermates only. The percentages feeding were 23 and 53%, respectively. In the second experiment, 19 adult male rats that had been caged with a dam and her litter for 6-9 days postpartum were less likely to feed on a dead rat pup (aged 69 days) than were 15 adult males that had been caged with an ovariectomized female. The percentages feeding were 0 and 87%, respectively. In both experiments, the particular donor offered as food had never been caged with the subject being tested. Carr et al. (1982) reported that adult male rats feed readily on a dead rat or mouse pup (1-8 days old) but as thc agc of the donor increases adult male rats treat rat donors as increasingly unacceptable food while continuing to accept mouse donors readily. These workers concluded that adult male rats feed indiscriminately on dead rat or mouse neonates because the rat pups lack the characteristic odor mediating species recognition (also see Fujiwara & Ueki, 1979; Gandelman, Zarrow, & Denenberg, 1971; Lobb & McCain, 1978; Rosenblatt, Siegel, & Mayer, 1979). But we suspect that the tendency by adult male rats to

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feed on live or dead neonates stems at least in part from their lack of experience with living neonates. 2.

Own-Body Experience

A majority of hungry rats reared individually with a house mouse not only reject a dead mouse but also reject a dead rat as food (Carr et al., 1983). However, each rat reared individually with a mouse was also exposed to one rat’s body-its own. Therefore, Sterling, DeMarco, and Carr (1983) tested and confirmed the hypothesis that the present food aversion in rats stems from experience with their own bodies. From the time of weaning until testing was completed, these workers reared rats individually, each with a collar about its neck. Some wore a large collar, the outside diameter of which prevented the rat from touching any part of its body with its head, and vice versa. Others wore a small collar that did not prevent head-body contact. Still others wore a large collar only for the 4 weeks immediately preceding testing, as a control for stress; and others wore no collar at all. At 3.5 months of age, all the rats were cyclically food deprived and offered a freshly sacrificed adult rat during a 2-hr test. Feeding was observed in 95% of the 20 rats wearing large collars, but in only 18% of the 17 rats wearing small collars, 6% of the 16 rats wearing collars for 4 weeks, and in 12% of the 16 rats wearing no collars. Those reared from weaning with large collars also exhibited reliably shorter feeding latencies and consumed reliably more tissue than did the rats in the other three groups. Quite clearly, even rats that have been reared individually from weaning until testing exhibit an aversion to feed on their own dead, provided they gained experience with their own bodies. The rats wearing large collars from weaning until testing may have been more stressed than those wearing small collars or no collars at all. But we believe that the rats wearing large collars for only 4 weeks prior to testing provided an adequate control for stress, per se. These controls resisted being collared and attempted to remove them much more than did the experimental rats. The controls were also more active in their home cages in the weeks prior to testing and they were more likely to scratch and bite their caretakers than the experimental rats. Yet the control rats exhibited the typical tendency to reject conspecific flesh. The experiment reported by Sterling et al. (1983) leads us to infer that the aversion by Norway rats to feed on their own dead emerges ontogenetically as the rats gain experience with their own bodies. We believe rats learn via headbody contact that certain things may be sniffed, licked, picked, or scratched, but must not be bitten (Birch, 1956). Somehow the development of these grooming responses prevents rats from feeding on dead conspecifics, even though the potential feeders had been isolated from conspecifics since the time of early weaning. In this connection we note that the rats wearing the large collars from

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weaning did not bite the only living things they had interacted with-their caretakers’ hands.

3. Previous Dietary Experience Intraspecific predation is said to increase in certain invertebrates, fishes, and amphibians that have fed upon congeneric or conspecific prey (Curio, 1976, pp. 189- 191; Polis, 1981). Further, Aschkenasy-Lelu (1967) observed more intermale aggression among rats reared on a diet that included raw beef than among rats reared on the same diet without meat. On the other hand, Slonaker and Card (1922) reported that female rats maintained on a meat-free diet were more likely to consume their young than were females maintained on the same diet augmented three times per week with meat, identified only as table scraps. Therefore part of our research program on the present food aversion has been devoted to exploring the effects of previous dietary experience on the tendency by rats to feed on their own dead. In these experiments, the meat offered to subjects prior to feeding tests consisted of the carcasses of freshly sacrificed rats or mice. Despite Slonaker and Card’s (1922) report that adding meat scraps to an otherwise meat-free diet reduced the tendency by female rats to consume their young, it seems possible that females that are forced to open and feed upon the carcasses of conspecifics as their sole source of food may later treat their own young as food. Carr and Landauer (1 98 1) tested this hypothesis by rearing two groups of females (N = 10 per group) from birth until they weaned their first litter, one receiving commercial lab chow and water and the other receiving intact rat carcasses and water (until they were weaned, both groups of females also had access to their dam’s milk and caecotrophe). When paired with males at 3 months of age, all the females became pregnant and delivered young. One female reared on lab chow killed her entire litter at 17 days postpartum. The remaining females exhibited normal maternal behavior through weaning. These findings indicate that feeding on conspecific flesh as their sole source of food does not potentiate infanticide in female rats. Among others, Kuo (1967, pp. 64-72) demonstrated that the preference by domestic cats and dogs for various food items can be manipulated by previous dietary experience. Therefore it seems possible that male rats reared on a standard diet of commercial lab c h ~but~ which, , ~ on occasion, are permitted to gain experience opening and feeding upon a rat carcass, may acquire a preference to feed upon a dead rat over their standard diet of lab chow. After all, the aversion by rats to feed on their own dead is mediated by the chemical signal from the dead conspecific’s inedible coat: the tissue beneath is readily accepted as food “Commercial lab chow contains meat byproducts as well as plant materials, but the chow is dry, highly processed, and lacks the appearance and texture of fresh animal tissues. It also does nor possess an inedible covering.

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(see Section II,C,l). Therefore, as rats gain experience opening the coat, that response may become simply instrumental to the consummatory act of feeding. Moreover, an acquired preference for conspecific flesh may promote the killing of live conspecifics, especially relatively defenseless pups. To test this hypothesis, Carr and Arnholt (1983) subjected rats to a 7-day feeding cycle that was repeated eight times. For the first 5 days of each cycle, the rats had constant access to lab chow pellets. Throughout the sixth day they were deprived and throughout the seventh day they received a special meal, during which approximately one-third received one of the following: a dead mouse, a dead rat, or lab chow. During succeeding special meals, the proportion of subjects feeding on their dead rat or mouse increased reliably and the latency to begin feeding decreased reliably. We infer that the aversion to feed on conspecific flesh is attenuated as rats gain experience opening and feeding on their own dead. Later, during a two-choice feeding test conducted while the subjects were food deprived, those that earlier had fed intermittently on dead mice reliably preferred to feed first on a dead mouse over lab chow, thus confirming earlier reports by Kuo (1967, pp. 64-72) concerning acquired food preferences. But the subjects that earlier had fed intermittently on dead rats reliably preferred to feed first on lab chow over a dead rat. The subjects reared exclusively on lab chow also preferred to feed first on lab chow over either a dead rat or a dead mouse. Moreover, in a second test during which the subjects were offered either a live mouse or rat pup, 33% killed a mouse and 15% killed a rat pup. But the three groups did not differ reliably in their tendency to kill either mice or rat pups for food. A similar experiment (Carr, Choi, & Sterling, unpublished report) involving mice as subjects yielded comparable results (see Section II,D,l). We infer that feeding intermittently on dead conspecifics neither induces a preference for such flesh nor potentiates intraspecific predation, at least in domestic Norway rats and house mice.

4 . Social Facilitation Under certain conditions, Norway rats are more likely to sample a novel food item if earlier they had observed a conspecific feeding on such an item (Barnett, 1975, pp. 72-73; Calhoun, 1962, p. 86; Steiniger, 1950). Indeed, social facilitation has been shown to occur in rats when the novel food item is one of their own dead (Carr et al., 1979a). Once a day for 14 days some experimental rats were permitted to observe their cagemate feeding on a dead rat while temporarily isolated behind a wire mesh screen. Other control rats observed their cagemate feeding on lab chow. Later, when first offered a dead rat, 80% of the 10 experimental rats fed on their donor within 1 hr, but only 25% of the 8 control rats fed within the same time period. Moreover, the experimental rats exhibited reliably shorter feeding latencies and consumed reliably more tissue than did the

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controls. It is unlikely that the facilitative effect was due to the experimental rats having observed (i.e., seen and smelled) the inaccessible carcasses, per se. An earlier experiment had shown that mere exposure to such stimuli did not potentiate feeding. Rather, the present findings represent another example of imitative foraging (Wilson, 1975, p. 51) akin to that reported by Galef and Clark (1971a,b). The findings summarized in this section reveal that the aversion by Norway rats to feed on conspecific flesh is labile in both directions. In the main, the aversion stems ontogenetically from the animals’ experience with their own bodies (i.e., head-body contact), but experience with other animals (i.e., with nonconspecifics or particular types of conspecifics) also contributes to it. Such experiences tend to elevate the aversion. On the other hand, the aversion is attenuated among rats that have observed other rats feeding on dead conspecifics. Rats also show a slight increase over trials in the proportion feeding on dead conspecifics. Moreover, once they do feed, their latency to begin feeding during succeeding trials decreases and the amount they consume increases (Carr et a l . , 1979a; Carr & Arnholt, 1983). Similar findings have been reported in domestic dogs (Girden, 1932; Maslow, 1932).

F. PHYLOGENY Perhaps the most perplexing question associated with the present food aversion is its phylogeny. Although far from universal, the tendency by hungry flesh eaters to reject conspecific flesh is widespread, especially among mammals (Polis, 1981). But what selection pressures caused this behavioral trait to arise (possibly more than once) and spread across so many taxa? And why, among different species, does the aversion vary from nonexistent to very strong? Finally, what is the relationship between the tendency to reject dead conspecifics as food and the even stronger tendency to reject live conspecifics as prey, especially the young or infirm which are the favorite targets of predators attacking nonconspecifics (Curio, 1976, pp. 113-1 17)? Conceivably, feeding on one’s own dead may be maladaptive. If so, then natural selection would favor those members of a flesh-eating species that possess an inhibitory mechanism which blocks feeding behavior when activated by cues identifying a carcass as that of a conspecific (Errington, 1946; Lorenz, 1970a). But the question remains: precisely what is it about conspecific flesh that renders feeding upon it maladaptive? We have explored four hypotheses designed to answer this question and we find little direct support for any of them, at least in Norway rats.

I.

Is Conspecific Flesh Nutritionally Inadequate?

Some believe that conspecific flesh should be ideal food for flesh eaters, because it consists of the same materials of which the feeder is composed, and in

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the same proportions (Adolph, 1967; Errington, 1967, p. 58; Harris, 1979; Lorenz, 1970a). Yet feeding on one’s own dead may produce subtle, deleterious effects heretofore undetected because so little research has been done on the topic. If so, such deleterious effects should most likely manifest themselves in animals reared exclusively on conspecific flesh during the period of rapid growth from birth to early adulthood. However, Carr and Landauer (1981) found little support for this hypothesis. These workers reported that rats reared for the first 12 weeks of life exclusively on rat carcasses and water (plus their dam’s milk and caecotrophe) weighed only 5.4% less than rats reared on commercial lab chow and water. Among rats 10-12 weeks old, this difference in body weight is equivalent to only about one week’s growth. Viewed in this light, the adverse effect of feeding exclusively on conspecific flesh seems moderate, and an occasional meal on such flesh is likely to be beneficial, relative to remaining hungry. Later, some of the rats reared on rat carcasses were seen to mate and care for their young normally (see Section II,E,3).

2 . Is Conspecific Flesh Tainted? Along with others, Polis (198 I ) hypothesized that the aversion to feed on dead conspecifics may serve to minimize exposure to parasites and pathogens to which the potential feeder might be especially vulnerable by virtue of its close genetic affinity to the conspecific carcass. Polis cited 12 examples where feeding on dead conspecifics forms a possible vector for the transmission of infectious organisms. To date, this hypothesis has not been subjected to empirical test and we know of no way to test it directly.

3. Does Feeding on Conspecific Flesh Potentiate lntraspecific Predation ?

Intraspecific predation is said to increase in certain invertebrates, fishes, and amphibians, if the animals have fed upon congeneric or conspecific prey (Curio, 1976, pp. 189-191; Polis, 1981). Hence the aversion to feed on dead conspecifics may prevent animals from acquiring a taste for such flesh, thereby minimizing intraspecific predation. Especially among mammals, preying on conspecifics is not likely to serve as an evolutionarily stable strategy (Dawkins, 1976, pp. 89-90; Fisher, 1958, pp. 224-227; Wilson, 1975, pp. 128-129). But research reported earlier (Section II,E,3) revealed that feeding intermittently on dead conspecifics neither induces a taste for such flesh nor potentiates intraspecific predation, at least in domestic rats and house mice (Carr et a l . , 1983; Carr, Choi, & Sterling, unpublished report). 4 . Does Conspecific Flesh Taste Bad?

Lorenz (1966, p. 120) believes that some flesh eaters reject dead conspecifics as food simply because “they do not taste good.” But this hypothesis tells us

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little about the adaptive significance of the aversion. Moreover, at least in Norway rats conspecific flesh is quite acceptable-they feed readily on the carcasses of skinned conspecifics. The chemical signal mediating the present food aversion is confined to the dead rat’s furry coat and does not pervade the interior of the carcass (see Section II,C, 1). In this section, we reviewed findings testing the hypothesis that feeding on conspecific flesh is maladaptive for one reason or another, and that the tendency to reject such flesh arose via some inhibitory mechanism that blocks feeding behavior when activated by cues identifying a carcass as that of a conspecific. We find no direct support for this hypothesis in domestic rats or house mice, but it may account for the present food aversion in other flesh-eating species.

111. A RESPONSE-COMPETITION MODEL

In the preceding section, we reviewed four hypotheses that invoke some maladaptive consequence of feeding on conspecific flesh to account for the evolution of the present food aversion. Each of these hypotheses assumes that natural selection favored the development of some inhibitory mechanism that mediates the aversion, but none identifies that mechanism explicitly, and none attempts to account for its ontogeny. In this section we propose an hypothesis which does the opposite, i.e., this hypothesis does not invoke some maladaptive consequence of feeding on conspecific flesh, but it does name the inhibitory mechanism (i.e., response-competition) and it does offer an account of the aversion’s ontogeny. The response-competition model is derived from and is consistent with much of what we have already learned about the aversion by Norway rats to feed on conspecific flesh. A. CENTRAL TENET It is generally recognized that some behavioral traits emerge simply as concomitants of some other critical trait wich confers considerable selective advantage upon its possessors (Krebs & Davies, 198I , Chap. 4; Lorenz, 1970a). For example, the combined benefits derived from mammalian sociality are said to outweigh the combined costs, such as increased competition for limited resources (e.g., food and cover) and increased exploitation by predators, parasites, and pathogens (Alcock, 1979, pp. 395-400). The central tenet of the present model is that the aversion by rats and perhaps other flesh-eating mammals to feed on their own dead represents a minor part of the combined costs associated with sociality. Like MacLean (1978, p. 325), we suggest that the aversion evolved concomitantly with mammalian social patterns. Moreover, we suggest that the aversion emerges in each developing animal

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during the primary socialization process (Scott, 1958, pp. 116-1 18, 1967), and as the animal gains experience with its own body.

B . OTHERASSUMP~IONS Shown schematically in Fig. 3, the model summarizes the interrelations among the aversion’s sensory and motivational bases, neural substrate, ontogeny, and phylogeny. We assume that rats encountering a dead conspecific are exposed to two kinds of external signal, one being the chemical signal mediating species recognition and the other being some unknown signal identifying the

Exter~nal Signal (conspecific)

External Signal (food)

I

Soc ia I Behavior

Feed Behar

System

System

Social Signals Transient

Transient

Excitatory Inhibitory Variable

FIG.3 . Graphic representation of a response-competition model designed to account for the tendency by Norway rats to feed on a conspecific vs a nonconspecific donor (see text for explanation).

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carcass as a potential food item. Further, we assume that the former signal tends to activate a neural control system mediating social behavior while the latter signal tends to activate a different neural control system mediating feeding behavior. Each control system also tends to be modulated by internal signals reflecting relatively transitory drive states (e.g., hunger or fear) as well as more permanent states, including the animal’s memory of previous experience with its own body, with other animals, and with various food items. We also assume that the output of each control system varies directly with the combined intensity of the external and internal signals impinging upon it. Finally, as the term response-competition implies, we assume that the two control systems are mutually inhibitory and that the relative intensities of the signals (both external and internal) impinging upon each system will determine which system will prevail over the other, in a manner similar to other boundary state models (e.g., Fentress, 1973, pp. 205-216, 1976, pp. 151-158).’ It follows from the model’s assumptions that, as young Norway rats develop, stimuli emanating from other rats in their group come to serve as powerful releasers, capable of evoking a variety of social responses, including aggregation, huddling, grooming, play, reproductive activities, and intraspecific aggression. Moreover, the young rats’ own bodies evoke normal grooming responses, e.g., sniffing, licking, scratching-but not biting. Later, when these rats encounter the intact carcass of a freshly sacrificed conspecific, the chemical signal identifying the carcass as that of a conspecific tends to evoke some social responses (e.g., huddling or grooming) and perhaps certain mediating responses (e.g., fear) which compete with and inhibit feeding behavior. On the other hand, Norway rats feed readily on the intact carcass of a freshly sacrificed nonconspecific, because it lacks the chemical signal identifying it as a conspecific and, therefore, evokes no social responses that compete with feeding behavior.

C.

EVALUATION

In this section, we test the model in the light of what we already know about the major determinants of the aversion by rats to feed on conspecific flesh, including its sensory and motivational bases, neural substrate, ontogeny, and phylogeny. We further suggest additional ways in which the model might be tested, using rats and other species that also exhibit the aversion. sWe recognize that this model oversimplifies reality by neglecting other important neural control systems which no doubt exist and interact with the two here mentioned. Nevertheless, such models niay be justified on the grounds that they can be used to summarize a complex set of research findings, as well as to stimulate additional research. Other workers have described similar models to account for the interactions between two or more major classes of behavior (i.e., Gallistel, 1980, pp. 286-287).

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Sensory and Motivational Bases

The model is consistent with research findings summarized earlier in this article concerning the sensory and motivational bases of the present food aversion (see Sections II,C, and 11,D).Rats encountering the intact carcass of a freshly sacrificed conspecific are more likely to engage in social behavior (e.g., huddling or grooming) than feeding behavior, because the external signal identifying the carcass as that of a conspecific is stronger than the external signal identifying the carcass as food. But with the passage of time following death, the former signal dissipates and/or is masked by the increasingly intense external food signal. Therefore feeding behavior gradually replaces social behavior. During this transformation process, the subjects’ tendency to feed on the carcass increases with their level of food deprivation, due to the increase in the intensity of the transient internal signal reflecting hunger. Moreover, rats feed more readily on a freshly sacrificed conspecific if they are unable to detect the chemical signal mediating species recognition, because they are anosmic or because the furry coat from which the signal arises has been removed. Likewise, normal rats feed more readily if an external food signal (e.g., an homogenate of conspecific internal parts) is applied to the intact carcass of a freshly sacrificed conspecific. Additional research on the sensory basis of the present food aversion might involve manipulations of the subjects’ ability to recognize one of their own dead as a conspecific. For example, hungry rats may be more likely to feed on a conspecific donor if the donor has been reared with members of another species (e.g., mice), thus masking the conspecific signal with a nonconspecific signal that ordinarily evokes feeding behavior. A preliminary test of this hypothesis failed (Tousley, Schwartz, & Carr, 1974), but this failure may have resulted from the use of a relatively short feeding test. Additional research on the motivational basis of the present food aversion might involve the use of a tranquilizer to test the model’s prediction that fear serves as a mediating response which inhibits rats from feeding on their own dead. Also, one might compare the feeding behavior of genetically emotional vs nonemotional strains of rats (e.g., Maudsely reactive vs nonreactive rats), as well as genetically obese rats (e.g., Zucker strain) with normals (Caralogue of NIH Rodents, 1973).

2 . Ontogeny The model is also consistent with research findings summarized earlier in this article concerning the ontogeny of the present food aversion (see Section 11,E). The aversion develops as rats gain experience with their own bodies (i.e., headbody contact) and with other animals, e.g., nonconspecifics or particular types

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of conspecifics.6 As shown in Fig. 3, these experiences are treated as enduring internal signals (i.e., memories) that modulate the output of the social control system. On the other hand, the aversion to feed on conspecific flesh decreases as the rats gain experience feeding on such flesh or observe other rats doing so. These experiences are treated as enduring signals that modulate the output of the feeding control system. Additional research on the ontogeny of the present food aversion could involve any experiential manipulation that raises (or lowers) the subjects’ tendency to interact socially with a conspecific donor which should also raise (or lower) the subjects’ tendency to feed on that donor. For example, sexually experienced male rats should be less likely to feed on a receptive female donor than are naive males or prepuberal castrates. On the other hand, sexually experienced males may be more likely to feed on a male conspecific donor than are naive males, because the former type exhibits more intermale aggression than the latter (Flannelly, Blanchard, Muracke, & Flannelly, 1982). Additional research may reveal that subjects’ dietary history influences their tendency to feed on their own dead. Relative to rats reared on commercial lab chow, those reared on a variety of palatable supermarket items tend to overeat and become obese (Sclafani & Gorman, 1977; Simson & Gold, 1982). Rats reared on such a complex diet may also be more likely to feed on conspecific donors than are controls reared on lab chow. 3 . Neural Substrate

Little is known about the neural substrate of the present food aversion. De Ruiter (1967) believes that activation of the neural circuits controlling social behavior tends to inhibit the circuits controlling feeding behavior, and vice versa. But the evidence he offers is largely indirect, i.e., it is behavioral rather than neurological. Anthony and Carr (1983) showed that the ventromedial hypothalamus is not an essential link in the circuits controlling the present food aversion. Therefore, additional research might be better directed toward circuits controlling social behavior, especially those mediating species recognition (Grossman, 1967, p. 533; MacLean, 1973; Pribram & Kruger, 1954; Roy, 1980, Chap. 1). Indeed, although it has yet to be employed, the present food aversion may serve as a useful index by which to probe the CNS for such circuits. In this connection, we note that the external signal mediating species recognition evokes both social hMayr (1974) distinguishes between behavior patterns mediated by neural control systems derived from closed vs open genetic programs. Our response-competition model is compatible with either type of program but, at least in Noway rats, the aversion to feed on conspecific flesh clearly involves an open genetic program.

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behavior and the present food aversion. Finally, since the aversion is acquired experientially, its neural circuitry may be coextensive with that mediating other acquired food aversions (Braun, Lasiter, & Kiefer, 1982). 4. Phylogeny

According to the response-competition model here proposed, the present food aversion evolved concomitantly with mammalian social patterns. Further, it emerges in each developing animal as it gains experience with other animals (usually conspecifics), and with its own body. Therefore, the model’s ability to account for the sensory basis and ontogeny of the aversion (see Sections III,C, 1, and 111,C,2) also provides the causal linkage binding the aversion to the phylogeny of mammalian sociality.

5. Limitations of the Model

The aversion to feed on one’s own dead requires that the potential feeder be able to recognize the carcass as that of a conspecific. But the strength of the aversion may vary even among mammalian species that do not differ in their ability to discriminate between conspecific vs nonconspecific carcasses. Therefore, species recognition may be a necessary but not sufficient condition for the present food aversion. A complete explanation of the aversion would account for differences among species in its strength and our model falls far short of thisperhaps because it does not take into account species differences in (1) the degree and kind of sociality they exhibit, (2) the extent to which they rely upon scavenging animal tissue for survival, and (3) their ability to cope with deprivation. The possible effect of these three factors on the strength of the present food aversion is illustrated by comparing Norway rats with house mice. Members of both species direct social responses toward conspecific donors but not toward nonconspecific donors (see Section 11,D,3), suggesting that they can discriminate between the two types of donor, probably via species-specific chemical signals. In fact, both species are capable of discriminating between the odors from individual conspecifics (Carr et al., 1970, 1976; Colgan, 1983; Halpin, 1980). Yet, Norway rats exhibit a stronger tendency to reject conspecific flesh as food than do house mice (see Section 11,D,2). IV.

CONSTRAINING INTRASPECIFICPREDATION VIA RESPONSE-COMPETITION

We submit that the principle of response-competition mediated by the chemical signal responsible for species recognition can account, at least in part, for the ontogeny and phylogeny of the tendency by Norway rats to reject their own dead as food. Response-competition may also account for the present,food aversion in

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other species, regardless of the nature of the signal mediating species recognition. Indeed, the principle of response-competition may even account for the tendency by rats and other animals (including humans) to reject live conspecifics as prey, as well as the tendency to reject dead ones as food. The former tendency is likely to be stronger than the latter, because live conspecifics can resist predatory attack-dead ones cannot resist being scavenged. Nevertheless, the two constraints may prove to be simply different facets of a single general rule observed by flesh-eating mammals, i.e., all food-getting activities should be directed to animals other than one’s own kind. If a number of experimental manipulations were to affect them in the same manner (i.e., inhibit or facilitate them), this would imply that the two constraints are functionally equivalent, thereby permitting the response-competition model to address both. At least three manipulations are already known to affect both constraints in the same manner. First, increasing deprivation level raises the tendency by rats to feed on a dead adult rat and to kill a rat pup (Carr et a/., 1979a; Paul & Kupferschmidt, 1975). Second, rendering rats anosmic facilitates feeding on a dead adult rat and killing a rat pup (Carr et al., 1979b; Myer, 1964). Third, rearing rats with mice inhibits rats from feeding on a dead mouse and killing a live one (Carr et al., 1983; Myer, 1964). Others interested in intraspecific predation as a way of life have commented on its frequency. Dawkins (1976, p. 89) wonders why it is so rare. But Polis (1981) contends that this is the wrong way to pose the question. He believes that we should ask why it is so common, especially among the invertebrates. If forced to choose between the two, we stand with Dawkins. Given his concept of “selfish genes” and the widespread rejection of good-of-the-species reasoning, it is not immediately obvious why many flesh eaters reject dead conspecifics as food and live ones as prey, especially the young or infirm which are favorite targets of predators attacking nonconspecifics (Curio, 1976, pp. 113-1 17). But we would put the basic question differently. Like Wilson (1971), we ask: what set of genetic factors and ecological circumstances favors intraspecific predation as a way of life?

Acknowledgments We thank Dr. Lia Annos for help during the initial phase of this research and Jean C a n for considerable technical assistance throughout the program. We also thank Pamela Chiartas who prepared the figures in this paper and Dr. David R. Peardon who supplied the roof rats. Portions of this research were supported by research Grants MH24546, HD07043, and MH30365 from the Department of Health, Education, and Welfare, and by a research grant from the Rohm and Haas Company

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References Adolph, E. F. (1967). Critic’s comments. In “The Chemical Senses and Nutrition” (M. R. Kare and 0. Maller, eds.), pp. 181-183. John Hopkins Press, Baltimore. Alberts, J . R., & Brunjes, P. C. (1978). Ontogeny of thermal and olfactory determinants of huddling in the rat. J . Comp. Physiol. Psychol. 92, 897-906. Alcock, J . (1979). “Animal Behavior,” 2nd ed. Sinauer, Sunderland, Massachusetts. Anthony, S. L., & Carr, W. J . (1983). A natural food aversion in rats rendered hyperphagic by hypothalamic knife cuts. Bull. Psychon. Soc. 21, 301-302. Aschkenasy-Lelu, P. (1967). Consequences de rkgimes carnks chez le rat 11. Action sur diffkrents aspects du comportment. Arch. Sci. Physiol. 21, 91-1 13. Austin, 0. L. (1948). Predation by the common rat (Rattus norvegicus) in the Cape Cod colonies of nesting terns. Bird Banding 19, 60-65. Bandler, R., Jr., & Moyer, K. E. (1970). Animals spontaneously attacked by rats. Comm. Behav. Biol. 5, 177-182. Barber, C . (1971). “Animals at War.” Harper and Row, New York. Barker, L. M., Best, M. R., & Domjan, M. (eds.). (1977). “Learning Mechanisms in Food Selection.” Baylor Univ. Press, Waco, Texas. Barnett, S. A. (1975). “The Rat,” 2nd ed. University of Chicago Press, Chicago. Bernard, B. K. (1974). Frog killing (ranicide) in the male rat: Lack of effect of hormonal manipulations. Physiol. Behav. 12, 405-408. Best, J . B. (1960). Diurnal cycles and cannibalism in planaria. Science 131, 1884-1885. Birch, H. G. (1956). Sources of order in the maternal behavior of animals. Am. J . Orthopsychiat. 26, 279-284. Boice, R. (1972). Some behavioural tests of domestication in Norway rats. Behaviour 42, 198-23 1. Botkov, D. K. (1968). Essai de catkgorisation de phknomtne cannibalisme chez le monde animal avec quelques notes sur son importance biologique. Bulg. Akad. Nauk.. Izv. Zoo/. Inst. Soj: 27, 81-101.

Braun, J . J . , Lasiter, P. S., & Kiefer, S . W. (1982). The gustatory neocortex of the rat. Phvsiol. P.y.vchol. 10, 13-45. Brummer, H., & Theissen, U. (1974). Beobachtungen iiber Kannibalismus beim Hund. Dtsch. Tierarzd. Wochenschr. 81, 88-90. Buffon, 0. G. L. (181 1). “Natural History, Vol. VI.” Law and Gilbert, London. Bygott, D. (1972). Cannibalism among wild chimpanzees. Nature (London) 238, 410-41 1. Calhoun, J . B. (1962). “The Ecology and Sociology of the Norway Rat.” Public Health Service Publication No. 1008. U.S. Department of Health, Education, and Welfare, Bethesda, Maryland. Cam, W. J . , & Arnholt, E. (1983). The effect of diet on a natural food aversion in Norway rats (Rattus norvegicus). Nutr. Behav. 1, 223-231. Carr, W. J . , Choi, S . Y ,, Arnholt, E., & Sterling, M. H. (1983). The ontogeny of a natural food aversion in domestic rats (Rattus norvegicus) and house mice (Mus musculus). J . Comp. Psycho/. 97, 260-268. C a r , W. J . , Dissinger, M. L., & Scannapieco, M. R. (1982). The stimulus-basis of a natural food aversion in Norway rats and house mice. Phvsiol. Behav. 28, 281-287. Carr, W. J . , Hirsch, J . T . , Campellone, B. E., & Marasco, E. (1979a). Some determinants of a natural food aversion in Norway rats. J . Comp. Physiol. Psychol. 93, 899-906. Carr, W. J., & Landauer, M. R. (1981). Growth rate and behavior of Norway rats reared on conspecific flesh. Bull. Psychon. Sor. 18, 224-226. Carr, W. I . , Landauer, M. R., Wiese, R. E., Marasco, E., & Thor, D. H. (1979b). A natural food aversion in Norway rats. J . Comp. Physiol. Psychol. 93, 574-584.

AVERSION TO FEED ON CONSPECIFIC FLESH

27 1

Carr, W. J.. Martorano, R. D., & Krames, L. (1970). Responses of mice to odors associated with stress. J . Comp. Physiol. Psychol. 71, 223-228. Carr, W. J., Schwartz, D., Chism, E., &Thomas, B. (1981). A natural food aversion in Norway rats and house mice. Behav. Neur. Biol. 31, 314-323. Carr, W. J., Yee, L., Gable, D., & Marasco, E. (1976). Olfactory recognition of conspecifics by Norway rats. J . Comp. Physiol. Psychol. 90, 821-828. Catalogue of NIH Rodents: Strains and Stocks of Laboratory rodents and rabbits provided by the NIH Laboratory Animal Genetic Center. (1973). National Institutes of Health, Bethesda, Maryland. (DHEW Publication No. (NIH) 74-606). Cloudsley-Thompson, J. L. (1 965). “Animal Conflict and Adaptation.“ Dufour, Chester Springs, Pennsylvania. Colgan, P. (1983). “Comparative Social Recognition.” Wiley, New York. Curio, E. (1976). “The Ethology of Predation.” Springer-Verlag. New York. Dawkins, R. (1976). “The Selfish Gene.” Oxford University Press, New York. De Ruiter, L. (1967). Feeding behavior of vertibrates in the natural environment. In “Handbook of Physiology, Section 6: Alimentary Canal, Volume I, Control of Food and Water Intake” (C. F. Code, ed.), pp. 97- 116. American Physiological Society, Washington. Ditrnars, R. L. (1937). “Snakes of the World.” Macmillan, New York. Dickeman, M. (1975). Demographic consequences of infanticide in man. Annu. Rev. Ecol. SYs. 6 , 107- 137. Errington, P. L. (1946). Predation and vertebrate populations. Q.Rev. Biol.21, 144-177, 221-245. Errington, P. L. (1967). “Of Predation and Life.” Iowa State Univ. Press, Ames, Iowa. Fentress, J. C. (1973). Specific and nonspecific factors in the causation of behavior. In “Perspectives in Ethology” (P. P. G. Bateson and P. H. Klopfer, eds.), pp. 205-216. Plenum Press, New York. Fentress, 1. C. (1976). Dynamic boundries of patterned behavior: interactions and self-organization. In “Growing Points in Ethology” (P. P. G. Bateson and R. A. Hinde, eds.), pp. 151-158. Cambridge Univ. Press, Cambridge. Fisher, R. A. (1958). “The Genetical Theory of Natural Selection.” Dover, New York. Flannelly, K. J., Blanchard, R. J . , Muraoka, M. Y., & Flannelly, L. (1982). Copulation increases offensive attack in male rats. Physiol. Behav. 29, 381-385. Fleming, A. S . , & Rosenblatt, J. S. (1974). Olfactory regulation of maternal behavior in rats: 11. Effects of peripherally induced anosmia and lesions of the lateral olfactory tract in pup-induced virgins. J . Comp. Physiol. Psyrhol. 86, 233-246. Fox, L. R. (1975). Cannibalism in natural populations. Annu. Rev. Ecol. Svs. 6 , 87-106. Fujiwara, M.. & Ueki, S. (1979). The course of aggressive behavior induced by a single injection of delta-tetrahydrocannabinol and its characteristics. Physiol. Behav. 22, 535-539. Galef, B. G . , Jr. (1977). Social transmission of food preferences: An adaptation for weaning in rats. J . Comp. Physiol. Psychol. 91, 1 136- I 140. Galef, B . G., Jr., & Clark, M.M. (1971a). Parent-offspring interactions determine time and place of first ingestion of solid food by wild rat pups. Psvchon. Sci. 25, 15-16. Galef, B. G . , Jr., & Clark, M. M. (1971b). Social factors in the poison avoidance and feeding behavior of wild and domesticated rat pups. J . Comp. Phvsiol. Psychol. 75, 341-357. Gallistel, C. R. (1980). “The Organization of Action: A New Synthesis.” Hillsdale, New Jersey: Erlbaum. Gandelman, R., Zarrow, M. X . , & Denenberg, V. H. (1971). Stimulus control of cannibalism and maternal behavior in anosmic rats. Physiol. Behav. 7 , 583-586. Gandolfi, G . , & Parisi, V. (1973). Ethological aspects of predation by rats, Raftus norvegicus (Berkenhout), on bivalves Unio pictorum L. and cerasroderma Lamarcki (Reeve). Boll. Zool. 40. 69-74.

27 2

W . .I.CARR A N D DARLENE F . KENNEDY

Girden, E. S . (1932). Cannibalism in dogs. J . Comp. Psycho/. 14, 409-413. Grecian, P., Earley, P., Melniczek, J . , & Carr, W. J. (1984). The c#ect of’ deprivation on the tendency bv domestic rats and house mice to ,feed on conspec$c,flesh. Paper presented at the meeting of the Eastern Psychological Association, Baltimore, Maryland. Grossman, S . P. (1967). “A Textbook of Physiological Psychology.” Wiley, New York. Gustavson, C. R. (1977). Comparative and field aspects of learned food aversions. In “Learning Mechanisms in Food Selection” (L. M. Barker, M. R . Best. and M. Donijan. eds.), pp. 23-43. Baylor University Press, Waco, Texas. Halpin, Z. T. ( 1980). Individual odors and individual recognition: Review and commentary. Biol. Behav. 5 , 233-248. Harner, M. (1977). The ecological basis of Aztec sacrifice. A m . Ethnol. 4, 117-135. Harris, M. (1977). “Cannibals and Kings.” Random House, New York. Harris, M. (1979). Our pound of flesh. Not. Hist. 88(2), 30-36. Hediger, H. (1964). “Wild Animals in Captivity.” Dover, New York. Herold, W. (1939). Neure Beobachtungen iiber das Wanderratte (Epimysnorvegicus Exrl.). Ces. Vorratsschutz . 15, 22- 24. Hill, W. F. (1978). Effects of mere exposure on preferences in nonhuman mammals. Psycho/. Bull. 85, 1177-1199. Hornbuckle, P. A., & Beale, T. (1974). Escape reactions to the blood of selected mammals by rats. Behav. B i d . 12, 573-576. Hrdy, S . F. (1979). Infanticide among animals: A review. classification, and examination of the implications for reproductive strategies of females. Ethol. Sociohiol. 1, 13-40, Irwin, F. W. (1961). On desire, aversion, and the affective zero. Psycho/. Rev. 68, 293-300. Johns, M. A. (1979). The role of the vomeronasal system in mammalian reproductive physiology. In “Chemical Signals: Vertebrates and Aquatic Invertebrates” (D. Muller-Schwarze and R . M. Silverstein. eds.), pp. 341-364. Plenum Press, New York. Johnson, R. N. (1972). “Aggression in Man and Animals.” Saunders, Philadelphia. Keller, G. L. (1982). Physical euthanasia methods. Lab Animal 11(4), 20-26. Krebs, J. R . , & Davies, N. B. (1981). “An Introduction to Behavioural Ecology.” Sinauer, Sunderland, Massachusetts. Kruuk, H. (1972). “The Spotted Hyena.” University of Chicago Press, Chicago. Kuo, Z-Y. (1967). “The Dynamics of Behavior Development.” Random House, New York. Lobb, M.. & McCain. G . (1978). Population density and nonaggressive competition. Anim. Learn. Behav. 6 , 98-105. Lore, R., & Luciano, D. (1977). Attack stress induces gastrointestinal pathology in domesticated rats. Phvsiul. Behav. 18, 743-745. Lorenz, K . (1966). “On Aggression.” Harcourt, New York. Lorenz, K . (1970a). On killing members of one’s own species. Bull. Atom. Scient. 26(8), 2-5, 5 I 56. Lorenz, K. (1970b). “Studies in Animal and Human Behavior, Vol. I . ” Harvard Univ. Press, Cambridge. MacLean, P. D. (1973). “A Triune Concept of the Brain and Behavior.” Univ. of Toronto Press, Toronto. MacLean, P. D. (1978). A mind of three minds: Educating the triune brain. In “Seventy-Seventh Yearbook of the National Society for the Study of Education, Part 11” (J. S . Chall and A. F. Mirsky, eds.). pp. 308-342. Univ. of Chicago Press, Chicago. . Psycho/. 14, 401-407. Maslow, A. H. (1932). The “emotion” of disgust in dogs. .IComp. Mayr, E. (1974). Behavior programs and evolutionary strategies. A m . Scient. 62, 650-659. Meyer-Holzapfel, M. (1968). Abnormal behavior in zoo animals. In “Abnormal Behavior in Animals” (M. W. Fox, ed.), pp. 476-503. Saunders, Philadelphia.

AVERSION TO FEED ON CONSPECIFIC FLESH

273

Milgram, N. W., Krdmes, L., & Alloway, T. M. (1977). “Food Aversion Learning.” Plenum Press. New York. Moyer, K . E. (1976). “The Psychobiology of Aggression.” Harper and Row. New York. Myer, J. S. (1964). Stimulus control of mouse killing in rats. J . Cotnp. Physiol. Psvchol. 58, 112117. Norman. F. I . (1975). The murine rodents Rarti~sraftus, e.rulans and norvegicus as wain predators. Atoll R ~ s Bull. . 182, 1-13. O’Boyle. M. (1974). Rats and mice together: The predatory nature of the rat’s mouse-killing response. Psvrhol. Bull. 81, 261-289. Paul, L . , & Kupferschmidt, J . (1975). Killing of conspecific and mouse young by male rats. J . Comp. Physiol. Psychol. 88, 755-763. Pinel. J . P. J . , Gorzalka, B. B.. & Ladak, F. (1981). Cadaverine and putrescine initiate the burial of dead conspecifics by rats. Physiol. Behav. 27, 8 19-824. Polis, G. A. (19x1). The evolution and dynamics of intraspecific predation. Annu. Rev. Ecol. Svs. 12, 225-25 I . Potter, R. (1981). Modification of u “natural” aversion to cannibalism in inbread mice. Paper presented at the meeting of the Animal Behavior Society. Knoxville, Tennessee. Pribram, K . H., & Kruger, L. (1954). Functions of the “olfactory brain.” Ann. N . Y . Acud. Sci. 58, 109- 138. Price, B. I . ( 1978). Deniystification. enriddlement, and Aztec cannibalism: A materialist rejoinder to Harner. Am. Ethnol. 5 , 98-1 15. Rosenblatt. J . S . . Siegel, H. I . . & Mayer. A. D. (1979). Progress in the study of maternal behavior in the rat: hormonal, sensory, and developmental aspects. In “Advances in the Study of Behavior” ( J . S. Rosenblatt, R . A. Hinde. C. Beer, and M. C. Busnel, eds.), Vol. 10, pp. 225-331. Academic Press, New York. Roy, M. A. (1980). An introduction to the concept of species identity. In “Species Identity and Attachment” (M. A. Roy, ed.), pp. 1-22. Garland STPM, New York. Rozin, P. ( 1967). Specific avcrsions as a component of specific hungers. J . Comp. Phvsiol. Psychol. 64, 237-242. Rozin, P. (1976). The selection of food by rats, humans, and other animals. In “Advances in the Study of Behavior” (J. S . Rosenblatt, R. A. Hinde, E. Shaw, and C. Beer, eds.), Vol. 6, pp. 21-76. Academic Press, New York. Rozin, P. (1977). The significance of learning mechanisms in food selection: Some biology, psychology, and sociology of science. In “Learning Mechanisms in Food Selection” (L. M. Barker, M. R. Best. and M. Domjan, eds.), pp. 557-589. Baylor Univ. Press, Waco, Texas. Rozin, P., & Fallon, A. E. (1981). The acquisition of likes and dislikes for foods. In “Criteria of Food Acceptance: How Man Chooses What He Eats” (J. Solms and R. L. Hall, eds.). pp. 3548. Forster, Zurich. Sahlins, M. (1983). Raw women, cooked men, and other “great things” ofthe Fiji islands. In “The Ethnography of Cannibalism” (P. Brown and D. Tuzin, eds.), pp. 72-93. Society for Psychological Anthropology, Washington, D.C. Schiff, J . M. (1860). Der erste Hirnnerv ist der Geruchsnerv. Unters. Naturl. Mensch. Tier. 6 , 254267. Sclafani, A,, & Gorman. A. N. (1977). Effects of age, sex, and prior body weight on the development of dietary obesity in adult rats. Ph)~siol.Behav. 18, 1021-1026. Scott, J . P. (1958). “Aggression.” Univ. of Chicago Press, Chicago. Scott, J . P. (1967). The development of social motivation. In “Nebraska Symposium on Motivation 1967. Vol. XV” (D.Levine, ed.), pp. I 11-132. Univ. of Nebraska Press, Lincoln. Sherrington, C. S. (1900). Experiments on the value of vascular and visceral factors for the genesis of emotion. Pror. R . Soc. London 66, 390-403.

274

W . J . CARR AND DARLENE F. KENNEDY

Shenington, C. S. (1947). “The Integrative Action of the Nervous System,” 2nd ed. Yale Univ. Press, New Haven, Connecticut. Simon, E. L., & Gold, R. M. (1982). Effects of dietary fat upon hypothalamic hyperphagia and obesity in weanling rats. Nutr. Behav. 1, 79-88. Slonaker, I. R., &Card, T. A. (1922). The effect of a restricted diet. V. On mortality, cannibalism, and the sex ratio. Am. J . Physiol. 64, 297-310. Steiniger, F. (1950). Beitrage zur soziologie und sonstigen biologic der Wanderratte. Z . Tierpsychol. 7, 356-379. Sterling, M. H., DeMarco, A,, & Carr, W. J. (1983). The eflect of head-body contact on a natural food aversion in Norway rats. Paper presented at the meeting of the Eastern Psychological Association, Philadelphia, Pennsylvania. Stevens, J. D., Prince, M. D., & Cummings, J. F. (1977). Euthanasia chambers: Are yours safe and inexpensive? Lab Anim. 6(2), 39-42. Stevens, D. A,, & Gerzog-Thomas, D. A. (1977). Fright reactions in rats to conspecific tissue. Physiol. Behav. 18, 47-5 I . Thor, D. H., & Flannelly, K. J. (1976). Age of intruder and territorial-elicited aggression in male Long-Evans rats. Behav. Biol. 17, 237-241. Tousley, B., Schwartz, D., & Cam, W. J. (1974). Feeding responses of rats to mouse versus rat carcasses. Paper presented at the meeting of the Eastern Psychological Association, Philadelphia, Pennsylvania. vom Saal, F. S . , & Howard, L. S. (1982). The regulation of infanticide and parental behavior: Implications for reproductive success in male mice. Science 215, 1270- 1272. Wernicke, 0. (1937). Lebensmittelkunde, einschl. Fleishbeschau und Schlactofwesen. Berl. Tierarztl. Wochenschr. 45, 690-691 . Wilson, E. 0. (1971). Competitive and aggressive behavior. In “Man and Beast. Comparative Social Behavior” (J. F. Eisenberg and W. S. Dillon, eds.), pp. 183-190. Smithsonian Institution Press, Washington. Wilson, E. 0. (1975). “Sociobiology: The New Synthesis.” Harvard Univ. Press, Cambridge. Wuensch, K. L. (1983). Cross-species-rearing affects responses of wild house mice to contraspecific stimuli. Doctoral dissertation, Miami University, Miami, Florida. Dissertation Abstracts Internarional43, 23848-2385B. (University Microforms No. DA8227809). Young, P. T. (1936). “Motivation of Behavior.” Wiley, New York.

Index

A

C

Aggression, 38-44 Alarm calls, 127-134, 145, 233-234 Altricial birds, 105-152 acoustic sensitivity, 118-128 alarm calls, 127-134, 145 audition and defense behavior, 128- 134 auditory evoked potentials, 119-128 begging, 108-115, 140-141, 143, 146 behavior organization of, 138-148 cuckoos, 142-148 electromyographic (EMG) analysis, 1 I I 1 I5 feeding behavior, 108-1 15 great tits, 138-148 light sensitivity in, 116-118, 141, 148 nestling behavior, 108-1 15 passive-defense behavior, 115-1 16, 138, 141, 142, 145 pied flycatcher, 107- I18 redstarts , 140- 148 sensory factors in behavioral ontogeny, 105-152 visual mechanisms, 134-138 Amygdala, 24-26 Androgen-insensitivity syndrome, 27-28 Anger, 234-235 Animal vocal expression, 191-195 Assertiveness, 236 Associative fluency, 75-76 Auditory evoked potentials, recovery cycles of, 123-125

Caching, see food storage CAH, see Congenital adrenal hyperplasia Chase play, see Play, chase Component patterning of vocal expression, 215-237 cross-species universality, 225-237 predictions, 222-225 stimulus evaluation checks, 222-225 theory, 215-225 Congenital adrenal hyperplasia (CAH), 19-20, 27 Conspecific flesh, aversion to, see Food aversion Contentment, 229-231 Creative thinking, 75-76, 87 Cuculus canorus (cuckoo), 142- 148

D Danger, 232-233 Disgust, 231, 254-256 Displeasure, 231 Dominance, 5, 9, 11, 40-44

E ECP, see Play, energy cost of Emotion, 189-243 anger, 234-235 contentment, 229-23 I danger, 232-233 disgust, 231 displeasure, 23 1 facet description of, 201-204 fear, 232-233 frustration, 234 function of, 198-200

B Birds altricial, see Altricial birds food storage by, 153-188 Biting, 5 27 5

276

INDEX

Emotion (cont'd.) happiness, 229-23 I helplessness, 23 1-232 nature of, 198-200 ontogenetic continuity, 204-206 phylogenetic continuity, 204-206 psychobiological approach, 198-206 sadness, 23 1-232 transitions between, 235-237 types, 227-235 vocal expression of, 189-242 EP, see Evoked potentials Equifinality, 88-91 Evoked potentials (EP) auditory, 119-128 visual, 134-138 wulst, 134

larder hoards, 154 marsh tits, 160-163 memory and, 164-168 northwestern crows, 162, 176 nutcrackers, 161-162, 164, 165, 177-180 patterns, 158-160 pines, 154, 177-181 and recovery, 160-168 red fox, 162 scatter hoarding, 155, 158 social consequences of, 168- 17 I and social organization, 170- I7 I South Island robin, 155 spacing scattered caches, 171-173 squirrels, 180- 18 I timing of recovery, 175-176 variation in, 154-158 Frustration, 234-235

F Fear, 232-233 Firedula hypoleuca (pied flycatcher),

107-118 Food aversion, 245-275 dietary experience, 259-260 intraspecific predation, 262 motivational factors, 252-256 ontogeny, 256-261, 266-267 own-body experience, 258-259 phylogeny, 261-263, 268 response-competition model, 263-268 sensory factors, 25 1-252 social experience, 256-258 social facilitation, 260-261 Food storage, 153-188 acorn woodpeckers, 154- 155 black-capped chickadees, 162-163, 167 burrow hoarding, 155, 158 central place foraging, 173- 174 decision making, 171-176 and early breeding, 168-169, 181-182 eastern chipmunk, 155, 158 economics, 171-176 and emigration, 169- 170 and food plants, 176- 18 1 granaries, 154 inventory decisions, 174- I75 and irruption, 169-170 jays, 181

G Group integration, 42-43

H Happiness, 229-23 I Helplessness, 231-232 Hippocampus, 167 Hormones, 2, 17-28 activational effects, I8 adrenal, 23-24 corticosterone. 23 glucocorticoids, 23-24 gonadal steroids, 18-23 organization actions on CNS, 18 progesterone, 21 progestins, 21 testosterone, 18-23 Hostility-harshness rule, 193- 195 Hunger in mice, 253-254 in rats, 252-254

I Intraspecific predation, 262

277

INDEX

L Limbic systcm, 226 Melunerpes jormicivorus (acorn woodpecker), 154-155

M Memory features of, 164- 168 interocular transfer in birds, 163 neural mechanisms, 167-168 and recovery of stored food, 160-168 retention intervals. 165-166 serial position effects, 166 spatial in birds, 182 Mock combat, see Play-fighting

N Norway rats. 248-263

0 Oaks, 154, 181

P Purus mujor (great tit), 138- 148 Passive-defensive behavior, 115-1 16, 138, 141, 142, 145 Perroicu uustrulis (South Island robin), 155 Phoenicurus phvenirurus (redstart), 140- 148 Pines. 154, 177-181 adaptations of, 178-179 dispersal of, 179-180 Play, 1-103 acculturation function, 34, 37 adult, 84-85 approach-avoidance, 10 and associative fluency, 75-76 benefits of, 78-93 chase, 10, 16 as cognitive training, 66 correlational studies, 69-72 costs of, 79-82

and creative thinking, 75-76, 87 definition of, 61-66 developmental determinants, 92-93 developmental significance of, 32-34 dodging, 10 effects of, 85-88 energy cost of (ECP), 79-80 equifinality, 88-91 exercise hypothesis, 74, 92 experimental studies, 67-69 function of, 32-46, 59- I03 and group integration, 42-43 human, 75-78 immediate consequence of, 45-46 lability of, 82-84 in mammals, 4-14 methodological issues, 93-97 motor-learning function, 34, 40 as motor training, 66, 72 nonequivalence, 91 nonspecificity, 91-92 object, 75-76 optimal design studies, 72-78 and problem solving, 76, 87 role reversal in, 9, I 1 sex differences in, 1-58 determinants of, 4-32 neuroendocrine basis of, 17-28 and social behavior. 34-44 and social deprivation, 33, 44-45 and social development, 34-44 social influences in, 28-31 as socialization, 66 threshold effects, 92 Play-fighting, 3-10, 46, 63-64 and intraspecies aggression, 7- 10, 38-44, 65 facial expressions, 9 hormonal influences on, 18, 27-28 neural basis of, 24-27 sex differences in, 14-16 Play-mothering, 10-1 I , 16-17, 35-38, 46 Problem solving, 76, 87 Progesterone, 2 1

R Rattus norvegicus (Norway rats), 248-263 Rough-and-tumble play. see Play-fighting

278

INDEX

S

V

Sadness, 231-232 Scatter hoarding, 155, 158 SEC, see Stimulus evaluation checks Self-presentation, 210 Sex roles, socialization of, 1-58 Social communication, 38-39 Social deprivation, sex differences in response to, 33, 44-45 Social isolation, 67-68 Social play, see Play Species recognition, 249 Stimulus evaluation checks (SEC), 200-201, 222-225 coping potential, 224-225 g o a h e e d significance, 223-224 intrinsic pleasantness, 223, 236 norm conformity, 225 novelty, 222-223

Visual deprivation, 67-68 Vocal affect expression, component patterning theory of, 215-225 Vocal affect signaling, 189-243 Vocalization animal, 191-195 deception in, 212-215 emotional determinants of, 206-215 hostility-harshness rule, 193-195, 210 human, 195-198 modalities, 206-209 motivation-structural role, 193- 195 paralinguistic features, 209 pull effects, 209-2 12 push effects, 209-212 types, 206-209

W T Tamias striatus (eastern chipmunk), 155, 158 Testosterone, 18-23

Wrestling, 5

Contents of Previous Volumes Volume 1

Volume 3

Aspects of Stimulation and Organization in Approach/Withdrawal Processes Underlying Vertebrate Behavioral Development T. C . SCHNEIRLA

Behavioral Aspects of Homeostasis D. J . McFARLAND

Problems of Behavioral Studies in the Newborn Infant H. F. R. PRECHTL The Study of Visual Depth and Distance Perception in Animals RICHARD D. WALK Physiological and Psychological Aspects of Selective Perception GABRIEL HORN Current Problems in Bird Orientation KLAUS SCHMIDT-KOENIG

Individual Recognition of Voice in the Social Behavior of Birds C . G . BEER Ontogenetic and Phylogenetic Functions of the Parent-Offspring Relationship in Mammals LAWRENCE V. HARPER The Relationships between Mammalian Young and Conspecifics Other Than Mothers and Peers: A Review Y. SPENCER-BOOTH Tool-Using in Primates and Other Vertebrates JANE VAN LAWICK-GOODALL Aiithor Index-Subject Index

Habitat Selection in Birds P. H. KLOPFER and 1. P. HAILMAN Airthor Indo.r-Sitbject Index

Volume 2 Psychobiology of Sexual Behavior in the Guinea Pig WILLIAM C . YOUNG Brecding Behavior of the Blowfly V. G . DETHIER Sequences of Behavior R . A. HINDE and J . G . STEVENSON The Neurobehavioral Analysis of Limbic Forebrain Mechanisms: Revision and Progress Report KARL H. PRIRRAM

Volume 4 Constraints on Learning SARA J . SHEITLEWORIH Female Reproduction Cycles and Social Behavior in Primates T . E. ROWELL The Onset of Maternal Behavior in Rats, Hamsters, and Mice: A Selective Review ELAINE NOIROT Sexual and Other Long-Term Aspects of Imprinting in Birds and Other Species KLAUS IMMELMANN

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 Inde.r-Siibject Index

Author Index-Subject Index

219

280

CONTENTS OF PREVIOUS VOLUMES

Volume 5

Volume 7

Some Neuronal Mechanisms of 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

Functional Analysis of Masculine Copulatory Behavior in the Rat BENJAMIN D. SACHS and RONALD J . BARFIELD

The Ontogeny of Behavior in the Chick Embryo RONALD W. OPPENHEIM Prticesses Governing Behavioral States oi’ Readiness WALTER HEILIGENBERG Time-sharing as a Behavioral Phenomenon D. 1. McFARLAND

Sexual Reccptivity and Attractiveness in the Female Rhesus Monkey ERIC B. KEVERNE Prenatal Parent-Y oung I nteract icins i n B irds and Their Long-Term Effects MONICA IMPEKOVEN Life History of Male Japanc\e Monhcy\ YUKIMARU SUGIYAMA

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

Feeding Behavior of the Pigctin H PHILIP ZEICLER

Arrrhor /nde.r-Si~bjectIndex

Sltl,;cc~r llltll, \

Volume 6 Volume 8 Specificity and the Origins of Behavior P. P. G. BATESON The Selection of Foods by Rats. Humans. and Other Animals PAUL ROZIN Social Transmission of Acquired Behavior: A Discussion of Tradition and Social Learning in Vertebrates BENNETT G . GALEF, JR Care and Exploitation of Nonhuman Primate Infants by Conspecifics Other Than the Mother SARAH BLAFFER HRDY

Comparative Approaches t~ Social Bcliavlor i n Clo\ely Related Species ( i f Bird\ FRANK McKlNNEY The Influence of Daylength and Male Vocalizations on the Estrogen-Dcpcndent Rchavlor of Female Canaric\ and Budgerigar\. with Discussion ( 1 1 I h t a troni Othci- Spccic\ ROBERT A . HINDE and ELIZABETH STEt31. flthologicnl Aspect\ of Cheniical Coniniunic;ition in Ants BERT HoLLDOBLER

Hypothalamic Mechanisms of Sexual Behavior. with Special Reference to Bird.; J . B. HUTCHISON

Filial Rcsponsivene\\ to Olfiictory Cue\ in the Laboratory Rat MICHAEL LEON

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

A Conipari\on of the Propertie\ (it Different

Reinforcers IERRY A . HOGAN and T . J . ROPER

Sirhjrcr Imlr t

. Y r h ; ~ , l ~ rl l r ~ l l ~ t

CONTENTS OF PREVIOUS VOLUMES

Volume 9 Attachment as Related to Mother-Infant Interaction MARY D. SALTER AINSWORTH Feeding: An Ecological Approach F. REED HAINSWORTH and LARRY L. WOLF Progress and Prospects in Ring Dove Research: A Personal View MEI-FANG CHENC Sexual Selection and Its Component Parts. Soniatic end Genital Selection. as Illustrated hy Men and the Great Apes R. V. SHORT

28 1

JAY S . ROSENBLATT, HAROLD I . SIEGEL, and ANNE D. MAYER Sirhiect 1ride.r

Volume 11 Interrelationships among Ecological, Behavioral, and Neuroendocrine Processes in the Reproductive Cycle o f AIIOIIS cwolinetisis and Other Reptiles DAVID CREWS Endocrine and Sensory Regulation of Maternal Behavior in the Ewe PASCAL POINDRON and PIERRE LE NEINDRE

Socioccology of Five Sympatric Monkey Specie\ in the Kibale Fore\[. tiganda THOMAS T. STRUHSAKER m d LYSA LELAND

The Sociobiology of Pinnipeds PIERRE JOUVENTIN A N D A N D R E CORNET

Ontogenesis a n d Phylogenesis: Mutual C'onstr;iint\ GASTON RICHARD

Repertoires and Geographical Variation in Bird Song JOHN R . KREBS and DONALD E. KROODSMA

. ~ l t h / l ' ( ' // l l l / l ' \

Volume 10 I.earnin2. Change. and Evolution: An Enquiry i i i t t , h e Teleononiy of Learning ti C. PLOTKIN and I,'. J . ODLING-SMEE Social Bch;ivior. Group Structure. and the

Control ot Sex Reversal in Hermaphroditic Fi\h l)OClGLAS Y SHAPIRO Mamnialian Social Odors: A Critical Review RICHARD E. BROWN

Ikvelopment of Sound Communication in Mammals GUNTER EHRET Ontogeny and Phylogeny of Paradoxical Reward Effects ABRAM AMSEL and MARK STANTON Ingestional Aversion Learning: Unique and General Processes MICHAEL DOMJAN The Functional Organization of Phases of Memory Consolidation R. 1. ANDREW Irldc~r

Thc Development of Friendly Approach Behavior in the Cat. A Study o f Kitten-Mother Relations and the Cognitive Ilevelopmcnt of the Kitten front Birth to Eight Weeks MILDRED MOELK Progress in tlic Study of Matcrnal Behavior i n the Rat: Hormonal. Nonhornional. Sensory. and I)cvelopmental Aspects

Volume I2 Pavlovian Conditioning of Signal-Centered Action Patterns and Autonomic Behavior: A Biological Analysis of Function KAREN L . HOLLIS

282

CONTENTS OF PREVIOUS VOLUMES

Selective Costs and Benefits in the Evolution of Learning TIMOTHY D. JOHNSTON

Genes and Behavior: An Evolutionary Perspective ALBERT0 OLIVER10

Visceral-Somatic Integration in Behavior, Cognition, and ”Psychosomatic” Disease BARRY R. KOMISARUK

Suckling Isn’t Feeding. or Is I t ? A Search for Developmental Continuities W. G . HALL and CHRISTINA L. WILLIAMS

Language in the Great Apes: A Critical Review CAROLYN A. RISTAU and DONALD ROBBINS

Index

Volume 14

II7& X

Cooperation-A Biologist‘s Dilemma JERRAM L. BROWN

Group Mating in the Domestic Rat as a Context for Sexual Selection: Consequences for the Analysis of Sexual Behavior and Neuroendocrine Responses MARTHA K. MCCLINTOCK

Determinants of Infant Perception GERALD TERKEWITZ. DAVID J LEWKOWICZ. and JUDITH M . GARDNER

Plasticity and Adaptive Radiation of Dermupteran Parental Behavior: Results and Perspectives MICHEL VANCASSEL

Observations on the Evolution and Behavioral Significance of “Sexual Skin” in Female Primates A. F. DIXSON

Social Organization of Raiding and Eniigra tions in Army Ants HOWARD TOPOFF

Volume 13

Techniques for the Analysis of Social Structure in Animal Societies MARY CORLISS PEARL and STEVEN ROBERT SCHULMAN Thermal Constraints and Influences o n Communication DELBERT D. THIESSEN

Learning and Cognition in the Everyday Life of Human Infants HANUS PAPOUSEK and MECHTHILD

PAPOUSEK Ethology and Ecology of Sleep in Monkeys and Apes JAMES R. ANDERSON lndrx